New record of organic-walled, morphologically distinct microfossils from the late Paleoproterozoic Changcheng Group in the Yanshan Range, North China

Accepted Manuscript New record of organic-walled, morphologically distinct microfossils from the late Paleoproterozoic Changcheng Group in the Yanshan Range, North China Lanyun Miao, Małgorzata Moczydłowska, Shixing Zhu, Maoyan Zhu PII: DOI: Reference:

S0301-9268(18)30182-7 https://doi.org/10.1016/j.precamres.2018.11.019 PRECAM 5218

To appear in:

Precambrian Research

Received Date: Revised Date: Accepted Date:

8 April 2018 8 November 2018 27 November 2018

Please cite this article as: L. Miao, M. Moczydłowska, S. Zhu, M. Zhu, New record of organic-walled, morphologically distinct microfossils from the late Paleoproterozoic Changcheng Group in the Yanshan Range, North China, Precambrian Research (2018), doi: https://doi.org/10.1016/j.precamres.2018.11.019

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

New record of organic-walled, morphologically distinct microfossils from the late Paleoproterozoic Changcheng Group in the Yanshan Range, North China

Lanyun Miaoa, b, c, Małgorzata Moczydłowskac*, Shixing Zhud and Maoyan Zhua, b*

a

State Key Laboratory of Palaeobiology and Stratigraphy & Center for Excellence in

Life and Paleoenvironment, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, No. 39 East Beijing Road, Nanjing 210008, China b

College of Earth Sciences, University of Chinese Academy of Sciences, No. 19

Yuquan Road, Beijing 100049, China c

Department of Earth Sciences, Palaeobiology, Uppsala University, Villavägen 16, SE

752 36 Uppsala, Sweden d

Tianjin Institute of Geology and Mineral Resources, China Geological Survey,

Tianjin 300170, China

*Corresponding author: [email protected] & [email protected]

1

Abstract Eukaryotic life has likely existed since the late Paleoproterozoic, yet little is known about its early diversity and phylogenetic relationships. Organic-walled microfossils (OWMs) with conspicuous morphology provide a unique material to investigate the deep evolution of eukaryotic and prokaryotic microbial clades. Here we report a diverse assemblage of OWMs from the lower Changcheng Group (c. 1673–1638 Ma, Changzhougou and Chuanlinggou formations) in the Yanshan Range, North China, which consists of 15 species, including 2 that are newly described, and are attributed to eukaryotic and prokaryotic natural groups. The fossil assemblage is dominated by spheromorphs with less numerous process-bearing vesicles, as are colonial and filamentous forms. Among these, 6 morphologically complex taxa (Dictyosphaera, 2 species of Germinosphaera, Pterospermopsimorpha, Simia, and Valeria) are identified as unambiguous unicellular eukaryotes. Four species (Cucumiforma, Navifusa, Schizofusa and large Leiosphaeridia) with relatively simple morphology but having large size, thick wall, and some showing median-split excystment structures, are of probable eukaryotic affinity. However, various colonial microfossils could be either eukaryotes or prokaryotes. The new record of morphologically disparate OWMs represents one of the earliest occurrences of eukaryotes in both China and the world, and indicates that the eukaryotic life were already well established in the late Paleoproterozoic and were of moderate diversity, similar to that of the Mesoproterozoic. Keywords: organic-walled microfossil; eukaryote; Paleoproterozoic; Changcheng Group; North China

2

1. Introduction The emergence and early radiation of eukaryotes are of primary significance in the study of evolution of life on Earth and it is recognized that their advanced metabolic processes required relatively well-oxygenated milieus, which are directly related to global environmental development at the time (Lenton and Watson, 2011; Lyons et al., 2014; Planavsky et al., 2014). Molecular clock estimates for the age of the last eukaryotic common ancestor (LECA) range from c. 2300 Ma to c. 1000 Ma (Douzery et al., 2004; Hedges et al., 2004; Berney and Pawlowski, 2006; Parfrey et al., 2011; Eme et al., 2014) and largely depend on the molecular clock models and fossil calibrations used (Eme et al., 2014; Sánchez-Baracaldo et al., 2017). Paleontological evidence suggests that eukaryotes probably existed in the late Paleoproterozoic (Runnegar, 1994; Lamb et al., 2009; Moczydłowska et al., 2011; Butterfield, 2015). The most convincing candidates among those are the fossil taxa Valeria Jankauskas (=Yankauskas), 1982, emend. Nagovitsin, 2009, and Tappania Yin, 1997 (Yin, 1997; Prasad et al., 2005; Butterfield, 2015; Javaux and Lepot, 2018). Valeria is a unicellular microfossil with concentric striations, and has been recorded at c. 1650 Ma from the Mallapunyah Formation, northern Australia (Javaux et al., 2004) and herein from the lower Changcheng Group in North China at c. 1.67–1.64 Ga. Tappania is ornamented with tubular processes and neck-like extension, and occurs in c. 1631 Ma Deonar Formation, India (Ray et al., 2002; Prasad et al., 2005), and in the chronologically less well constrained Ruyang Group, North China at c. 1744–1411 Ma age (Yin, 1997; He et al., 2009; Hu et al., 2014; Lan et al., 2014; Agić et al., 2015, 2017). The coiled, ribbon-shaped macrofossil Grypania (Walcott) Walter, Oehler and Oehler, 1976 (age range from the c. 1891±3 Ma Negaunee Iron Formation, USA to c. 551 Ma Doushantuo Formation, China) (Han and Runnegar, 1992; Pietrzak-Renaud

3

and Davis, 2014; Wang et al., 2016), was originally considered to be a green alga in affinity (Runnegar, 1994) and subsequently treated as unidentified eukaryote (Knoll et al., 2006). However, recent study suggests a cyanobacterial origin of Grypania (Sharma and Shukla, 2009). Fossil diversity studies indicate that early eukaryotes reached a moderate diversity in the early Mesoproterozoic (Knoll et al., 2006; Cohen et al., 2015), which have been demonstrated by fossil assemblages such as the late Paleoproterozoic or early Mesoproterozoic Ruyang Group (Yin, 1997; Agić et al., 2017), the c. 1.58–1.45 Ga Chamberlain and Greyson formations of the lower Belt Supergroup, USA (Adam et al., 2016, 2017), the c. 1.5–1.4 Ga Roper Group, Australia (Peat et al., 1978; Javaux et al., 2001; Javaux and Knoll, 2017), the c. 1.5 Ga Kotuikan Formation of the Billyakh Group, Siberia (Vorob’eva et al., 2015), and the c. 1.4 Ga Kaltasy Formation, East European Platform (Sergeev et al., 2016). However, the exact extent of eukaryotic diversification prior to the Mesoproterozoic remains poorly known due to relatively sparse eukaryotic fossil records and is only approximately settled in the timescale. Sedimentary successions of the late Paleoproterozoic Changcheng Group in the Yanshan Range, North China (Fig. 1a–c) preserve relatively abundant OWMs and have been investigated for the last few decades (Xing and Liu, 1973; Sun, 2006). The earliest occurrence of OWMs in this group is known from the Changzhougou and Chuanlinggou formations (c. 1673–1638 Ma) (Fig. 1b), which were both previously reported having a relatively high taxonomic richness (e.g. Xing and Liu, 1973; Yan, 1982, 1985, 1991, 1995; Luo et al., 1985, 1986; Sun, 1989, 2006; Yan and Liu, 1993), and representing one of the earliest records of eukaryotes. However, the taxonomy of OWMs from these two formations was considered highly overestimated (Lamb et al.,

4

2009; Peng et al., 2009). Hence, the diversity of microfossils from the lower Changcheng Group remains unclear, especially the potential eukaryotic forms. To better evaluate the early diversity of eukaryotes and solve certain taxonomic problems that directly affect diversity estimates, we conducted a palynological study of the Changzhougou and Chuanlinggou formations from the Zhangjiakou area, Hebei Province, and the Tianjin area in the Yanshan Range. Here we report newly discovered taxa and provide substantial taxonomic revision of the previously reported microfossils from these two formations and tentatively infer their biological affiliations.

2. Geological background Geographically, the Yanshan Range extends over a large area of the northern Hebei Province, Beijing Municipalities, and northern Tianjin, as well as the western Liaoning Province. Tectonically, this range belongs to the middle part of the northern North China Craton (Fig. 1c), termed alternatively as the Yanliao rift, Yanliao aulacogen, or Yanliao Depression (Chen, 1983; Wang et al., 2015b; Ma et al., 2017). Proterozoic sedimentary cover within this area is widely exposed and was initially referred to as the “Sinian System” of China (Tien, 1923). This succession nonconformably overlies Archean or Paleoproterozoic metamorphosed rocks and consists predominantly of carbonates with a large suite of unaltered siliciclastic rocks and minor igneous rocks down section, all together reaching a thickness of nearly 10 km. This succession has been divided into 3 lithostratigraphic groups and 12 formations, comprising the following in ascending order: the Changcheng Group (Changzhougou, Chuanlinggou, Tuanshanzi, and Dahongyu formations), Jixian Group (Gaoyuzhuang, Yangzhuang, Wumishan, Hongshuizhuang, and Tieling formations), Xiamaling

5

Fig. 1. (a) Simplified geological map showing the distribution of Proterozoic successions in the studied area and sampled at the Pangjiapu and the Changzhoucun-Qingshanling section (CQ section). (b) Generalized stratigraphic column of the Proterozoic strata in the Yanshan Range, with geochronological data and important fossil occurrences. (c) Location of the North China Craton (NCC) and the studied area. Abbreviations in (b): Cam–Cambrian; CMs–carbonaceous macrofossils; NA– Neoarchean; Neo–Neoproterozoic; OWMs–organic walled microfossils; PMs–permineralized microfossils; Qb–Qingbaikou. Lithology and palaeontology data in (b) are based on Du, 1982; Duan et al., 1985; Sun, 2006; Zhu et al., 2016. Geochronological data are from Gao et al., 2008a, 2008b, 2009; He et al., 2011; Li et al., 2010, 2011, 2014; Peng et al., 2012; Wang et al., 2015b; Zhang et al., 2013; Zhang et al., 2015a, 2015b. The question mark in (b) represents the status of Xiamaling Formation

6

being removed from the Qingbaikou Group but hasn’t been classified into any lithological group (Zhu et al., 2012).

Formation, and the Qingbaikou Group (Longshan and Jing’eryu formations) (Fig. 1a– b) (Tian and Zhai, 1996; Wang et al., 1996). These rock units contain a wealth of paleontological records, including organic-walled microfossils preserved in shale or mudstone, permineralized microfossils in cherty nodules or bands, carbonaceous macrofossils, and stromatolites (Fig. 1b) (Xing and Liu, 1973; Zhu et al., 1994; Sun, 2006; Shi et al., 2017a, 2017b). Each of these biotas are valuable in unravelling the early evolution of life and, particularly, of eukaryotic grades in the Proterozoic. The Changzhougou Formation of the Changcheng Group is the lowermost unit, representing the initial deposition within the Yanshan rift basin. It is approximately 859 m thick in the stratotype section at the Jixian section in the northern Tianjin area and is subdivided into three members. The basal member consists of fluvial conglomerate and coarse sandstone; the middle member is mainly composed of littoral quartzite sandstone; and the top member is dominated by sandstone interbedded with siltstone and silty shale (Tian and Zhai, 1996; Zhu et al., 2005). This succession is overlain with a gradual transition by the Chuanlinggou Formation, which primarily consists of fine-grained siliciclastic rocks such as mudstone, shale, and silty shale that are intercalated with thin layers of sandstone and was deposited in an intertidal to subtidal paleoenvironment (Tian and Zhai, 1996; Zhu et al., 2005). Geochronology of Proterozoic successions in the Yanshan Range has been well-studied by means of radiometric dating of tuff beds, magmatic rocks, or detrital zircons (Fig. 1b). The Qian’xi Complex crystalline basement in the Jixian area has been dated to 2534±6 Ma by the zircon 207Pb-206Pb method (Gao et al., 2009). There is no direct dating of the Changzhougou Formation, but its initial depositional age is

7

estimated to be c. 1650 Ma, constrained by the U-Pb zircon age of granite dykes (1673±10 Ma) that were emplaced in the Archean basement and contemporaneously covered by the Changzhougou Formation in the Miyun area (north of Beijing) (Li et al., 2011, 2013). However, some older ages of similar dykes in the same area have also been acquired, dated at 1731±4 Ma (Peng et al., 2012) and 1685±15 Ma (Gao et al., 2008b). Diabase dykes and dioritic porphyrite dykes cross-cutting the lower part of the Chuanlinggou Formation yielded 207Pb-206Pb zircon ages of 1638±14 Ma and 1634±9 Ma (Gao et al., 2009; Zhang et al., 2013), providing the minimum depositional age for the Chuanlinggou Formation. These ages are consistent with the emplacement age of potassium-rich volcanic rocks (1637±15 Ma) in the upper Tuanshanzi Formation (Zhang et al., 2013). Therefore, the depositional age of the Changzhougou and Chuanlinggou formations is inferred to be c. 1673–1638 Ma.

3. Materials and methods Fine-grained siliciclastic rocks including silty shale, shaley siltstone, mudstone and shale, were collected for palynological study from two localities in the Yanshan Range, the Changzhoucun-Qingshanling and the Pangjiapu sections (Fig. 1a). The Changzhoucun-Qingshanling section (40°12ʹ07ʺ N; 117°29ʹ56ʺ E), is exposed along the road between the Changzhoucun and Qingshanling villages in the Jizhou District of the northern Tianjin area. This section was measured from the upper part of Member 3 of the Changzhougou Formation to the lower part of Member 1 of the Chuanlinggou Formation, reaching a total thickness of c. 220 m, and 26 samples were collected (Fig. 2e). The upper portion of the Changzhougou Formation exposed in this section is characterized by fining-upward sequences, consisting of pale grey, thick-

8

bedded quartz sandstone intercalated with a few layers of greyish green, shaley siltstone. Up section, gradually changes into dark, thin-bedded sandstone interbedded with dark, silty shale (c. 10 m thick) (Fig. 2e). The lowermost part of the Chuanlinggou Formation is dominated by dark, silty shale and mudstone (greyish yellow when weathered) intercalated with thin layers of sandstone, which becomes less common upward. Ripple marks have been observed, indicating a shallow water depositional environment. Due to transitional facies, the lithologic boundary between these two formations is not sharply defined, and we tentatively place this boundary at the level where shale and mudstone become dominant. The Pangjiapu section is in the western part of the Yanshan Range and is geographically located c. 5 km northeast of Pangjiapu town, Zhangjiakou area, Hebei Province (40°37ʹ53ʺ N; 115°27ʹ17ʺ E) (Fig. 1a). This section is at a road-cut, currently not well exposed and has not been measured due to covering by dense vegetation (Fig. 2b). The stratigraphic study was initially conducted by Du et al. (1979), who described the Changzhougou Formation as a c. 170 m thick succession consisting of two members. The lower member begins with granule-bearing coarse sandstone at the base, changing into thick-bedded sandstone interbedded with finegrained sandstone and silty shale, then upwards into predominantly black shale with a few layers of siltstone. The upper member consists predominantly of white, thickbedded sandstone with minor silty shale and siltstone. The Chuanlinggou Formation conformably overlies the Changzhougou Formation and consists mainly of black shale with three layers of ironstone (preserved in the form of oolites and stromatolites) at the bottom. Eight samples were collected from this formation (Fig. 2a–c). The stratigraphic correlation between the two studied sections is primarily based on lithology.

9

Fig. 2. (a) Stratigraphic column of the Changzhougou and Chuanlinggou formations at the Pangjiapu section with sampling records. (b) General view of the Pangjiapu section, showing the Changzhougou Formation consisting of the lower Member that is covered by vegetation and thick sandstone in the upper Member. (c) Outcrop of the lower Changzhougou Formation at Pangjiapu section (note, the red color of the succession is due to dusts of iron oxides from nearby iron ore mine). (d) Outcrop of lowermost Chuanlinggou Formation at Changzhoucun-Qingshanling section where microfossils appear in the succession. (e) Stratigraphic column of measured Changzhougou and Chuanlinggou formations at Changzhoucun-Qingshanling section with sampling records. Legend of lithology is in Fig. 1b. Fossiliferous samples are marked in red. Colour of lithology in the stratigraphic columns represents the weathered colour in outcrop.

A modified conventional palynological preparation technique was applied to extract microfossils from rock samples (Fig. 2a, e). Experimental maceration has been partly performed in the palynological laboratory in the Nanjing Institute of Geology 10

and Palaeontology, Chinese Academy of Sciences (NIGPAS), following the procedure described by Peng et al. (2009), and partly in the laboratory at the Department of Earth Sciences, Uppsala University. Furthermore, this technique was performed according to laboratory protocols reported by Vidal (1988). Organic residues after chemical dissolution of rock samples in hydrofluoric (HF) and hydrochloric (HCl) acids were rinsed in water to a chemically neutral state, and then sieved gently on nylon mesh (hole size 15 μm) to remove any tiny kerogen particles. Gravitational settling was used for the concentration of organic residues instead of centrifuging to avoid harsh agitation that might have caused damage to microfossils. No chemical oxidation treatment was applied. Permanent strew mounts were made using both epoxy resin and glycerol jelly as a mounting medium. Microscope slides were examined under a transmitted light microscope (TLM) (Nikon Eclipse Ni-U), and photomicrographs were taken by an attached camera (DSFi1c) using software NIS-Elements 40000 in NIGPAS. Scanning electron microscope (SEM) images of microfossils were acquired by the Zeiss Supra35-VP Genesis 4000 SEM microscope in the Evolutionary Biology Centre at Uppsala University. For SEM examination, microfossils were coated with 20 nm of a palladium-gold conducting medium for 90 seconds. Measurements of microfossils were performed on photomicrographs via software “tpsDig2w32” (http://life.bio.sunysb.edu/morph/).

11

Fig. 3. Taxonomic composition, fossil occurrence and the relative abundance of OWMs from the Changzhougou and Chuanlinggou formations in the Yanshan Range. The relative abundance of each species is estimated based on the entire microfossil record in both formations. Only fossiliferous samples are presented here whereas the total record is shown in Fig. 2a, e.

4. Results and discussion 4.1 Diversity of OWMs from the lower Changcheng Group Numerous and well-preserved OWMs are recovered from the Changzhougou Formation of the Pangjiapu section and the Chuanlinggou Formation of the Changzhoucun-Qingshanling section. They are classified into 15 species, including 2 newly erected species (Fig. 3), based on morphological features such as overall 12

vesicle shape, ornamentation, wall surface texture, and, if the microfossil was preserved in a colonial form, the arrangement pattern of constituent cells. Assemblages from these two formations have a similar taxonomic composition with 7 species in common, and are dominated by abundant spheromorphs with less abundantly occurring process-bearing vesicles and colonial and filamentous forms (Fig. 3). The Chuanlinggou assemblage shows relatively higher diversity (12 species) than the one from the Changzhougou assemblage (10 species) (Fig. 3). Among these OWMs, the following 6 taxa have been identified and interpreted as unicellular eukaryotes, namely Dictyosphaera macroreticulata (Fig. 4a–f), Germinosphaera alveolata sp. nov. (Fig. 5g–k), G. bispinosa (Fig. 5d–f), Pterospermopsimorpha insolita (Fig. 7a–d), Simia annulare (Fig. 7e–g) and Valeria lophostriata (Fig. 11). Their eukaryotic affinity has been inferred by a combination of characteristic features (not individual one), including vesicle body plan and wall ornamentation or sculpture, presence of internal body, excystment structure and large cell dimensions (Javaux et al., 2003; Knoll et al., 2006; Moczydłowska et al., 2011; Knoll, 2014; Butterfield, 2015). D. macroreticulata is ornamented with well-developed reticulate pattern of vesicle wall, with wall diameter up to 60 μm (Fig. 4a–f). Such complex sculpture and large size well suggest its eukaryotic nature. In addition, Dictyosphaera from the Ruyang Group and the Greyson Formation of the Belt Supergroup has been observed with excystment structures such as circular opening and medial split (Yin et al., 2005; Adam et al., 2017). The Ruyang Dictyosphaera also consistently displays a feature associated with an encysted stage and was interpreted as a microalga (Agić et al., 2015, 2017). Such excystment structures or encysted stage are not detected from present Dictyosphaera (Fig. 4a–f), nor in previous studies of Changcheng microfossils

13

(e.g. Xing and Liu, 1973; Xing et al., 1985; Luo et al., 1986; Sun, 1989). This may indicates a tophonomic bias that these specimens were preserved in an immature developmental stage before such structures would be formed during cyst maturation, or the reticulate sculpture of Dictyosphaera from these fossil assemblages are merely a result of convergent evolution. Germinosphaera, the only process-bearing OWMs currently found in the lower Changcheng Group, are spheroidal vesicles characterized by a robust tubular extension (Fig. 3). The present specimens show two different wall texture: smooth wall surface (G. bispinosa, Fig. 5d–f) and alveolar or reticulate sculpture (G. alveolata sp. nov., Fig. 5g–k). Germinosphaera has been compared to the germinating zoospores of extant xanthophyte Vaucheria (Butterfield et al., 1994) and blastospores of the extant fungal phylum Glomeromycota (Retallack, 2015; Loron and Moczydłowska, 2017). The morphological similarity among the fossil Germinosphaera and the two modern phylogenetically unrelated groups of algal Xanthophytes and fungal Glomeromycota, probably resulted from convergent evolution. Pterospermopsimorpha insolita has a body plan of sphere-in-sphere with overall diameter up to 70 μm (Fig. 7a–d). And similar microfossil Simia annulare is a discoidal or spheroidal vesicle composed of a single internal body and equatorial fringe (maximum diameter 100 μm, Fig. 7e–g). Both taxa have been compared to reproductive cysts (phycoma) of modern prasinophyte algae because of their striking similarity in morphological appearance, which is known exclusively within prasinophytes (Tappan, 1980; Inouye et al., 1990; Guy-Ohlson, 1996; Moczydłowska et al., 2011; Moczydłowska, 2015; Loron and Moczydłowska, 2017). Regardless of

14

the possible prasinophyte affinity of the Changcheng specimens, their eukaryotic affinity could be suggested by the complex morphology and large dimension. Valeria lophostriata, being an originally spheroidal vesicle (Fig. 11a–b) with delicate concentric striations on the inner wall surface (Fig. 11f1–f3), may also be preserved in a fusiform shape (Fig. 11c–d) and show a median split. The striation pattern of this species was suggested by biomechanical analysis as having a function to guide biologically programmed excystment via median split (Pang et al., 2015). It has been widely accepted as unicellular eukaryote, and interpreted as some protistangrade phytoplanktonic species (Butterfield and Chandler, 1992), a prasinophycean microalgae (Moczydłowska et al., 2011; Moczydłowska, 2015), or the resting or reproductive cysts of an un-identified microorganism in the eukaryotic domain (Javaux and Knoll, 2017). Apart from the above 6 morphologically complex species, smooth walled microfossils actually predominate the Changzhougou and Chuanlinggou assemblages, such as Leiosphaeridia spp. (Fig. 6) and Schizofusa sinica (Fig. 9). Together with Cucumiforma sp. (Fig. 4g–h) and Navifusa sp. (Fig. 4i–j), microfossils assigned to these 4 taxa may contain probable eukaryotic microorganisms, considering their large size and excystment structure shown by some of them. Leiosphaeridia, the most abundant form in the study, has a diameter range from a few microns to more than 200 microns and vesicle wall from tanslucent to opaque (Fig. 6), suggesting that the present Leiosphaeridia may contain more than one biological species. Distinguishing them and inferring their biological affinity are challenging due to lack of diagnostic morphological features. However, some large thin- and thick-walled specimens of Leiosphaeridia spp. (e.g. Fig. 6f, o–t) showing median split or large circular opening (Fig. 6t) are consistent with being cysts of single-celled eukaryotes. The excystment

15

structure by median split or round pylome, occasionally with additional structures (folds, flaps, lips), is a feature of reproductive cysts known in extant algae of various classes (Dale, 1983, 2001; Evitt, 1985; Margulis et al., 1989; Edwards, 1993; Raven et al., 2005; Graham et al., 2009) and suggests that these microfossils represent the developmental stage in a life cycle. Although some extant cyanobacteria can form circular envelopes also with excystment structure, the excystment structure of the latter is partial rupture (Waterbury and Stanier, 1978), not complete split. Schizofusa sinica is a fusiform microfossil (Fig. 9) and interpreted as curlingup valves of spheroidal or ellipsoidal vesicles (Peat et al., 1978; Zhang, 1986; Wang et al., 2015a). Recently, it has been compared morphologically with enrolled halfvesicles formed after splitting alongside the excystment structure by median split during the asexual reproduction of the extant marine coccoidal alga Nannochloropsis in Eustigmatophyte (Lamb et al., 2009, fig. 9). These authors have not inferred the same affinity for Schizofusa but certainly recognized it as a eukaryotic unicellular microorganism. Because, to our knowledge, the analogous morphology and the mode of shedding and enrolling the wall edges of the vesicle halves has not been observed in prokaryotes. The ellipsoids Cucumiforma sp. (length 58–107 μm, Fig. 4g–h) and Navifusa sp. (length 57–140 μm, Fig. 4i–j) are interpreted as possible early eukaryotes based on the large size and thick wall. Cucumiforma sp. has wall sculpture of longitudinally arranged wrinkles or thickenings and narrow ends. The cyst nature of this species is inferred because of the presence of an excystment structure in the form of a simple slit that is extended between the vesicle poles (Fig. 4g; see discussion under species Remarks). Navifusa sp. is identified by its regular elongated ellipsoidal outline with rounded poles and smooth wall surface. The biological affinity of Navifusa remains

16

uncertain due to the absence of more diagnostic features (such as surface ornamentation, wall ultrastructure) that would allow comparison with certain clades. It has also been considered to be a filamentous cyanobacterium in order Oscillatoriales (Jankauskas et al., 1989, and described under the junior synonym Brevitrichoides as recognized by Hoffman and Jackson, 1994), eukaryote without any placement in specific clades (Vorob’eva et al., 2015; Sergeev et al., 2016), or chlorophycean microalga for Phanerozoic records (Brenner and Foster, 1994; Fatka and Brocke, 2008). Other than unicellular microfossils, colonial forms are also common in the new fossil record (Fig. 3), represented by Eomicrocystis irregularis (Fig. 5a–c), Satka colonialica (Fig. 8), Symplassosphaeridium sp. (Fig. 10f–g) and Tetraphycus laminiformis sp. nov. (Fig. 10a–d). Their biological affiliation at the domain level could not be confidently determined due to lack of diagnostic features, although the cell constituents composing these cell aggregates are all relatively small, less than 10 μm. Previous studies have recognized some of these colonial taxa as cyanobacteria, such as Eomicrocystis (Golovenok and Belova, 1984; Hofmann and Jackson, 1994), Satka colonialica (details see the species remarks, Horodyski, 1980), and Tetraphycus (Oehler, 1978; Hofmann and Jackson, 1991). Oscillatoriopsis sp. (Fig. 10e) is the only filamentous form recovered in the new fossil materials. It has been morphologically compared to extant Oscillatoria and interpreted as having cyanobacterial affinity (Schopf, 1968; Butterfield et al., 1994).

4.2 Comparison with other fossil records and evolutionary significance Paleontological records suggest that eukaryotic organisms had developed a moderate diversity and evolved multicullularity with macroscopic size since the very

17

begining of the Mesoproterozoic Era (Knoll, 2014; Cohen and Macdonald, 2015; Zhu et al., 2016; Bengtson et al., 2017). However, eukaryotic fossil records earlier than Mesoproterozoic are sparse. Previouly reported putative eukartyoic fossils include spheroidal OWMs from c. 3.2 Ga Moodies Group, South Africa (Buick, 2010; Javaux et al., 2010; Knoll, 2014; Javaux and Lepot, 2018), graphite discs from c. 2.4 Ga Hutuo Group, North China (Sun and Zhu, 1998), centimeter-sized structures from c. 2.1 Ga Francevillian B Formation in Gabon (Albani et al., 2010), Grypania spiralis from c. 1.89 Ga Negaunee Iron Formation, USA (Han and Runnegar, 1992; Sharma and Shukla, 2009; Pietrzak-Renaud and Davis, 2014), Eosphaera from c.1.88 Ga Gunflint Iron Formation, Canada (Kaźmierczak, 1979; Brasier et al., 2015), and carbonaceous compressions from c. 1.63 Ga Tuanshanzi Formation, North China (Zhu and Chen, 1995; Knoll et al., 2006; Zhang et al., 2013). But due to the simple morphology and lack of diagnostic features, their eukaryotic affiliation still remains uncertain. Eukaryotic fossils with complex morphology began to appear in the late Paleoproterozoic (Butterfield, 2015; Javaux and Lepot, 2018), from stratigraphic units represented by the c. 1.67–1.6 Ga Changcheng Group, north of North China (Lamb et al., 2009; Peng et al., 2009; Shi et al., 2017a; and this study), the late Paleoproterozoic or early Mesoproterozoic Ruyang Group, south of North China (Yin et al., 2005; Hu et al., 2014; Lan et al., 2014; Agić et al., 2015, 2017), c. 1.65 Ga Mallapunyah Formation, Australia (Javaux et al., 2004), and the c. 1.63–1.6 Ga Semri Group, Vindhyan Supergroup, India (Rasmussen et al., 2002; Ray et al., 2002; Prasad et al., 2005; Sharma and Shukla, 2009). The Changzhougou and Chuanlinggou formations of the lower Changcheng Group as revealed by this study contain 6 diagnostically (Dictyosphaera, 2 species of

18

Germinosphaera, Pterospermopsimorpha, Simia and Valeria) and 4 probable eukaryotic species (Cucumiforma, large Leiosphaeridia, Navifusa and Schizofusa) (Fig. 3). In addition, uniseriate filament Qingshania Yan, 1989 observed in thin sections of Chuanlinggou Formation, was also identified as early eukaryote and being multicellular algae, because of its large size (cell length 83–487 μm; cell width 80– 251 μm) and characteristic cylindrical cell shape with varying width in a single filament (Yan, 1989). Macroscopic compressions from the Changzhougou Formation (Zhu et al., 2000), the upper Chuanlinggou Formation and the base of Tuanshanzi Formation (upper Changcheng Group) (Hofmann and Chen, 1980; Zhu and Chen, 1995) were initially interpreted as probable eukaryotes or multicellular algae, but their eukaryotic affinity has been questioned (Knoll et al., 2006; Lamb et al., 2007) and needs further study. Other eukaryotic fossils of Changcheng Group are from the Dahongyu Formation (top Changcheng Group) which contains permineralised microbiota characterized by cyanobacterial taxa but with few unambiguous eukaryotic taxa such as Dictyosphaera, Pterospermopsimorpha and one probable acanthomorphic form (Shi et al., 2017a). Compared with the Semri and Ruyang groups and other younger fossil records, process-bearing microfossils are very rare in the Changcheng Group. Currently only Germinosphaera and one acanthomorph from Dahongyu Formation (Shi et al., 2017a, fig. 11.14–11.15) have been discovered. In particular, the microfossil Tappania with irregularly distributed tubular processes, is a common fossil component in the Semri Group (Prasad et al., 2005; Sharma and Shukla, 2009), late Paleoproterozoic or early Mesoproterozoic Ruyang Group (Yin, 1997; Agić et al., 2017), and other Mesoproterozoic microbiotas (e.g. Javaux et al., 2001; Nagovitsin, 2009; Adam et al., 2017; Javaux and Knoll, 2017). It is absent in the entire Proterozoic sedimentary

19

sequences in the Yanshan Basin. The same is true for the Shuiyousphaeridium which is a very complex microfossil ornamented with reticulate surface sculpture and numerous hollow processes and commonly occurrs in the Ruyang Group (Yin, 1997; Agić et al., 2015, 2017) but also was found in the c. 1.6 Ga Chitrakit Formation of Semri Group (Bengtson et al, 2009; Singh and Shama, 2014). The Ruyang assemblage contains some common fossil taxa with the Changcheng Group (e.g. Valeria, Dictyosphaera, Pterospermopsimorpha and Simia), but differs in having diverse acanthomorphic forms (e.g. Tappania, Shuiyousphaeridium and Gigantosphaeridium) (Yin, 1997; Agić et al., 2017). Similarly, the Semri Group shares ceratin eukaryotic taxa (Dictyosphaera and Pterospermopsimorpha) with the Changcheng Group, but has distinctive fossil components such as Cymatiosphaeroides kullingii and reticulate Trachysphaeridium sp. (Prasad et al., 2005; Sharma and Shukla, 2009). Collectively, as suggested by previous studies and present study, the late Paleoproterozoic appears to be an important time interval for the evolution of ancestral eukaryotes in the aspects of the complexity of eukaryotic cells with sophisticated cytoskeleton, mitochondria and endomembrane, the emergence of crown-group eukaryotes, the precence of complex life cycle represented by excystment structures, and the multicellular development (Butterfield, 2015; Bengtson et al., 2017; Javaux and Lepot, 2018), with further evidences from the probable multicellular eukaryotic filament Qingshania from the c. 1.64 Ga Chuanlinggou Formation (Yan, 1989). In addition, the diverse unicellular eukaryotic microfossils recovered from the lower Changcheng Group and from other microbiotas discussed above, suggest that eukaryotes were already well established in the late Paleoproterozoic and had a moderate diversity similar to that of the Mesoproterozoic,

20

although the extent of diversity is relatively low compared to the Neoproterozoic (Knoll et al., 2006; Cohen and Macdonald, 2015; Riedman and Sader, 2018). The rapid radiation of early eukaryotic life in the late Paleoproterozoic, is possibly related to the changing environmental condition, such as the oxygenation of the atmosphere and oceans, although the Great Oxygenation Event occurred early in the Paleoproterozoic (Poulton et al., 2010; Lyons et al., 2014).

5. Conclusions The Yanshan Basin, North China, is one of the few geological sites in the world with well-preserved, unmetamorphosed Proterozoic sedimentary sequences and contains a rich paleontological record, which may provide valuable insights into the early evolution of eukaryotes. Palynological study of 34 shale samples collected from the late Paleoproterozoic Changzhougou and Chuanlinggou formations of the lower Changcheng Group in the Yanshan Basin, yielded numerous well-preserved OWMs. They are attributed to 14 genera and 15 species, including 2 new species (Germinosphaera alveolata sp. nov. and Tetraphycus laminiformis sp. nov.), and are predominately spheromorphs, with a few process-bearing, colonial and filamentous microfossils. Among these, 6 morphologically complex species are identified as eukaryotes and 4 species are interpreted as probable eukaryotic microorganisms. These unicellular eukaryotes show complex ornaments such as reticulate and alveolar sculpture, concentric striation, vesicle fringe and robust process, indicating the invention of novel morphologies, and a complex life cycle with reproductive encysted stage suggested by the presence of internal body and excystment structure. Most importantly, these new fossils, together with previously described microfossils

21

demonstrate an initial radiation with moderate diversity of eukaryotes that occurred in the late Paleoproterozoic. The Changzhougou and Chuanlinggou assemblages are among the earliest microbial records globally that contain well-preserved ancestral eukaryotes. This study provides new insights that enhance our understading of the early evolution of eukaryotic life, and records the oldest occurrences of complex microfossil Dictyosphaera, Germinosphaera, Pterospermopsimorpha, Simia and Valeria, thus establishing their first appearance datum (FAD) to at least c. 1650 Ma ago.

6. Systematic paleontology The collection of microscopic slides with all studied and illustrated microfossils is housed in the NIGPAS. The species systematic descriptions are arranged in alphabetic order regardless of their inferred biological affinities or informal morphological groupings. Microfossils illustrated in figures are referenced to the NIGPAS catalogue number with prefix PB, followed by microscopic slide number and the location of specimens on the microscopic slide provided by the England Finder coordinates. Magnified fragments of some specimens are referenced as the entire specimen and with the additional Arabic numbers 1, 2, etc., to demonstrate the details of morphology. Under the species “Occurrence and stratigraphic range”, the original information is cited according to regional stratigraphic units used by the authors. However, these units are recognized as coeval to certain Systems/Periods or Erathems/Eras of the Proterozoic. The Vendian regional chronostratigraphic unit in the Russian stratigraphic subdivision and broadly estimated to 650–545 Ma (Semikhatov et al., 1991; Loron and Moczydłowska, 2017) is correlated with the

22

Ediacaran System dated to 635–541 Ma in the ICS International Chronostratigraphic Chart 2017 (Cohen et al., 2013). The lower boundary of Vendian was defined at the begining of the Laplandian (equivalent to Marinoan) glaciation (Semikhatov et al., 2015), whereas the Ediacaran System begins right after the end of Marinoan glaciation (Knoll et al. 2004; Xiao et al., 2016). Consequently, the lower Vendian could be referred to the top Cryogenian System and the preceding Riphean of the Russian chronostratigraphic scheme is equivalent to the Meso-Neoproterozoic Erathems (Loron and Moczydłowska, 2017).

Organic-walled microfossils Genus Cucumiforma Mikhailova, 1986 Type species. – Cucumiforma vanavaria Mikhailova, 1986, emend. Mikhailova in Jankauskas et al., 1989, from the c. 675 Ma Kamovsk Formation at Vanavara locality in Krasnoyarsk region, Siberia (Mikhailova, 1986; Jankauskas et al., 1989; Schopf and Klein, 1992). Remarks. – Cucumiforma is diagnostic of an oval shaped vesicle having crumpling folds that are in the form of parallel strands or wrinkles and oriented from pole to pole (Jankauskas et al., 1989). It is morphologically similar to Valeria elongata Nagovitsin but the latter is characterised by its surface sculpture of meridional striations and occasional equidistant ring zones with thinner wall that are perpendicular to striations (Nagovitsin, 2009). The known records of Cucumiforma are restricted to the Neoproterozoic successions in the Russian Federation, including C. vanavaria in the lower Vendian of East Siberia (Golubkova et al., 2010), Cucumiforma sp. in the lower Vendian Vychegda Formation of the Timan Ridge and the Ediacaran Ura Formation of the Baikal-Patom Uplift (Vorob’eva et al., 2006; Sergeev et al., 2011).

23

Fig. 4. (a–f) Dictyosphaera macroreticulata; (g–h) Cucumiforma sp.; (i–j) Navifusa sp. (a) PB22490, chl-cq 0504, X/41/2-4; (b) PB22491, chl-cq 0509, R/21/4; (c) PB22492, chl-cq 0511, R/26; (d) PB22493, chl-cq 0509, X/30/4; (e) PB22494, chl-cq 0505, K/29/2; (f) PB22495, chl-cq 0506, H/37/4; (g) PB22496, chz-pj 0308, U/37/4; (h) PB22497, chz-pj 0301, R/37/4; (i) PB22498, chz-pj 0810, H/26; (j) PB22499, chz-pj 0312, K/15. All scale bars represent 20 μm. The double bar is for (a–i), and single bar is for (j).

Cucumiforma sp. Fig. 4g–h Material. – Six completely preserved specimens from Changzhougou Formation at Pangjiapu section. Description. – Ellipsoidal vesicle with narrow rounded ends and surface covered by longitudinally aligned, discontinuous, short and thin wrinkles that are relatively 24

distantly located. Number of wrinkles is variable among specimens, from several to dozens. Dimensions. – Vesicle long axis 58–107 μm (mean = 88.8 μm; N = 5), short axis 36– 64 μm (mean = 49.8 μm; N = 5); width of wrinkles c. 1 μm, length varying from several to tens of micrometres. Remarks. – The ellipsoidal shape and longitudinally arranged wrinkles of Changcheng specimens, suggest their assignment to genus Cucumiforma. They differ from the type species C. vanavaria by having shorter and discontinuous wrinkles which are further apart, being less numerous and also varying in number substantially. Given that the longitudinal wrinkles of Changcheng specimens may possibly be originated from taphonomy, and the difference from the C. vanavaria, we leave it as an open nomenclature. The excystment structure in a form of simple slit (Fig. 4g) is recognized because this feature is consistent morphologically along the vesicle long axis despite the partial damage on its left side. The regular and sharp in outline slit edges are not produced by a random breakage of the vesicle wall and, in contrast, taphonomically ruptured wall would result in disorderly located cracks or holes. Cucumiforma sp. differs from Navifusa sp. (Fig. 4i–j) by its narrow poles of the vesicle and wall sculpture of longitudinally thin wrinkles or striations. Navifusa has wide round vesicle ends and no sculpture. The compressional folds of its wall are wide, irregularily distributed alongside and perpendicularily across the vesicle (Fig. 4i–j). A similar specimen reported by Lamb et al. (2009) originally described as “an ellipsoidal specimen that appears to have striations along its longitudinal axis” also from Changzhougou Formation at Pangjiapu section (Lamb et al., 2009, p. 101, fig. 8A), is here considered as Cucumiforma sp.

25

Genus Dictyosphaera Xing and Liu, 1973 Type species. – Dictyosphaera macroreticulata Xing and Liu, 1973, from the late Paleoproterozoic Chuanlinggou Formation in Jixian County, Yanliao region, China (previously referenced to as lower Sinian Chuanlingkou Formation in Chih County, Yenliao region, China) (Xing and Liu, 1973). The holotype of D. macroreticulata was reported not available for re-examination and a lectotype was selected as one of the specimens originally assigned to D. sinica (Xing and Liu, 1973, pl. 1, fig. 18) from the same material as the holotype of D. macroreticulata (Agić et al., 2015). Remarks. – The genus Dictyosphaera was established by Xing and Liu (1973) to accommodate microfossils characterized by having reticulate sculpture on the vesicle surface. The vesicle reticulation pattern occurs also among other taxa, such as Dictyotidium Eisenack, 1955 and Retisphaeridium Staplin et al., 1965. However, Dictyosphaera differs from Dictyotidium by having much lower ridges that form the reticulate sculpture. In addition, Dictyosphaera from Ruyang Group, North China, shows a remarkable feature of composite vesicle wall that is two-layered and composed of individual elements, i.e. the polygonal platelets, of the internal layer interlocked within the reticulate mesh of the external wall layer (Agić et al., 2015). The record of Dictyosphaera in the Gouhou Formation from North China (Tang et al. 2015) extends the stratigraphic range of the genus substantially if the early Cambrian age of the formation is confirmed (He et al., 2017). This new evidence of long-ranging taxon would add to a growing record of microorganisms that survived the Cryogenian ice ages and the end-Ediacaran extinction that eliminated most of the Proterozoic biota (Moczydłowska, 2008a; Laflamme et al., 2013; Ye et al., 2015). Dictyosphaera has a wide palaeogeographic distribution and been reported

26

from China (Xing and Liu, 1973; Xiao et al., 1997; Yin et al., 2005; Tang et al., 2015), Australia (Javaux et al., 2001), India (Prasad et al., 2005), and USA (Adam et al., 2017). Dictyosphaera macroreticulata Xing and Liu, 1973 Fig. 4a–f Synonymy. For synonymy see Agić et al., 2015, and additionally: 1986 Dictyophaera rugosa Luo et Sun (in Litt.) – Luo et al., p. 470, pl. II, figs. 11–13. 1989 Dictyophaera fasciata (sp. nov.) – Sun, p. 241, pl. III, figs. 6–9. 1991 Dictyophaera sinica Sin et Liu – Yan, pl. I, figs. 18–19. 1993 Dictyophaera plicativa (Schep.) Yan – Yan and Liu, pl. I, fig. 3. 2017 Dictyosphaera macroreticulata – Adam et al., fig. 3A–C. 2017 Dictyosphaera macroreticulata Xing in Xing and Liu (1973) – Agić et al., p. 108–109, figs. 3A–F, 4A–C and 14G. 2017a Dictyosphaera macroreticulata Xing and Liu, 1973 – Shi et al., p. 388–389, fig. 10.10–10.11. Material. – More than 30 specimens in various states of preservation from Chuanlinggou Formation at Changzhoucun-Qingshanling section. Description. – Round to slightly elliptical vesicle (originally spheroidal) with reticulate sculpture on the vesicle surface. Reticulation is defined by narrow and low relief, solid ridges forming the polygonal mesh with its individual elements being subcircular in shape under light microscope. Vesicle wall is thin to thick but mostly thick, occasionally bearing compressional folds. In poorly-preserved specimens, the vesicle texture may appear like alveolar, with irregular individual mesh elements. Excystment structure not observed.

27

Dimensions. – Vesicle diameter 29–62 μm (mean = 45.6 μm; N = 39); diameter of polygonal mesh elements 1–3 μm (mean = 1.6 μm; N = 75), being uniform or slightly differing in size in one specimen. Remarks. – Dictyosphaera also commonly occurs in the Proterozoic Gaoshanhe Group and Ruyang Group in the southwest margin of North China Plate (Hu and Fu, 1982; Yan and Zhu, 1992; Yin et al., 2005). Agić et al. (2015) synonymized most of the species of Dictyosphaera erected from the Changcheng Group (D. sinica), Gaoshanhe Group (D. delicata and D. gyrorugosa) and Ruyang Group (D. incrassata) to the type species D. macroreticulata and argued that they overlapped both in morphology and size classes (Xing and Liu, 1973; Hu and Fu, 1982; Yan and Zhu, 1992). Other species of Dictyosphaera, such as D. rugosa (vesicle diameter 35–80 μm; mesh size 0.5–1.0 μm) was originally recorded similar to D. sinica but different in its thicker vesicle wall and clear compressional folds (Luo et al., 1986). D. fasciata (vesicle diameter 70–110 μm; mesh size 0.5–1.0 μm) was considered different from other species of Dictyosphaera by its wide compressional folds that were arranged along the marginal area of the vesicle (Sun, 1989). Given the fact that both D. rugosa and D. fasciata were established based on microfossils from the Chuanlinggou Formation in Kuancheng County of Hebei Province and their minor difference in compressional folds, we regard them synonymous with the type species D. macroreticulata. Another specimen recorded as D. plicativa (Schep.) by Yan and Liu (1993) that was also from the Chuanlinggou Formation but in Jixian area, here is reassigned as D. macroreticulata because there is no much difference between the illustrated specimen (Yan and Liu, 1993, pl. 1, fig. 3) and the type species. The lowest

28

occurrence of Dictyosphaera in the Yanshan Range is from the Changzhougou Formation in Kuancheng County (Luo et al., 1986). Dictyosphaera from Changcheng Group (29–62 μm) has smaller vesicle size range than that from the Ruyang Group (22–286 μm) (Agić et al., 2015) but overlap. It shows similar reticulate sculpture of vesicle wall under TLM (Fig. 4a1, b1, c1) with Ruyang Dictyosphaera. But there is no SEM study of Changcheng Dictyosphaera to reveal the wall reticulate pattern, if it is the same with Ruyang Dictyosphaera whose vesicle wall comprises two layers: the external layer with a reticulate surface and the internal wall layer formed by interlocked polygonal platelets and corresponding to the polygonal pattern of the wall surface (Agić et al., 2015, 2017). Occurrence and stratigraphic range. – D. macroreticulata has been recorded in the late Paleoproterozoic Changzhougou and Chuanlinggou formations in Yanshan Range, North China (Xing and Liu, 1973; Luo et al., 1986; Sun, 1989); late Paleoproterozoic or early Mesoproterozoic Gaoshanhe and Ruyang groups in southwest of North China (Hu and Fu, 1982; Yin et al., 2005; Agić et al., 2015, 2017); c. 1.49 Ga Roper Group in Northern Australia (Javaux and Knoll, 2017); c. 1.47–1.45 Ga Greyson Formation in USA (Adam et al., 2017).

Genus Eomicrocystis Golovenok and Belova, 1984 Type species. – Eomicrocystis irregularis Golovenok (=Golovenoc) and Belova, 1984, from the c. 1.5 Ga Kotuykan (= Kotuikan) Formation, Billyakh Group, Kotuykan River, Anabar Uplift, Northern Siberia (Golovenok and Belova, 1984). Remarks. – Eomicrocystis was defined as small uniform cells forming threedimensional colonies based on permineralized microfossils from chert samples. Cells of Eomicrocystis are mostly spheroidal with smooth surface and without inclusions.

29

No sheath presents encompassing the colony and individual cells (Golovenok and Belova, 1984). As colonial microfossils, it appears similar to other form genera such as Coniunctiophycus Zhang, 1981, Myxococcoides Schopf, 1968, Symplassosphaeridium Timofeev, 1959, ex Timofeev, 1969, and Synsphaeridium Eisenack, 1965. However, Coniunctiophycus was defined as spheroidal or ellipsoidal colonies formed by subpolyhedral or spheroidal cells (diameter 1-7 μm) that were commonly with dark inclusion (Zhang et al., 1981), whereas colonies of Eomicrocystis could be irregular, spheroidal, ellipsoidal or botryoidal in outline (Golovenok and Belova, 1984). Myxococcoides is diagnostic of spherical to ellipsoidal cells that appear solitary or clumped in colonies. Individual cells of Myxococcoides also have no encompassing sheaths but commonly embedded in welldeveloped amorphous organic matrix (Schopf, 1968). It is often recognised as threedimensionally preserved microfossils in chert nodules, chert beds, or silicified stromatolites such as Bitter Spring Formation (Schopf, 1968), Balbirini Dolomite (Oehler, 1978), Amelia Dolomite (Muir, 1976), and Dismal Lakes Group (Horodyski and Donaldson, 1980). Symplassosphaeridium was erected as globular clusters of spherical vesicles (Timofeev, 1959), which differs from other colonial forms by its well-defined colonial outline. And Synsphaeridium differs by its irregular twodimensional aggregates of organic-walled hollow spheres that are interconnected but do not form globular clusters (Eisenack, 1965). It resembles Eomicrocystis morphologically when the latter is preserved as organic walled microfossils, but Eomicrocystis has relatively much smaller cell sizes, usually less than 10 microns (e.g. Golovenok and Belova, 1984, 1986; Jankauskas et al., 1989; Hofmann and Jackson, 1994; Cotter, 1997, 1999; Beghin et al., 2017; Javaux and Knoll, 2017).

30

Fig. 5. (a–c) Eomicrocystis irregularis; (d–f) Germinosphaera bispinosa; (g–k) Germinosphaera alveolata sp. nov., showing the distinct alveolar, or irregular meshwork of wall surface texture and a single robust hollow process which has a broad base and slightly tapers towards the end. (a) PB22500, chl-cq 0515, C/38/2; (b) PB22501, chl-cq 0601, U/12/4; (c) PB22502, chl-cq 0506, D/31/1-2; (d) PB22503, chl-cq 0502, W/29/3-4; (e) PB22504, chl-cq 0514, Y/33/1-2; (f) PB22505, chl-cq 0506, K/24/4; (g) Holotype, PB22506, chl-cq 0501, Q/36; (h) Paratype, PB22507, chl-cq 0504, Z/41; (i) Paratype, PB22508, chl-cq 0506, Q/32; (j) PB22509, chl-cq 0602, W/28; (k) PB22510, chl-cq 0517, N/39.

Eomycrocystis irregularis Golovenok and Belova, 1984 Fig. 5a–c

31

Synonymy. 1973 Margominuscula antiqua Naum. – Xing and Liu, p. 12, pl. I, fig. 8. 1984 Eomicrocystis irregularis V. Golovenok et M. Belova, sp. nov. – Golovenok and Belova, 1984, p. 29, pl. II, figs. 16–17. 1985 Leiominuscula aff. minuta Naum. – Xing et al., pl. 1, fig. 9. 1985 Leiominuscula pellucentis Sin et Liu – Xing et al., pl. 1, fig.13. 1985 Margominuscula antiqua Naum. – Xing et al., pl. 1, fig. 14. 1985 Trachyminuscula microrugosa Naum. – Xing et al., p. 49, pl. 1, fig. 17. 1985 Trachyminuscula sp. – Xing et al., pl. 1, figs. 15–16, 33. 1989 Eomicrocystis irregularis Golovenok and Belova, 1984 – Jankauskas et al., p. 91, pl. XIX, fig. 16. 1995 Coniunctiophycus aff. gaoyuzhuangense Zhang – Yan, pl. IV, fig. 3. 2017 Eomicrocystis irregularis – Beghin et al., p. 69, pl. 1, fig. m. Material. – 11 well preserved specimens from the Changzhougou Formation at Pangjiapu section and Chuanlinggou Formation at Changzhougcun-Qingshanling section. Description. – Loosely or tightly packed aggregates of cells in overall irregular shape consisting of a few to tens of spheroidal to ovoidal small cells. Individual cells are translucent, thin- to thick-walled with smooth wall surface and uniform or slightly varying in size. No surrounding organic matrix or sheath are observed. Dimensions. – Aggregate overall diameter 15–70 μm; cell diameter 3–8 μm (mean = 5.4 μm; N = 84). Remarks. – The small cell size, smooth-walled surface, irregular shape of aggregates, and the feature of no sheath and no encompassing organic matrix observed of specimens here warrant the assignment to Eomicrocystis rather than Myxococcoides, 32

Symplassosphaeridium and Synsphaeridium. They are further identified as Eomicrocystis irregularis based on the irregular outline of these aggregates, because E. irregularis differs from other species of Eomicrocystis by its irregular colonial outline. E. elegans is characteristic of complex botryoidal, compound colonies (Golovenok and Belova, 1984). E. minima differs in its considerably smaller cell size (0.6–2.0 μm) (Golovenok and Belova, 1986). And E. malgica is different from E. irregularis in the regular colonial shape as spheroidal colonies and somewhat smaller cell size (Golovenok and Belova, 1986). Similar aggregates from the Chuanlinggou Formation in Jixian area, reported under different names such as Leiominuscula aff. minuta, Leiominuscula pellucentis, Margominuscula antiqua, Trachyminuscula microrugosa and Trachyminuscula sp., (Xing and Liu, 1973; Xing et al., 1985), all consist of small vesicles (4–8 μm in diameter) and have no regular shape of aggregates. These specimens are reassigned as Eomicrocystis irregularis. The same is true for another specimen from Chuanlinggou Formation assigned as Coniunctiophycus aff. gaoyuzhuangense (Yan, 1995, pl. IV, fig. 3). Because Conjunctiophycus is diagnostic of spheroidal to ellipsoidal colonies whose cell consitituents often have spheroidal or ellipsoidal dark inclusions (Zhang, 1981). Occurrence and stratigraphic range. – Late Paleoproterozoic Chuanlinggou Formation from Yanshan Range, North China (Xing and Liu, 1973; Xing et al., 1985; Yan, 1995); c. 1.5 Ga Kotuikan Formation in Anabar Uplift, Siberia (Golovenok and Belova, 1984; Jankauskas et al., 1989); late Mesoproterozoic – early Neoproterozoic Atar/El Mreïti Group in Mauritania, northwestern Africa (Beghin et al., 2017).

33

Genus Germinosphaera Mikhailova, 1986, emend. Butterfield, Knoll and Swett, 1994, new emendation Type species. – Germinosphaera bispinosa Mikhailova, 1986, emend. Butterfield, Knoll and Swett, 1994, from Upper Riphean Dashkin Formation at River Uderei section in Krasnoyarsk region, Siberia (Mikhailova, 1986; Butterfield et al., 1994). Emended diagnosis. – Vesicle spheroidal, teardrop-shaped to slightly irregular in outline, having psilate or low relief sculptured alveolar wall surface and bearing a single to multiple processes. Processes are simple tubular or occasionally branching and open-ended. Processes are distributed irregularily on the vesicle wall, if multiple, and may be predominantly, but not exclusively, distributed in the equatorial plane of the vesicle. Remarks. – We revise the species of the genus Germinosphaera, which had been diagnosed as having psilate or shagrinate wall surface, and suggest that the wall surface described as shagrinate is a taphonomic alteration and not morphological feature. Therefore, all previously described species appear to have psilate wall. The vesicle diameter varies insignificantly between described species or overlaps, in total ranging 13–125 μm. The processes are simple tubular with the exception of occasionally branching in G. fibrilla and their width is 2–14 μm and length 2–13 μm. The process length remains uncertain because processes seem to be broken apart, often shortly above the vesicle wall, and their terminations are not observed. The number of processes varies from 1 to 7 and has been defined for discrete species as 1 (G. tadasii,in Jankauskas et al., 1989), 1–4 (G. bispinosa, G. fibrilla), and 2–7 (G. jankauskasii) (Butterfield et al., 1994). This low variability observed between the species and within discrete species is a non-conclusive feature. By comparison with extant xanthophyte alga Vaucheria, G. fibrilla and G. jankauskasii were suggested as

34

germinating organisms based on their indeterminate number and distribution of processes showing developmental or growing stages (Butterfield et al., 1994), and these would further preclude from recognizing the species. The process distribution, if multiple, is irregular on the entire spheroidal vesicle or, as ascribed to G. fibrilla, predominantly in the equatorial plane of the vesicle. The feature of equatorial distribution of processes has been thought to suggest the benthic mode of microorganism life (Butterfield et al., 1994). It may not be the case because even in G. fibrilla (Butterfield et al., 1994, fig. 17D, G) processes occur also on the upper vesicle surface not only in its outline. We consider all these species to be synonymous with the type species G. bispinosa as emended by Butterfield et al. (1994) (see section Remarks under this species). Thus, Germinosphaera currently has three species, namely G. bispinosa, G. guttaformis Mikhailova (in Jankauskas et al., 1989), and one new species G. alveolata sp. nov. described below. Germinosphaera morphologically resembles Caudosphaera Hermann and Timofeev (in Jankauskas et al., 1989), Clavitrichoides Mikhailova (in Jankauskas et al., 1989), and Jacutianema Timofeev and Hermann, 1979. But Caudosphaera is diagnostic of a single cell with a long tail-like outgrowth or extension (Jankauskas et al., 1989). It differs from other similar taxa by its tail-like extension which is pleated, tapering towards the end, and sometimes even dividing into thin filaments (Jankauskas et al., 1989). Moreover, it is not fully known that if the tail-like extension communicates with the vesicle cavity, as there is no such description when the authors erected this genus, neither can it be discerned clearly from the illustrated specimens by Hermann and Timofeev (in Jankauskas et al., 1989). Clavitrichoides was originally described as single trichome with one end broadened, in which the trichome is slightly thinner than the broadened end (Jankauskas et al., 1989), whereas Germinosphaera

35

has much narrower processes relative to its vesicle (Butterfield et al., 1994). Jacutianema, when preserved as a spheroidal vesicle with a filamentous extension, it bears no much difference from Germinosphaera. But Jacutianema is diagnostic of isolated or connected series of botuliform cells with various attachments or ornaments such as subterminal filamentous extensions, variably shaped vesicles, outer filamentous envelope, condensed cytoplasm, or subterminal pore (Butterfield, 2004). Germinosphaera alveolata sp. nov. Fig. 5g–k Holotype. – Specimen illustrated in Fig. 5g, PB22506, ChL-CQ 0501, Q/36, from the lowermost Chuanlinggou Formation, Changcheng Group, late Paleoproterozoic in age. Paratype. – Specimens illustrated in Fig. 5h, PB22507, ChL-CQ 0504, Z/41, and in Fig. 5i, PB22508, ChL-CQ 0506, Q/32, all from the same material as the holotype. Derivation of name. – From the Latin alveolatus – meaning “alveolar” and referring to the vesicle surface texture. Locus typicus. – North China, Tianjin area, Jizhou District, ChangzhoucunQingshanling section. Stratum typicum. – Dark grey mudstone interbedded with thin-bedded fine sandstone of the Chuanlinggou Formation. Material. – 22 specimens in various states of preservation from Chuanlinggou Formation at Changzhoucun-Qingshanling section Diagnosis. – Spheroidal to slightly elongate vesicle with a single robust process extending gradually from the vesicle wall. Vesicle and process surface is alveolar and formed by irregular reticulate sculpture with individual alveoli sub-circular or irregular in shape. Process is hollow, having a broad base, slightly tapering towards the end, and communicating freely with the vesicle cavity.

36

Dimensions. – Vesicle diameter 25–57μm (mean = 42.1 μm; N = 22); width of process base 5–17 (mean = 10.1 μm; N = 22); length of process unknown due to preservation. Remarks. – The aveoloar wall texture of the new species (Fig. 5g1) is interpreted as authentic feature rather than a taphonomic artefact. It is a consistent morphological feature observed in more than 20 specimens and renders the new species distinct from other species of Germinosphaera, which are revised here as having psilate wall surface and synonymized with the type species G. bispinosa (see under this species Remarks). Germinosphaera bispinosa Mikhailova, 1986, emend. Butterfield, Knoll and Swett, 1994 Fig. 5d–f Synonymy. For synonymy see Loron and Moczydłowska, 2017, and additionally: 1989 Germinosphaera bispinosa Mikhailova, 1986 – Mikhailova in Jankauskas et al., p. 142, pl. XLVII, fig. 2. 1989 Germinosphaera tadasii A. Weiss, sp. nov. – Weiss in Jankauskas et al., p. 143, pl. XLVII, figs. 3–5. 1989 Germinosphaera unispinosa Mikhailova, 1986 – Mikhailova in Jankauskas et al., p. 143, pl. XLVII, fig. 1. 1993 Gemmispora rudis Yan – Yan, pl. I, figs. 6–7. 1994 Germinosphaera fibrilla (Ouyang, Yin & Li, 1974) Butterfield, n. comb. – Butterfield et al., p.38, fig. 17A-H. 1994 Germinosphaera jankauskasii Butterfield, n. sp. – Butterfield et al., p.38, 40, fig. 16A-C.

37

2005 Germinosphaera bispinosa Jankauskas, 1989 – Prasad et al., p. 44, 46, pl. 11, fig. 3. 2005 Germinosphaera unispinosa Jankauskas, 1989 – Prasad et al., p. 44, pl. 11, fig. 2. 2016 Germinosphaera bispinosa Mikhailova, 1986 – Baludikay et al., fig. 6A–C. 2017 Germinosphaera bispinosa Mikhailova, 1986, emend. Butterfield, Knoll & Swett, 1994 – Loron and Moczydłowska, p. 24–25, pl. 1, fig. 3.Material. – 23 specimens in various states of preservation from Chuanlinggou Formation at Changzhoucun-Qingshanling section. Emended diagnosis: Spheroidal to slightly elongate or irregular vesicle with one to multiple tubular processes. Vesicle wall psilate. Processes may arranged irregularly or equatorially on the vesicle wall when multiple. Description. – Spheroidal or slightly elongate vesicle bearing one robust, tubular, hollow process. Vesicle wall is thick with psilate surface or slightly corroded. Process is short, nearly uniform in width, extending gradually from the vesicle wall and communicating freely with the vesicle cavity. Dimensions. – Vesicle diameter 30–58 μm (mean = 39.7 μm; N = 23); process width 5–14 μm (mean = 8.4 μm; N = 22); process length usually less than 13 μm due to preservation. Remarks. – Germinosphaera bispinosa was emended by Butterfield et al. (1994) to include species of Germinosphaera distinguished previously by having 1 or 2 processes (G. unispinosa and G. bispinosa) and the newly observed specimens having 1–4 processes, psilate wall, vesicle diameter 13–35 μm, and process width 2.5–3.5 μm. Loron and Moczydłowska (2017) attributed specimens with a larger diameter of the

38

vesicle and a single process to G. bispinosa according to the emended genus diagnosis but argued that the strict limit of vesicle diameter is not a diagnostic feature. Another species, Germinosphaera tadasii A. Weiss 1989 (in Jankauskas et al., 1989) (=Sivaglikania tadasii, in Schopf and Klein, 1992) was described as a spherical vesicle with a hollow process, 60–80 μm in diameter, and having psilate or shagrinate wall surface (Jankauskas et al., 1989). There is no much difference in the overall vesicle morphology of this species and of G. bispinosa, whereas the shagrinate surface ascribed as diagnostic feature alongside smooth in G. tadasii is inconsistent morphologically feature and the result of taphonomic degradation. The vesicle size alone is not a diagnostic feature, and therefore we consider G. tadasii to be a junior synonym of G. bispinosa due to its psilate wall surface. G. jankauskasii has been described as a vesicle having shagrinate wall, 45–90 μm in diameter, and bearing 2–7 processes randomely distributed (Butterfield et al., 1994). In the type species and other illustrated specimens the wall surface appears to be a corroded and with breakage holes and coalesced organic debris attached instead of the genuine wall texture. This renders G. jankauskasii indistinguishable from G. bispinosa and G. fibrilla having psilate wall. The diagnoses of two latter species stated psilate vesicle surface and insignificantly different vesicle diameter ranges, and the number of processes mentioned in species descriptions as 1–4 in both species. In fact, there are no objective morphological features or clear size classes to distinguish described species, all having psilate wall and variable number of processes from 1 to 7. The distribution of processes is irregular on the entire vesicle. Following these observations, the type species G. bispinosa emended by Butterfield et al., 1994, may include morphological variants with single to multiple tubular and occasionally

39

branching processes and the vesicle diameter ranging 13–125 μm. All these species are considered to represent developmental stages and are synonymous. The morphological variants of Germinosphaera have been suggested to be germinating propagules from the vegetative structure comparable to the extant xanthophyte alga Vaucheria (Butterfield et al., 1994). Specimens of G. bispinosa in present material have a single process (conversely to the species name), smooth-wall (Fig. 5d–f) and diameter 30–58 μm. This species recorded from the Tonian Visingsö Group in Sweden has diameter 38–40 μm (Loron and Moczydłowska, 2017, pl. 1, fig. 3), and from the Mbuji-Mayi Supergroup in Democratic Republic of Congo diameter larger than 100 μm (Baludikay et al., 2016, fig. 6A–C). These records show that the species, including synonymized here species, has greater total vesicle diameter ranging 13–125 μm. Germinosphaera from Changcheng Group was first reported as G. guttaformis (Yan, 1995, pl. IV, fig. 11), G. aff. gutaformis (Yan, 1995, pl. I, fig. 20) and G. aff. unispinosa (Yan, 1995, pl. I, fig. 20). But the specimens illustrated were not well preserved and highly corroded. Another specimen named Gemmispora rudis shows a dark round vesicle with a robust process, also from Chuanlinggou Formation in Jixan area (Yan and Liu, 1993, pl. 1, fig. 6). The wall surface of this specimen is assumed smooth or slightly corroded as it looks uniform in dark grey color except some large holes of it. Thus it is reassigned as G. bispinosa. Occurrence and stratigraphic range. – Lower Riphean Omakhta Formation and c. 1.0 Ga Neryuen Formation in Uchur-Maya region (Jankauskas et al., 1989; Semikhatov et al., 2000), c. 850 Ma Miroedikha Formation in Turukhansk region (Timofeev et al., 1976; Mendelson and Schopf, 1992), c. 750 Ma Dashkin Formation and c. 675 Ma Kamovsk Formation in Krasnoyarsk region (Mikhailova, 1986;

40

Jankauskas et al., 1989; Mendelson and Schopf, 1992; Schopf and Klein, 1992), Ediacaran Vychegda Formation in Timan Ridge, Russian Federation (Vorob’eva et al., 2009); Meso-Neoproterozoic Mbuji-Mayi Supergroup in Democratic Republic of Congo (Baludikay et al., 2016); late Paleoproterozoic Chuanlinggou Formation, Neoproterozoic Dongjia Formation in North China (Yin and Guan, 1999); c. 788–740 Ma Visingsö Group in Sweden (Loron and Moczydłowska, 2017; Moczydłowska et al., 2017); c. 750–700 Ma Svanbergfjellet Formation in Spitsbergen (Butterfield et al., 1994); Ediacaran Sirbu Shale of Bnander Group in India (Prasad et al., 2005).

Genus Leiosphaeridia Eisenack, 1958, emend. Downie and Sarjeant, 1963, emend. Turner, 1984 Type species. – Leiosphaeridia baltica Eisenack, 1958, from Ashgill Stage strata (late Ordovician) in Estonia (Eisenack, 1958). Synonymy. 1973 Pseudozonosphaera Sin et Liu gen. n. – Xing and Liu, p. 19, 56. 1982 Pseudofavososphaera Xing gen. n. – Xing and Liu, pl. III, fig. 13 (nomen nodum). 1985 Pseudofavososphaera Xing, 1982 – Xing et al., p. 56. 1995 Schizospora gen. n. – Yan, p. 364, 369–370. Remarks. – The form genus Leiosphaeridia is characterized by its spheroidal vesicle with psilate wall or perhaps having shagrinate or slightly granular microsculpture on the wall surface, if not being a taphonomic artefact (see recent discussion by Loron and Moczydłowska, 2017). Because of this morphological simplicity that may be the result of convergent evolution between unrelated biota and the ubiquitous presence of spheroidal microfossils throughout the geological ages, Leiosphaeridia is inferred to

41

be polyphyletic in origins. The genus or rather random grouping of spheroidal morphotypes comprises however certain specimens that are recognized in several case studies of microfossils of various ages as representing green microalgae of the prasinophycean and chlorophycean affinities (Arouri et al., 1999, 2000; Talyzina and Moczydłowska, 2000; Moczydłowska, 2008b, 2010, 2015; Moczydłowska and Willman, 2009; Moczydłowska et al., 2010, 2011). The recognition of species in Leiosphaeridia (Jankuskas et al., 1989) and their emendations (Javaux and Knoll, 2017) are based on the vesicle size classes and wall thickness, which are subjective features and vesicle size overlap substantially in various assemblages studied (Grey, 2005; Fig. 6). The wall thickness is not actually measured to be objective morphologic feature but estimated by the transparent vs dark colour of vesicle wall as its indication, but it may show taphonomic alteration and is non-diagnostic. The exception in recognizing the species in Leiosphaeridia may be in the case of distinct features observed, such as circular pylome (L. gorda) or trapezoid pattern of vesicle splitting (L. ternata) (Strother and Wellman, 2016; Loron and Moczydłowska, 2017). The purported Leiosphaeridia species distinguished by the vesicle diameter apparently increase the diversity in the Mesoproterozoic and may falsify it. Under this criterion of grouping spheroidal morphotypes, Pseudozonosphaera Xing and Liu, 1973 (smooth-walled or slightly granulate vesicle with marginal ringlike compression folds), Pseudofavososphaera Xing, 1982 (vesicle with randomly distributed holes or pits which are of different sizes), and Schizospora Yan, 1995 (elongate or spheroidal, smooth-walled vesicle with a partial rupture), are considered to be junior synonyms of Leiosphaeridia. The ascribed to these genera features of compression folds, pits and holes in the vesicle wall (Xing and Liu, 1973, 1982; Xing

42

et al., 1985; Yan, 1995) are taphonomically induced alterations. We attribute spheroidal vesicles from Changcheng Group with psilate wall and of various wall thickness (from light coloured and transparent to dark brown and opaque) and diameters to as Leiosphaeridia spp. Leiosphaeridia spp. Fig. 6a–u Synonymy. 1973 Pseudozonosphaera sinica Sin et Liu gen. et sp. n. – Xing and Liu, p. 19, 56, pl. VI, fig. 13; pl. XII, figs. 8–10. 1973 Pseudozonosphaera cf. sinica Sin et Liu sp. n. – Xing and Liu, p. 20, pl. X, figs. 3–4. 1973 Pseudozonosphaera verrucosa Sin et Liu gen. et sp. n. – Xing and Liu, p. 19, 56, pl. II, figs. 1, 6–7. 1985 Favososphaeridium cf. plicativus (Schep.) – Yan, pl. I, fig. 26. 1985 Favososphaeridium sp. – Yan, pl. I, fig. 27. 1985 Leiovalia oblonga (Eisenack) – Yan, pl. V, fig. 2. 1985 Leiovalia ovalis (Eis.) – Yan, pl. V, fig. 3. 1985 Leiovalia tenera Kirjanov – Yan, pl. V, fig. 1. 1985 Pseudozonosphaeridium sinicum (Sin et Liu) – Yan, pl. I, fig. 22. 1985 Pseudozonosphaeridium sp. – Yan, pl. I, fig. 23. 1985 Sticotosphaeridium implexum Tim. – Yan, pl. I, fig. 28. 1985 Sticotosphaeridium sp. – Yan, pl. I, fig. 29. 1985 Valvimorpha semisphaerica Yan gen. et sp. n. – Yan, p. 157, pl. V, fig. 14. 1986 Chuaria circularis Walcott – Zhang, fig. 4. 1991 Pseudozonosphaeridum lucidum Andr. – Yan, pl. I, fig. 20.

43

Fig. 6. (a–u) Leiosphaeridia spp., exhibiting large variations in vesicle size, wall thickness, and compression folds depending on the preservational state. (a) PB22511, chl-cq 0516, M/24/1; (b) PB22512, chz-pj 0301, X/23/3-4; (c) PB22513, chz-pj 0814, V/25/4; (d) PB22514, chz-pj 0812, S/46/2; (e) PB22515, chz-pj 0811, J/17/4; (f) PB22516, chz-pj 0814, W/32/4; (g) PB22517, chz-pj 0813, W/39/1-3; (h) PB22518, chz-pj 0805, D/25/1; (i) PB22519, chz-pj 0811, W/19/2; (j) PB22520, chl-cq 0514, V/24/2; (k) PB22521, chl-cq 0511, J/34; (l) PB22522, chz-pj 0805, W/33/3; (m) PB22523, chz-pj 0812, Y/26/1; (n) PB22524, chz-pj 0811, O/36; (o) PB22525, chz-pj 0312, T/42/1; (p) PB22526, chz-pj 0311, H/36; (q) PB22527, chz-pj 0811, P/21/4; (r) PB22528, chz-pj 0312, U/34/2-4; (s) PB22529, chzpj 0811, G/22/3; (t) PB22530, chz-pj 0811, D/18/4; (u) PB22531, chl-cq 0514, B/18/1. Arrow in (o)

44

marks the smooth wall surface in contrast to the taphonically induced wrinkled surface shown in (o1) of the same specimen.

1991 Pseudozonosphaeridum cf. asperellum (Sin et Liu) – Yan, pl. I, fig. 21. 1991 Stictosphaeridium cf. rugosum Yin – Yan, pl. I, fig. 17. 1993 Chuaria circularis Walcott – Yan and Liu, pl. IV, fig. 4. 1993 Majasphaeridium carpogenum Hermann – Yan and Liu, pl. II, fig. 4. 1995 Pseudofavososphaera obsoleta Xing et Liu – Yan, pl. IV, fig. 9. 1995 Pseudofavososphaera tenera sp. nov. – Yan, p. 362, pl. III, fig. 15. 1995 Schizospora piriformis gen. et sp. nov. – Yan, p. 364, 370, pl. I, fig. 14. 1995 Stictosphaeridium implexum Tim. – Yan, pl. IV, fig. 10. 1995 Stictosphaeridium aff. sinapticuliferum Tim. – Yan, pl. III, fig. 13. Material. – More than 500 specimens in various states of preservation from Changzhougou Formation at Pangjiapu section, and Chuanlinggou Formation at Changzhoucun-Qingshanling section. Description. – Smooth-walled spheroidal vesicles often with taphonomically formed compression folds. Vesicle wall is thin to thick and consequently transparent to dark in appearance. Vesicle diameter ranges substantially from tens to hundreds microns. Excystment structure by partial rupture or median split. Dimensions. – Vesicle diameter 23–231 μm (mean = 70.3 μm, N = 493). Remarks. – The distinction of excystment structure by median split or rupture from taphonomically induced breakage has been demonstrated, illustrated and discussed in several studies (Wicander, 2007; Grey and Willman, 2009; Loron and Moczydłowska, 2017). The excystment by rupture (Fig. 6d, i) and large pylome (Fig. 6t) is also shown herein in contrast to taphonomic breakage (Fig. 6f, p, q). The circular opening is

45

morphologically pre-determined (Fig. 6t) in difference to irregular holes resulting from vesicle damage seen in the same specimen. In early studies of microfossils from the Changcheng Group, diverse taphonomic changes were considered as morphologic features leading to describing many species and genera, which are among Leiosphaeridia as synonymized here (see genus remarks). Consequently, the species of Pseudozonosphaera, Pseudofavososphaera and Schizospora are transferred here to Leiosphaeridia spp. Many Changcheng fossils previously recognised as various species assigned to Kildinella, Leiominuscula, Leiopsophosphaera, Nucellosphaeridium, Orygmatosphaeridium, Protoleiosphaeridium, Protosphaeridium, Trachysphaeridium and Trematosphaeridium, Zonosphaeridium (Xing and Liu, 1973; Luo et al., 1985, 1986; Xing et al., 1985; Yan, 1985, 1991, 1995; Sun, 1989, 2006; Yan and Liu, 1993), are considered as Leiosphaeridia spp. (although not listed in Synonymy), since these genera had been previously revised as junior synonyms of Leiosphaeridia Eisenack, 1958 (Jankauskas et al., 1989; Fensome et al., 1990; Wicander, 2007; Moczydłowska, 2008b). Other Changcheng microfossils with psilate or coarse vesicle wall previously identified under Favososphaeridium, Leiovalia, Stictosphaeridium, Valvimorpha, Chuaria, and Majasphaeridium are reassigned as Leiosphaeridia spp. (Xing and Liu, 1973; Yan, 1985, 1991, 1995; Yan and Liu, 1993; Zhang, 1986).

Genus Navifusa Combaz, Lange and Pansart, 1967, ex Eisenack, 1976. Type species. – Navifusa navis (Eisenack, 1937) Eisenack, 1976. The holotype (Eisenack, 1937, pl. 16, fig. 8) was lost and the neotype was selected from the Silurian strata on the Öland Island in Sweden (Eisenack, 1976, p. 192, pl. 3, fig. 17).

46

Remarks. The genus Navifusa has been diagnosed as elongate ellipsoidal vesicle with round ends and without processes, and with smooth or ornamented vesicle wall (Combaz et al., 1967; Eisenack et al., 1979). It is morphologically similar to Archaeoellipsoides Horodyski and Donallson, 1980. But the latter was erected based on three-dimensionally preserved silicified microfossils (Horodyski and Donaldson, 1980), and later studies seem only assigned silicified ellipsoids to such taxa (e.g. Zhang, 1985; Golubic et al, 1995; Sharma-Shukla, 2009), while Navifusa is mostly recognized as flattened organic walled microfossils. Navifusa is a long-ranging taxon known from the upper Paleoproterozoic (this study) to Carboniferous successions (Eisenack et al., 1979; Fatka and Brocke, 2008). Precambrian species include Navifusa majensis Pyatiletov, 1980b, N. bacillaris German, 1981, and N. actinomorpha Maithy, 1975 (Hofmann and Jackson, 1994; Samuelsson, 1997; Golubkova et al., 2010; Couëffé and Vecoli, 2011; Baludikay et al., 2016; Porter and Riedman, 2016; Riedman and Porter, 2016). Navifusa sp. Fig. 4i–j Material. – 4 specimens in various states of preservation from Changzhougou Formation at Pangjiapou section. Description. – Elongated, ellipsoidal vesicle with two rounded ends. Vesicle wall is usually thick, with psilate or slightly granular surface. Some specimens show a few longitudinally arranged long and narrow compression folds. Excystment structure not observed. Dimensions. – Vesicle length 57–140 μm (mean = 104.8 μm; N = 3); vesicle width 33–62 μm (mean = 46.6 μm; N = 3).

47

Remarks. – Navifusa sp. is very rare in Changzhougou Formation. Considering its non-diagnostic morphology, we describe it under an open nomenclature.

Genus Oscillatoriopsis Schopf, 1968, emend. Butterfield, Knoll and Sweet, 1994 Type species. – Oscillatoriopsis obtusa Schopf, 1968, from c. 825 Ma Bitter Springs Formation at Ross River area in central Australia (Schopf, 1968, 1970). Oscillatoriopsis longa Timofeev, Hermann, 1979, emend. Butterfield, Knoll and Sweet, 1994 Fig. 10e Material. – A single fragmentarily preserved specimen from Changzhougou Formation at Pangjiapu section. Description. – Unbranched, uniseriate, multicellular trichome without constriction at septa and no surrounding sheath being observed. Dimensions. – Fragmented specimen length 56 μm, filament width c. 20 μm.

Genus Pterospermopsimorpha Timofeev, 1966, emend. Mikhailova and Jankauskas, 1989 (in Jankauskas et al., 1989) Type species. – Pterospermopsimorpha pileiformis Timofeev, 1966, emend. Mikhailova, 1989 (in Jankauskas et al., 1989). The holotype was lost and the lectotype was selected from the microfossil collection from the c. 850 Ma Miroedikha Formation in Turukhansk Uplift, Siberian (Jankauskas et al., 1989; Mendelson and Schopf, 1992).

48

Fig. 7. (a–d) Pterospermopsimorpha insolita. (e–g) Simia annulare. (a) PB22532, chz-pj 0813, M/33/1-3; (b) PB22533, chl-cq 0513, X/54/1; (c) PB22534, chl-cq 0512, Y/24/2-4; (d) PB22535, chzpj 0807, N/29/2; (e) PB22536, chl-cq 0517, N/15/4; (f) PB22537, chl-cq 0514, O/31; (g) PB22538, chlcq 0602, U/26/3.

Remarks. – Pterospermopsimorpha is a disphaeromorph taxon characterized by sphere-in-sphere body plan and may appear similar to Simia Mikhailova and Jankauskas, 1989 (in Jankauskas et al. 1989) which is a spheroidal or discoidal microfossil with an equatorial flange (Jankauskas et al., 1989; Moczydłowska, 2015; Riedman and Porter, 2016; Sergeev et al., 2017). It has been interpreted as a member of green algae on the basis of its remarkable similarity to the phycoma (resting/reproductive cyst) of the extent Class Prasinophyceae (Tappan, 1980; GuyOhlson, 1996; Moczydłowska et al., 2011; Moczydłowska, 2015; Loron and Moczydłowska, 2017). Pterospermopsimorpha insolita Timofeev, 1969, emend. Mikhailova, 1989 (in Jankauskas et al., 1989) Fig. 7a–d

49

Synonymy. For synonymy see Loron and Moczydłowska, 2017, and additionally: 1987 Pterospermopsimorpha cf. pileiformis Timofeev, 1966 – Yin, p. 459, pl. 5, fig. 6. 1987 Pterospermopsimorpha sp. B – Yin, p. 459, pl. 5, fig. 11. 1993 Pterospermopsimorpha aff. insolita Tim. – Yan and Liu, pl. I, fig. 12. 1994 Pterospermopsimorpha pileiformis Timofeev, 1966 – Butterfield et al., p. 44, fig. 14H. 1995 Pterospermopsimorpha aff. binata Tim. – Yan, pl. III, fig. 20. 1997 Simia annulare (Timofeev) Mikhailova, 1989 – Samuelsson, p. 176, fig. 9C–F. 1999 Simia annulare (Timofeev) Mikhailova, 1989 – Samuelsson et al., fig. 7a, g. 2016 Pterospermopsimorpha insolita – Baludikay et al., fig. 7I–L. 2017 Pterospermopsimorpha insolita Timofeev, 1969, emend. Mikhailova, 1989 (in Jankauskas et al., 1989) – Loron and Moczydłowska, p. 18–20, pl. 4, figs. 1–6. Material. – 2 specimens from the Changzhougou Formation at Pangjiapu section, and 4 from the Chuanlinggou Formation at Changzhoucun-Qingshanling section. Description. – Spheroidal to ellipsoidal vesicle, originally spheroidal, enclosing a large, dark spheroidal internal body. Outer vesicle wall is thin or thick, translucent and smooth or slightly corrugated due to poor preservation. The internal body is dense in appearance and mostly located at the centre of the outer vesicle wall. Dimensions. – Overall vesicle diameter 38–70 μm (mean = 50.4 μm; N = 6); internal body diameter 23–49 μm (mean = 30.9 μm; N = 6); ratio of internal body/outer vesicle wall diameter 0.44–0.85 (mean = 0.64; N = 6). Remarks. – The genus Pterospermopsimorpha was emended by Mikhailova and Jankauskas (in Jankauskas et al., 1989) and three species of it were described. P. pileiformis as the type species differs from other species by its shagreen sculpture of

50

vesicle wall. P. insolita differs in its smooth surface of outer vesicle, and P. granulata is distinguished by its granular sculpture of outer vesicle surface (Jankauskas et al., 1989). Another species of Pterospermopsimorpha named P. binata was recently synonymised as P. insolita (Loron and Moczydłowska, 2017). Following these criteria, microfossils previously assigned to P. cf. pileiformis and P. sp. B from the Qinggou Formation in North China (Yin et al., 1987) and P. pileiformis from the Svanbergfjellet Formation in Spitsbergen (Butterfield et al., 1994), were originally described having smooth or psilate outer envelope. These specimens may well be reassigned as P. insolita. In addition, “Simia annulare” from Chapoma Formation in East European Platform and Qaanaaq Formation in Northwest Greenland, was described as a spheroidal to ovoid vesicle surrounded by a thin, psilate outer membrance, and Simia was considered as a double-walled sphaeromorph (Samuelsson, 1997; Samuelsson et al., 1999). Considering the difference between Simia and Pterospermopsimorpha (genus Remarks), fossils identified as “Simia annulare” in these studies could be reassigned as P. insolita. Occurrence and stratigraphic range. – P. insolita is a cosmopolitan species and has been recorded worldwide in the successions of the late Paleoproterozoic to early Neoproterozoic. It is known from late Paleoproterozoic Chuanlinggou Formation (Yan and Liu, 1993; Yan, 1995), early Mesoproterozoic Beidajian Formation (Agić et al., 2017), Qinggouzi (= Qinggou) Formation (Tonian in age, and this age was constrained by correlation to the Cuijiatun and Majiatun formations which underlies the Tonian Xingmincun Formation in Liaoning Province) (Yin, 1987; Liu et al., 2005; Zhang et al., 2016) in North China; c. 1.63–1.60 Ga Kheinjua Supergroup in India (Sarangi et al., 2004; Prasad et al., 2005); c. 1.3–1.2 Ga Qaanaaq Formation in Northwest Greenland (Samuelsson et al., 1999); late MesoproterozoicLinok

51

Formation (Timofeev, 1969; Jankauskas et al., 1989; Semikhatov et al., 2015), c. 1030 Ma Lakhanda Formation in Uchur-Maya region (Jankauskas et al., 1989; Mendelson and Schopf, 1992), and early Neoproterozoic Chapoma Formation in East European Platform, Russian Federation (Samuelsson, 1997); c. 1.27–0.75 Ga Bylot Supergroup in Canada (Hofmann and Jackson, 1994); Meso-Neoproterozoic Abetifi Formation in Ghana (Couëffé and Vecoli, 2001); Meso-Neoproterozoic Mbuji-Mayi Supergroup in Democratic Republic of Congo (Baludikay et al., 2016); Neoproterozoic Browne and Kanpa formations and c. 811–716 Ma Alinya Formation in Australia (Cotter, 1999; Riedman and Porter, 2016); c. 788–740 Ma Visingsö Group in Sweden (Loron and Moczydłowska, 2017; Moczydłowska et al., 2017); c. 750–700 Ma Svanbergfjellet Formation in Spitsbergen (Butterfield et al., 1994); c. 742 Ma Chuar Group in USA (Nagy et al., 2009).

Genus Satka Jankauskas, 1979a Type species. – Satka favosa Jankauskas, 1979a, from Lower Riphean Satka and Bakal formations in Southern Ural Mountains, Russian Federation (Jankauskas, 1979a). This chronostratigraphic unit is currently estimated to be early Mesoproterozoic in age (Loron and Moczydłowska, 2017). In addition, upper Satka Formation was dated to 1550±30 Ma by the Pb–Pb method on limestones (Kuznetsov et al., 2008). Remarks. – The genus Satka was designated, based on the type species S. favosa Jankauskas 1979a, as “Spheroidal or ellipsoidal vesicle composed of discrete polygonal, tetra- to hexagonal convex plates, which were separated by deep grooves on the vesicle surface and formed the cell-like structure inside the vesicle (or mesh

52

structure on the inner wall surface and inside the vesicle)” (Jankauskas, 1979a, p. 1466; Jankauskas et al., 1989, p. 50–51; translation by M. Moczydłowska). Satka colonialica Jankauskas, 1979b was diagnosed as “Large, thin-walled vesicle made of plates. The vesicle shape is elongate-ellipsoidal, pillow-shaped or more complex. Surface microgranular. Diameter 150 μm, individual plates 4–8 μm. The plated structure (made of plates) of the vesicle not always clearly expressed and better seen on the vesicle contour” (Jankauskas, 1979b, p. 192–194; Jankauskas et al., 1989, p. 51; translation M. Moczydłowska). Satka squamifera Pyatiletov, 1980a, was described as spheroidal to ovoidal vesicles, 45–100 μm in diameter, made of rounded slightly convex plates 7–15 μm in diameter, which are divided between each other by shallow grooves (Jankauskas et al., 1989, p. 52; translation M. Moczydłowska). Recently, Satka colonialica Jankauskas, 1979b was transferred as a new combination to newly established genus Squamosphaera Tang et al., 2015, which is diagnosed by having domical processes (Tang et al., 2015). Other species, such as Satka elongata Jankauskas, 1979b and Satka granulosa Jankauskas, 1980 were synonymized with Satka favosa (Javaux and Knoll, 2017). The question remains if the transfer of Satka colonialica to a different genus Squamosphaera as a new combination Squamosphaera colonialica Tang et al., 2015 is substantiated. Squamosphaera was defined as “spheroidal to tomaculate vesicles ornamented with a moderate number of broadly domical processes” (Tang et al., 2015). However, originally Satka colonialica was described as, ellipsoidal to complex shaped vesicle made of “plates” or “lamellar structures” (пластинчатого строения) (Jankauskas, 1979b, p. 192). It is debatable to morphologically equal “plates” with domical processes. Moreover, the “plates” in the holotype of Satka colonialica (Jankauskas, 1979b, fig. 1.4; Jankauskas et al., 1989, pl. IV, fig. 4), display the clear

53

angular or quadrate shape at the right down side (also presenting on the right upper side) of this specimen (Jankauskas et al., 1989, pl. IV, fig. 4), which are detached and look like “platy” rather than in domical shape. We observed the studied specimens (Fig. 8), which greatly resemble Satka colonialica illustrated by Jankauskas, 1979b (p. 192–193, fig. 1.4, 1.6) and Jankauskas et al., 1989 (pl. IV, figs. 4, 7) in both the overall morphology from ellipsoidal to complex shaped, and the appearance of surface “plates” that are angular in shape as more easily being identified on the fossil outline or contour. The colonial nature of present specimens is interpreted here as evidenced by well-preserved subround tetrads (Fig. 8a, a1). From the fossil surface, individual cells are closely juxtaposed with neighbouring cells (Fig. 8a2, k-l), and quadrate to angular in shape, making them look like “plates” (Fig. 8a2, d, f–h), but the angular shape is probably due to mutual compression between cells. Accordingly, Satka colonialica is viewed as a tightly packed cell colony with unique cell arrangement rather than an empty envelope with domical processes. And, this species is retained here valid as a form species on the basis of the morphological similarity of its constituent cells (quadrate to angular in shape and looking like “plates”) to the plates in the type species Satka favosa (Jankauskas, 1979a). In addition, Satka colonialica when preserved in ellipsoidal outline (Fig. 8h–j), is morphological similar to Satka favosa to some extent.

54

Fig. 8. (a–l) Satka colonialica, showing various shapes of multicellular colonies’ outline and their wide range of overall size, but having constituent cells of the same in shape and size, and consistent topologic arrangement. (a1) enlargement of specimen in (a) displaying well-preserved sub-round tetrads. (a2) enlargement of specimen in (a) showing juxtaposed quadrate to angular cells which look like “plates” due to mutual compression between cells. Arrows in (c) mark two planar tetrads. (k–l) SEM images documenting well-defined individual cells and their topology in tetrads. (a) PB22567, chl-

55

cq 0601, W/22; (b) PB22568, chl-cq 0505, U/37/2; (c) PB22569, chl-cq 0516, E/38/2-4; (d) PB22570, chl-cq 0516, L/35/1-2; (e) PB22571, chl-cq 0501, J/39/4; (f) PB22572, chl-cq 0513, Y/36/1; (g) PB22573, chl-cq 1001, C/23/2-4; (h) PB22574, chl-cq 0504, E/23/1-2; (i) PB22575, chl-cq 06a04, J/16/2-4; (j) PB22576, chl-cq 0517, F/11/3; (k) PB22577, chl-cq 05d, no England Finder coordinate. (l) PB22578, chl-cq 05g, no England Finder coordinate. The double bar represents 20 μm for (a–j), and single bar represents 5 μm for (k–l).

Satka colonialica Jankauskas, 1979b Fig. 8a–l Synonymy. 1979b Satka colonialica Jankauskas sp. n. – Jankauskas, p. 192–193, fig. 1.4, 1.6. 1989 Satka colonialica Jankauskas 1979 – Jankauskas et al., p. 51, pl. IV, figs. 4, 7. 1980 “polygonally segmented sphaeromorphs” – Horodyski, p. 657, pl. 2, figs. 8–12. 1980 “bumpy surfaced sphaeromorphs”– Horodyski, p. 657, pl. 2, figs. 13–15. 2005 Satka colonialica Jankauskas – Prasad et al., p. 52, pl. 4, figs. 11, 15; pl. 7, figs. 6, 11; pl. 8, fig. 7. 2005 Satka squamifera Pyatiletov – Prasad et al., p. 52, pl. 4, figs. 10, 13; pl. 5, figs. 1–2; pl. 7, fig. 12; pl. 8, fig. 6. 2016 Unnamed form D – Porter and Riedman, p. 846, fig. 23.2. 2017 Satka favosa – Adam et al., fig. 2C. Material. – More than 30 well-preserved specimens and numerous poorly-preserved ones from Chuanlinggou Formation at Changzhoucun-Qingshanling section; 9 specimens from Changzhougou Formation at Pangjiapu section. Description. – Round to ellipsoidal, elongate or more complex in overall shape of colony, composed of tightly packed cells. From colonial surface, constituent cells are juxtaposed with neighbouring cells. Individual cells are smooth walled, mostly quadrate or angular in surface outline due to mutual compression and seen in portions 56

of colony as rows of cells. Cell wall is thin to thick, and translucent to dark. No external envelope is observed. Dimensions. – Colony size 12–75 μm; individual cell diameter 3–9 μm (mean = 4.7; N = 164). Remarks. – Constituent cells in studied specimens are the same in size, shape (mostly quadrate) and the pattern of arrangement, suggesting them as one biological species, although the overall colonial outline varies greatly from round to complex shaped. The wide range of colony size (small to large) and variable outline (sub-round to irregular in shape; Fig. 8a–l) may show the development and growth of the colony. Our specimens are morphologically resembling some modern cyanobacteria from the Order Pleurocapsales Myxosarcina and Chroococcidiopsis which also form threedimensional and tightly packed cell aggregates having sub-round, elongated to complex-shaped outlines (Waterbury and Stanier, 1978, figs. 23–25). Constituent cells of these modern analogues also could be angular in shape due to mutual compression and sometimes arranged in rows (Waterbury and Stanier, 1978, fig. 24b). The cell walls of species among the Pleurocapsales, unlike other cyanobacteria, have additional comparatively thick external fibrous layer (named F layer) closely attached to the outer membrane layer. These layers, together with peptidoglycan layer forming the basic cell wall structure of Gram-negative bacteria, including cyanobacteria, increase their cell thickness as the cells is growing (Waterbury and Stanier, 1978). The F layer in walls of species belonging to Pleurocapsales may have a great potential to be preserved as microfossils. Therefore, it is possible to consider S. colonialica as being of cyanobacterium affinity. Microfossils from lower Belt Supergroup, such as “polygonally segmented and bumpy surfaced sphaeromorphs” from Chamberlain Shale (Horodyski, 1980, pl. 2,

57

figs. 8–15, 21), and “colonial Satka favosa” from Greyson Formation (Adam et al., 2017, fig. 2C), here are viewed as S. colonialica as indicated by the colonial feature and overall morphology. The Chamberlain microfossils were compared to the outer sheath of extant colonial Entophysalis sp. by Horodyski (1980), suggesting its cyanobacterial origin. “Satka squamifera” from Vindhyan Supergroup in India, was originally depicted as “colnies oval to elliptic, flattened, mostly elongate…” (Prasad et al., 2005, p. 52), showing ellipsoidal (Prasad et al., 2005, pl. 4, fig. 10; pl. 8, fig. 6) to complex fossil outline (Prasad et al., 2005, pl. 4, fig. 13; pl. 7, fig. 12). These fossils here are reassigned as S. colonialica based on the colonial nature and morphological similarity to our specimens (Fig.8). The same is true for specimen described as “Unnamed form D” from Chuar Group (Porter and Riedman, 2016, p. 846, fig. 23.2) exhibiting tightly packed quadrate constituent cells (originally described as “polygonal pillows”) which are very similar to our specimen not only in cell morphology and arrangement but also in cell size (Fig. 8k). Occurrence and stratigraphic range. – From Mesoproterozoic to early Neoproterozoic Kheinjua and Rohtas groups of Vindhyan Supergroup in Madhya Pradesh area, India (Prasad et al., 2005; Ray et al., 2002; Sarangi et al., 2004); Middle Riphean Zigazino-Komarovo Formation in Ural Mountains, Russian Federation (Jankauskas, 1979b); c. 1.57–1.45 Ga Chamberlain and Greyson formations of lower Belt Supergroup in Montana (Horodyski, 1980; Adam et al., 2017), and c. 780–740 Ma Chuar Group in Arizona, USA (Porter and Riedman, 2016).

Genus Schizofusa Yan, 1982

58

Type species. – Schizofusa sinica Yan, 1982 from late Paleoproterozoic Chuanlinggou Formation, Jizhou District, northern Tianjin area, North China (Yan, 1982). Synonymy. 1982 Schizofusa Yan gen. n. – Yan, p. 2, 5. 1985 Diplomembrana Yan gen. n. – Yan, p. 150, 159–160. 1985 Schizovalvia Yan gen. n. – Yan, p. 152–153, 160. Remarks. – The genus Schizofusa has been recognized as fusiform to ellipsoidal vesicle with a slit-like opening having, or not, bordered folds extending from pole to pole, and consisted of two species S. sinica and S. aperta (Yan, 1982). Similar fusiform microfossils from the Roper Group in Australia were earlier interpreted as curling-up valves of the outer membrane of some disphaeromorphs after releasing the inner sphaeromorphic vesicle by median split (Peat et al., 1978, fig. 5o–s). This interpretation was followed by Zhang (1986) who studied acritarchs from the Chuanlinggou Formation in the Yanshan Range (Zhang, 1986, pl. 1, fig. 5), and considered Schizofusa as representing rolled valves of the vesicle. Subsequently, Lamb et al. (2009) recovered fusiform microfossils from the Changzhougou Formation at Pangjiapu section and interpreted the shape of vesicle opening as the result of enrolment of vesicle after excysting by median split. Such enrolling of vesicle after splitting into two parts (Lamb et al., 2009, fig. 5A, D) are observed in extant coccoid microalga Nannochloropsis (Eustigmatophyte) and being cast-off during vegetative reproduction and subsequently enrolled into fusiform shape (Lamb et al., fig. 9A–B). Schizofusa was further suggested to be derived from originally smooth-walled spheroidal vesicle such as Leiosphaeridia based on studies of permineralized

59

microfossils from the Ediacaran Doushantuo Formation in Hubei Province, South China (Wang et al., 2015a). The inferred developmental phases from a spherical vesicle (Leiosphaeridia) gradually changing into two fusiform valves (Schizofusa) were considered as showing synonymous taxa and thus Schizofusa being redundant. However, if this would be the case, both morphotypes should co-occur frequently through the geologic time but Schizofusa is restricted to specific stratigraphic intervals. The morphological recognition of form-taxa supports the two genera being sustained, and Schizofusa is well-defined by its mode of opening or division with forming the lips or folded edges and differs from simply splitting leiosphaerids (Grey, 2005). More than 100 specimens studied show a substantial morphological variety in the shape of the opening, opening bordered fold, longitudinal folds, vesicle size and the wall thickness (Fig. 9a–o). Some fossils have slit-like opening (Fig. 9a, g, k, m), others have V-shaped opening at one end (Fig. 9b, e, i, j, n), or no opening is present (Fig. 9c, d, h, l). This morphological variability probably results from different degree of enrollment of separated valves. Similar, if not identical enrolment is also observed in spheroidal Valeria lophostriata (Fig. 11c–d). Therefore, Schizofusa is probably originated from enrolled valves of smooth-walled spheroidal vesicles (such as Leiosphaeridia) which is featured by median split, but the original vesicle of being ellipsoidal has not been excluded. Because, some Ediacaran species of Schizofusa (S. risoria and S. zangwenlongii) have been described as being originally ellipsoidal, with their slit-like opening extending along the longitudinal axis of the vesicle (Grey, 2005). Based on the above interpretation, genera Diplomembrana and Schizovalvia both erected based on microfossils from Chuanlinggou Formation, are synonymized here and considered to be preservation variants of Schizofusa. Because

60

Diplomembrana was defined as a fusiform to elongate-oval vesicle containing another fusiform or ellipsoidal hollow inner body, and both fusiforms often have longitudinal slit and occasionally develop lateral folds (Yan, 1985). Such “fusiform within fusiform” structure is interpreted here as resulted from two valves that have enrolled together (e.g. Fig. 9f). And Schizovalvia is diagnostic of fusiform, triangular to obcordiform vesicle which usually has a longitudinal V-shaped slit between ends (Yan, 1985). Schizofusa sinica Yan, 1982 Fig. 9a–o Synonymy. 1982 Schizofusa sinica Yan gen. et sp. nov. – Yan, p. 2, 5, pl. I, figs. 1–10. 1982 Schizofusa aperta Yan gen. et sp. nov. – Yan, p. 2, 6, pl. I, figs. 11–18. 1985 Leioarachnitum apertum (Comb. nov.) Luo et Zhang – Luo et al., pl. I, figs. 8, 12 (nomen nodum). 1985 Leioarachnitum sinitum (Comb. nov.) Luo et Sun – Luo et al., pl. I, figs. 10, 13 (nomen nodum). 1985 Leioarachnitum vittatum Andreeva – Yan, pl. II, fig. 21. 1985 Leioarachnitum aff. vittatum Andr. – Luo et al., pl. I, fig. 11. 1985 Leioarachnitum sp. 1 – Luo et al., pl. I, fig. 7. 1985 Leiofusa sp. – Yan, pl. II, fig. 20. 1985 Macroptycha aff. biplicata Tim. – Luo et al., pl. I, fig. 9. 1985 Macroptycha multiplicata Tim. – Yan, pl. II, fig. 18.

61

Fig. 9. (a–o) Schizofusa sinica, showing morphological variants of size, wall thickness, mode of opening, compressional folds, and the degree of vesicle enrolling. (a) PB22539, chz-pj 0814, C/31/4; (b) PB22540, chz-pj 0812, K/43; (c) PB22541, chl-cq 0509, F/35/3; (d) PB22542, chz-pj 0813, S/22/4; (e) PB22543, chz-pj 0812, W/44/2; (f) PB22544, chz-pj 0308, G/27/3; (g) PB22545, chz-pj 0812, L/26/3; (h) PB22546, chl-cq 0509, D/29/1-2; (i) PB22547, chz-pj 0814, S/31/1-3; (j) PB22548, chz-pj 0814, O/47/4; (k) PB22549, chz-pj 0815, D/11/4; (l) PB22550, chz-pj 0814, U/44/4; (m) PB22551, chz-pj 0803, G/35/4; (n) PB22552, chz-pj 0801, J/30; (o) PB22553, chz-pj 0806, R/22/1-3. Arrows in (o) mark step-wise darkening of vesicle walls resultant from multiple enrollment, and in (b, e, i, j and n) denote V-shaped opening.

1985 Macroptycha uniplicata Tim. – Yan, pl. II, fig. 17. 1985?Macroptycha sp. – Luo et al., pl. I, fig. 6. 1985 Macroptycha sp. – Luo et al., pl. II, fig. 8. 1985 Scaphita sp. – Yan, pl. II, fig. 19. 1985 Scaphomorphida – Luo et al., pl. II, figs. 7, 10. 1985 Veryhachinum sp. – Luo et al., pl. II, figs. 2–3. 62

1986 Leioarachnitum aperta (Yan) – Luo et al., pl. II, fig. 7. 1986 Leioarachnitum primistinum Luo et Sun sp. nov. – Luo et al., p. 471, pl. II, figs. 8–10. 1986 Leioarachnitum cf. vittatum Andr. – Luo et al., p. 471, pl. I, fig. 16. 1986 Leioarachnitum sp. – Luo et al., p. 472, pl. I, fig. 7. 1986 Leiosphaeridia Eisenack – Zhang, fig. 5 1986 Macroptycha sp. 1 – Luo et al., pl. I, fig. 5. 1986 Macroptycha sp. 2 – Luo et al., pl. II, fig. 1. 1986 Veryhachium sp. – Luo et al., p. 472, pl. II, figs. 18–19. 1989 Leioarachnitum aperta (Yan) Luo et Zhang – Sun, pl. I, fig. 13. 1989 Leioarachnitum longplicatum Sun sp. nov. – Sun, p. 241, pl. II, figs. 7–8. 1989 Leioarachnitum primistinum Luo et Sun – Sun, pl. I, figs. 11. 1989 Leioarachnitum sinitum (Yan) Luo et Sun – Sun, pl. I, figs. 12, pl. II, fig. 9. 1989 Leioarachnitum simplex Sun (sp. nov.) – Sun, p. 241, pl. I, figs. 15–16. 1989 Leioarachnitum sp. – Sun, pl. I, fig. 14. 1989 Macroptycha triplicata Timofeev – Sun, pl. II, fig. 2. 1989 Macroptycha uniplicata Timofeev – Sun, pl. I, fig. 10. 1989 Scaphita rugosa Sun (sp. nov.) – Sun, p. 241–242, pl. II, figs. 3–4. 1989 Trachysphaeridium incrassatum Sun (sp. nov.) – Sun, p. 247, pl. II, figs. 5–6. 1991 Foliomorpha glottiformis sp. nov. – Yan, p. 189–190, 193, pl. III, fig. 4. 1991 Leiofusa aff. simplex (Combaz, 1967) Eisenack, 1976 – Yan, p. 187, pl. II, fig. 13–14. 2017 Schizofusa sinica Yan, 1982 – Loron and Moczydłowska, p.21, pl. 3, fig. 7.

63

Material. – More than 100 specimens in various states of preservation from Changzhougou Formation at Pangjiapu section and Chuanlinggou Formation at Changzhoucun-Qingshanling section. Description. – Smooth-walled fusiform in shape vesicle with longitudinal slit- or Vshaped opening, or without opening. Slit opening extends along the vesicle from pole to pole and may possess additionally dark, border folds. V-shaped opening may be present at two or one pole of the vesicle. Vesicle wall is occasionally thin and translucent but mostly thick and dark. Vesicle size varies substantially. Dimensions. – Vesicle length at long axis 47–289 μm (mean = 125.6 μm; N = 82); vesicle width at short axis 13–115 μm (mean = 48.1 μm; N = 80). Remarks. – Recently, Schizofusa aperta has been synonymized with the type species S. sinica alongside some other species of the genera Diplomembrana, Schizovalvia, and Taeniatum (Loron and Moczydłowska, 2017). Furthermore, the genera Diplomembrana and Schizovalvia are included herein in the synonymy of the genus Schizofusa, and consequently their species are taxonomically revised as Schizofusa sinica (not listed in Synonymy). Other fusiform-like specimens with smooth surface from Changzhougou and Chuanlingou formations previously were identified as several species assigned to Leioarachnitum, Leiofusa, Macroptycha, Scaphita, Scaphomorphida, Veryhachinum, Leiosphaeridia, Trachysphaeridium, and Foliomorpha (listed in the Synonymy), are here reassigned as S. sinica (Luo et al., 1985, 1986; Yan, 1985, 1991; Sun, 1989). Occurrence and stratigraphic range. – The late Paleoproterozoic Changzhougou and Chuanlinggou formations in Yanshan Range, North China (Yan, 1982, 1985, 1991; Luo et al., 1985, 1986; Sun, 1989); c. 788–740 Ma the informal Upper

64

Formation of Visingsö Group in Sweden (Loron and Moczydłowska, 2017; Moczydłowska et al., 2017).

Genus Simia Mikhailova and Jankauskas, 1989 (in Jankauskas et al., 1989) Type species. – Simia simica (Jankauskas, 1980) Jankauskas, 1989, from Upper Riphean Podinzersk Formation at Shisheniak River section in Southern Ural Mountains, Russian Federation (Jankauskas, 1980; Jankauskas et al., 1989). The age of the formation has been recently attributed to the Tonian (Porter and Riedman 2016). Remarks. – The genus Simia has been interpreted as belonging to the Class Prasinophyceae because of its phycoma-like vesicle structure and resemblance to extant morphological counterparts (Moczydłowska et al., 2011; Moczydłowska, 2015; Loron and Moczydłowska, 2017). Simia annulare Timofeev, 1969, emend. Mikhailova, 1989 (in Jankauskas et al., 1989) Fig. 7e–g Synonymy. See Loron and Moczydłowska, 2017 for synonymy, and additionally: 2008 Simia annulare (Timofeev, 1969) Mikhailova and Jankauskas, 1989 – Moczydłowska, fig. 4C. 2017 Simia annulare – Beghin et al., fig. 3e. 2017 Simia annulare Timofeev, 1969, emend. Mikhailova, 1989 (in Jankauskas et al. 1989) – Loron and Moczydłowska, p. 21–22, pl. 5, figs. 1–3. 2017 Simia annulare (Timofeev, 1969) Mikhailova in Jankauskas et al., 1989 – Tang et al., p. 5, fig. 3E.

65

Material. – 5 well preserved specimens from Chuanlinggou Formation at Changzhoucun-Qingshanling section. Description. – Circular to ovoidal vesicle, originally discoidal, consisting of internal body and a narrow equatorial flange made of thin membrane and extending from the internal body. The wall of internal body is thick, firm and dark, and often bearing ring-like compression folds at peripheral margin. Equatorial flange is narrow, semitransparent, with uneven outline due to poor preservation. The wall texture may appear shagrinate but it is the taphonomic feature. Dimensions. – Overall vesicle diameter 42–102 μm (mean = 66.0 μm; N = 4); internal body diameter 40–91 μm (mean = 59.8 μm; N = 4); width of equatorial flange is approximately 13.0 μm or less and depending on the state of preservation. Remarks. – Almost all compression folds in studied specimens of Simia occur on the marginal area of the internal body and are ring-shaped (Fig. 7e–g). This unique arrangement of folds, which is one of diagnostic features of Simia annulare, is consistent and thus suggests the assignment to this species. Occurrence and stratigraphic range. – Simia annulare has a worldwide distribution and stratigraphic range from late Paleoproterozoic to Ediacaran. It has been recorded from the late Mesoproterozoic–early Neoproterozoic En Nesoar Formation in Africa (Beghin et al., 2017); the late Mesoproterozoic–early Neoproterozoic Tilhar Formation from Ganga Valley in India (Tang et al., 2017); Tonian Liulaobei Formation from Anhui Province in North China (Zang and Walter, 1992; Tang et al., 2013); c. 788–740 Ma the informal Upper Formation of Visingsö Group in Sweden (Loron and Moczydłowska, 2017; Moczydłowska et al., 2017); late Tonian to early Cryogenian Khajpakh Formation (Vidal et al., 1993; Moczydłowska, 2008a), Ediacaran Nepa Horizon in Siberia (Nagovitsin and Kochnev, 2015); Upper Riphean

66

Kildin Group in East European Platform (Jankauskas et al., 1989); Neoproterozoic Kanpa and Hussar formations, and c. 811–716 Ma Alinya Formation from Officer Basin in Australia (Zang, 1995; Cotter, 1999; Riedman and Porter, 2016).

Genus Symplassosphaeridium Timofeev (1959) 1969 Type species. – Symplassosphaeridium tumidulum Timofeev, 1959, from the early Ordovician “Obolus”-shale beds in Vologda area, Russian Federation (Timofeev, 1959). Remarks. – Symplassosphaeridium has been originally recognised as globular compacted cell cluster (Timofeev, 1959). It differs from Synsphaeridium by its spheroidal or globular colonial shape, and relatively smaller constituent cells (Hofmann and Jackson, 1994) (More morphological comparison with other colonial microfossils, see genus Remarks of Eomicrocystis). Symplassosphaeridium sp. Fig. 10f–g Material. – 7 well-preserved specimens from Chuanlinggou Formation at Changzhoucun-Qingshanling section. Description. – Spheroidal to ellipsoidal colonies consisting of tightly packed round or oval small spheroidal cells with smooth wall surface. Individual cells are overlapping to some degree with each other. Dimensions. – Colony overall diameter 23–50 μm; cell diameter 6–11 μm (mean = 8.4 μm; N = 30). Remarks. – Constituent cells of present specimens occasionally show the planer group of four (Fig. 10g, g1), suggesting the spheroidal cells multiplied by binary fission in two planes and the cell division was not simultaneous in all cells. The

67

general morphology of colonies and individual cells without more diagnostic features prevents from recognizing the species within the genus and studied microfossils are grouped as Symplassosphaeridium sp.

Fig. 10. (a–d) Tetraphycus laminiformis sp. nov.; (e) Oscillatoriopsis sp.; (f–g) Symplassosphaeridium sp. (a) Holotype, PB22554, chl-cq 0506, D/34/4; (b) PB22555, chl-cq 1002, W/14/4; (c) Paratype, PB22556, chl-cq 0515, U/14/2-4; (d) PB22557, chz-pj 0814, Y/17; (e) PB22558, chz-pj 0811, W/39/1; (f) PB22559, chl-cq 0515, J/45/1; (g) PB22560, chl-cq 05d, no England Finder coordinate. Scale bar of 20 μm is for (a–f), and 10 μm is for (g).

Genus Tetraphycus Oehler, 1978 Type species. – Tetraphycus gregalis Oehler, 1978, from c. 1.6 Ga Balbirini Dolomite, McArthur Group at McArthur River locality in Northern Territory, Australia (Oehler, 1978; Jackson et al., 2000). 68

Diagnosis. – Cells spheroidal to slightly polygonal due to mutual compression, 0.4– 5.0 um in diameter. Cell walls psilate to finely granular. Cellular inclusions lacking. Cells commonly in planar tetrads although cross tetrads, diads, and clusters of eight may be present. Tetrads may be isolated or may occur in groups in a single area, set within a common amorphous organic matrix (Oehler, 1978). Tetraphycus laminiformis sp. nov. Fig. 10a–d Holotype. – Specimen illustrated in Fig. 10a, PB22554, ChL-CQ 0506, from the lower Chuanlinggou Formation, Changcheng Group, late Paleoproterozoic. Paratype. – Specimen illustrated in Fig. 10c, PB22556, ChL-CQ 0515, U/14/2-4, from the same material as holotype. Derivation of name. – From the Latin laminiformis – meaning “sheet-like” and referring to the sheet-like geometry of microfossil. Locus typicus. – North China, Tianjin area, Jizhou District, ChangzhoucunQingshanling section. Stratum typicum. – Dark grey mudstone interbedded with thin-bedded fine sandstone of the Chuanlinggou Formation. Material. – 9 specimens preserved as fragmented specimens but clearly showing the geometry of numerous cells, from Changzhougou Formation at Pangjiapu section, and Chuanlinggou Formation at Changzhoucun-Qingshanling section. Diagnosis. – Sheet-like colonies composed of tightly attached tetragonal or angular small cells. Cells are small, smooth-walled, mostly grouped in units of four that are juxtaposed to each other in a planar view. No amorphous organic matrix or sheath present.

69

Dimensions. – Fragmented colonies diameter up to 84 μm; individual cell diameter 2–5 μm (mean = 2.9 μm; N = 69). Remarks. – The distinct feature of cells being grouped predominantly in tetrads in the new species (Fig. 10a–d) supports its attribution to Tetraphycus Oehler, 1978, which is diagnosed by tetrads isolated or occurring in groups within a common organic matrix (Oehler, 1978). Although there is no amorphous organic matrix observed around the new species. The organic matrix maybe previously presented when the organisms were alive but may not survive diagenesis to be preserved organically. The new species differs from other species of Tetraphycus by the arrangement of tetrads or cells in a colony in a single layer and tightly packed (Fig. 10a–d). In contrast, Tetraphycus acinulus has much smaller constituent cells (0.4–1.3 μm) that often appear in pairs, planer tetrads or forming clusters up to 8 cells; Tetraphycus diminutivus also has smaller constituent cells (0.7–1.9 μm) with tetrads closely adpressed forming irregular clusters; Tetraphycus gregalis shows similar cell sizes (1.9–4.1 μm) to the new species here but tetrads inside are closely packed forming irregular clusters; and Tetraphycus major has the same size range of constituent cells (2.2–5.0 μm) but tetrads of it are generally isolated or solitary (Oehler, 1978). It is worth noting that Archaeophycus Wang, Zhang and Luo, 1983 also has constituent cells that are grouped as tetrads, but cells of this genus are typically larger (6–30 μm) (Dong et al., 2009) than that of our specimens (2–5 μm). Some present specimens are preserved in the process of cell division (Fig. 10c), displaying the enlarged spheroidal cells before division, semi-circular cells during or shortly after the binary fission, and tetrads after successive cell divisions. This pattern indicates that the cell division occurred in two planes at right angles resulting in the formation of sheet-like colony.

70

Fig. 11. (a–f) Valeria lophostriata, showing intraspecific variations in vesicle size and wall thickness, and mode of preservation as spheroidal and fusiform-like vesicles. (f1) outline sketch of specimen in (f), marking the internal (yellow) and external (green) wall surface. (f2) detail of wall surface of specimen in (f, f1), showing the smooth external wall surface and equally distant thin striations on the internal surface. (f3) detail of internal wall surface of specimen in (f, f1), showing well preserved concentric striations. (a) PB22561, chz-pj 0813, P/38/1; (b) PB22562, chz-pj 0805, E/28/3; (c) PB22563, chz-pj 0811, M/30/1-3; (d) PB22564, chz-pj 0301, S/29/3; (e) PB22565, chz-pj 0813, F/28/3; (f) PB22566, chz-pj 08a, no England Finder coordinate. Scale bar of 50 μm is for (a–e), and 9 μm is for (f).

71

Genus Valeria Jankauskas, 1982, emend. Nagovitsin, 2009 Type species. – Valeria lophostriata Jankauskas (1979b) 1982, from Middle Riphean Zigazino-Komarovo Formation, Southern Ural Mountains, Russian Federation (Jankauskas, 1979b, 1982). Remarks. – At present, two species of Valeria are well-recognized: V. lophostriata having spheroidal vesicle with concentric pattern of striations, and V. elongata Nagovitsin, 2009 with elongated vesicle and longitudinally arranged striations extending from pole to pole (Nagovitsin, 2009). Valeria lophostriata Jankauskas (1979b), 1982 Fig. 11a–f Synonymy. For synonymy see Jankauskas et al., 1989, Javaux and Knoll, 2017, and additionally: 1995 Foliomorpha striolata sp. nov. – Yan, p. 365, pl. II, fig. 19. 1995 Thecatovalvia annulata gen. et sp. nov. – Yan, p. 364, 369, pl. II, fig. 15. 1995 Valvimorpha annulata sp. nov. – Yan, p. 365, pl. I, fig. 17; pl. III, figs. 1–2. 1997 Valeria lophostriata Jankauskas – Vidal and Moczydłowska-Vidal, fig. 1C. 1997 Valeria lophostriata (Jankauskas, 1979) Jankauskas, 1982 – Samuelsson, p. 181–182, fig. 10B–C. 2007 Valeria lophostriata Jankauskas, 1982 – Javaux, fig. 1.5–1.8. 2007 Valeria lophostriata Jankauskas, 1982 – Yin and Yuan, fig. 1.4. 2008a Valeria lophostriata (Jankauskas, 1979) Jankauskas, 1982 – Moczydłowska, fig. 6C. 2010 Valeria lophostriata Jank. – Nagovitsin et al., p. 1195, fig. 2.11. 2014 Valeria lophostriata – Xiao et al., fig. 6D–H. 2015 Valeria lophostriata – Nagovitsin and Kochnev, fig. 4II–20.

72

2015 Valeria lophostriata – Pang et al., p. 254–255, figs. 3A–H, 6C–E. 2016 Valeria lophostriata Yankauskas, 1982 – Baludikay et al., fig. 7H. 2016 Valeria lophostriata Jankauskas (1979) 1982 – Riedman and Porter, p. 875, fig. 4.1. 2016 Valeria lophostriata (Jankauskas, 1979b) Jankauskas, 1982 – Porter and Riedman, p. 842, fig. 19.1–19.3. 2017 Valeria lophostriata (Jankauskas, 1979b) Jakauskas, 1982 – Javaux and Knoll, p. 218, fig. 7.1–7.4. 2017 Valeria lophostriata – Adam et al., fig. 3D–E. 2017 Valeria lophostriata (Jankauskas, 1979) Jankauskas, 1982 – Agić et al., p. 119, fig. 12I. Material. – More than 100 specimens in various states of preservation from Changzhougou Formation at Pangjiapu section and Chuanlinggou Formation at Changzhoucun-Qingshanling section. Description. – Spheroidal vesicle with well-defined and evenly spaced concentric striations on the internal surface of the wall. Vesicle wall is mostly thick, with smooth outer surface. The pattern of striation is uniform on a single specimen and the width of individual striae is almost equal to or slightly smaller than the distance between two adjacent striae. The originally spheroidal vesicle is preserved often as its halves that are sub-round to fusiform in outline after forming the excystment structure by median split and then splitting apart. Dimensions. – Spheroidal vesicle diameter 73–176 μm (mean = 125.3 μm; N = 15); fusiform vesicle length along long axis 100–237 μm (mean = 164.6 μm; N = 24). Two size-classes of V. lophostriata are recognized by observing the width of individual striae and the distance between two adjacent striae. In one class, the width of striae is

73

0.3–0.4 μm (mean = 0.36 μm; N = 19), and the distance is 0.3–0.4 μm (mean = 0.38 μm; N = 14); in the other class, the width of striae is 0.7–1.3 μm (mean = 0.93 μm; N=32), and the distance is 0.8–1.3 μm (mean = 1 μm; N = 35). Remarks. – V. lophostriata has various preservation morphotypes. When preserved as a whole vesicle, it is round in outline (Fig. 11a–b), or if preserved as a half vesicle after splitting along the excystment structure, it rolled up into fusiform-like vesicle (Fig. 11c–d). Striations observed under optical microscope as parallel dark thin lines, are actually low ridges occurring on the internal surface of the wall (Fig. 11f2, f3). The distinct concentric striations of V. lophostriata make it easy to identify this species even if it is only preserved as a fragment. Microfossils ornamented with such pattern of striations preserved as half vesicles, and ribbon-like fragment from Changzhougou and Chuanlinggou formations in Kuancheng area, were described as new taxa Thecatovalvia annulata, Valvimorpha annulata and Foliomorpha striolata (Yan, 1995), which are all considered synonymous with V. lophostriata. Occurrence and stratigraphic range. – V. lophostriata has a worldwide distribution, and is stratigraphically long ranging taxon from late Paleoproterozoic to Cryogenian. It would be possibly extended up to early Cambrian if the detrital zircon age (518 Ma) of Valeria-bearing Gouhou Formation in North China is confirmed (Tang et al., 2015; He et al., 2017). It has been recorded from late Paleoproterozoic Changcheng Group, late Paleoproterozoic or early Mesoproterozoic Ruyang Group in North China (Yan, 1995; Pang et al., 2015; Agić et al., 2017); c. 1.65 Ga Mallapunyah Formation, c. 1.49 Ga Roper Group and c. 811–716 Ma Alinya Formation in Australia (Javaux, 2007; Riedman and Porter, 2016; Javaux and Knoll, 2017); c. 1.27–0.75 Ga Bylot Supergroup in Canada (Hofmann and Jackson, 1994); late Mesoproterozoic Kamo Group, Mesproterozoic Zigazino-Komarovo Formation, Tonian-Cryogenian

74

Dashkinsky Formation, Tonian Ust'-Kirbin, Chapoma and Karuyarvinskaya formations in Russian Federation (Jankauskas, 1979b, 1982; Pyatiletov, 1980a; Volkova, 1981; Samuelsson, 1997; Khabarov et al., 2002; Pavlov et al., 2002; Nagovitsin, 2009); c. 1.3–1.2 Ga Qaanaaq Formation in Northwest Greenland (Samuelsson et al., 1999); Meso-Neoproterozoic Mbuji-Mayi Supergroup in Democratic Republic of Congo (Baludikay et al., 2016); Tonian-Cryogenian Båtsfjord Formation in Norway (Vidal and Siedlecka, 1983); c. 1.47–1.45 Ga Greyson Formation and c. 0.78–0.74 Ga Chuar Group in USA (Vidal and Ford, 1985; Nagy et al., 2009; Porter and Riedman, 2016; Adam et al., 2017).

Acknowledgements This study was supported by the Strategic Priority Research Program (B) of the Chinese Academy of Sciences (XDB18000000), the National Natural Science Foundation of China, and the Chinese Academy of Sciences for funding LM’s one year study at Uppsala University. Research by MM was granted by the Swedish Research Council (Vetenskapsrådet, VR) through research grant no. 621-2012-1669. We thank Cui Luo and Bing Pan for their assistance in the fieldwork, Limei Feng for her help in laboratory acid maceration, Heda Agić and Milos Bartol for their assistance in SEM preparation.

References Adam, Z.R., Skidmore, M.L., Mogk, D.W., 2016. Paleoenvironmental implications of an expanded microfossil assemblage from the Chamberlain Formation, Belt Supergroup, Montana, in: MacLean, J.S., Sears, J.W. (Eds.), Belt Basin: Window to Mesoproterozoic Earth. Geological Society of America.

75

Adam, Z.R., Skidmore, M.L., Mogk, D.W., Butterfield, N.J., 2017. A Laurentian record of the earliest fossil eukaryotes. Geology 45, 387–390. Agić, H., Moczydłowska, M., Yin, L., 2015. Affinity, life cycle, and intracellular complexity of organic-walled microfossils from the Mesoproterozoic of Shanxi, China. Journal of Paleontology 89, 28–50. Agić, H., Moczydłowska, M., Yin, L., 2017. Diversity of organic-walled microfossils from the early Mesoproterozoic Ruyang Group, North China Craton – A window into the early eukaryote evolution. Precambrian Research 297, 101– 130. Albani, A.E., Bengtson, S., Canfield, D.E., Bekker, A., Macchiarelli, R., Mazurier, A., Hammarlund, E.U., Boulvais, P., Dupuy, J.-J., Fontaine, C., Fürsich, F.T., Gauthier-Lafaye, F., Janvier, P., Javaux, E., Ossa, F.O., Pierson-Wickmann, A.-C., Riboulleau, A., Sardini, P., Vachard, D., Whitehouse, M., Meunier, A., 2010. Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago. Nature 466, 100. Arouri, K., Greenwood, P.F., Walter, M.R. 1999. A possible chlorophycean affinity of some Neoproterozoic acritarchs. Org Geochemistry 30, 1323–1337. Arouri, K., Greenwood, P.F., Walter, M.R. 2000. Biological affinities of Neoproterozoic acritarchs from Australia: microscopic and chemical characterisation. Org Geochemistry 31, 75–89. Baludikay, B.K., Storme, J.Y., François, C., Baudet, D., Javaux, E.J., 2016. A diverse and exquisitely preserved organic-walled microfossil assemblage from the Meso–Neoproterozoic Mbuji-Mayi Supergroup (Democratic Republic of Congo) and implications for Proterozoic biostratigraphy. Precambrian Research 281, 166–184.

76

Beghin, J., Storme, J.-Y., Blanpied, C., Gueneli, N., Brocks, J.J., Poulton, S.W., Javaux, E.J., 2017. Microfossils from the late Mesoproterozoic – early Neoproterozoic Atar/El Mreïti Group, Taoudeni Basin, Mauritania, northwestern Africa. Precambrian Research 291, 63–82. Bengtson, S., Belivanova, V., Rasmussen, B., Whitehouse, M., 2009. The controversial “Cambrian” fossils of the Vindhyan are real but more than a billion years older. Proceedings of the National Academy of Sciences 106, 7729–7734. Bengtson, S., Sallstedt, T., Belivanova, V., Whitehouse, M., 2017. Three-dimensional preservation of cellular and subcellular structures suggests 1.6 billion-year-old crown-group red algae. PLOS Biology 15, e2000735. Berney, C., Pawlowski, J., 2006. A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record. Proceedings of the Royal Society B: Biological Sciences 273, 1867–1872. Brasier, M.D., Antcliffe, J., Saunders, M., Wacey, D., 2015. Changing the picture of Earth's earliest fossils (3.5–1.9 Ga) with new approaches and new discoveries. Proceedings of the National Academy of Sciences. Brenner, W., Foster, C.B., 1994. Chlorophycean algae from the Triassic of Australia. Review of Palaeobotany and Palynology 80, 209–234. Buick, R., 2010. Ancient acritarchs. Nature 463, 885. Butterfield, N.J., 2004. A vaucheriacean alga from the middle Neoproterozoic of Spitsbergen: implications for the evolution of Proterozoic eukaryotes and the Cambrian explosion. Paleobiology 30(2), 231–252. Butterfield, N.J., 2015. Early evolution of the Eukaryota. Palaeontology 58, 5–17.

77

Butterfield, N.J., Chandler, F.W., 1992. Palaeoenvironmental distribution of Proterozoic microfossils, with an example from the Agu Bay Formation, Baffin Island. Palaeontology 35, 943–957. Butterfield, N.J., Knoll, A.H., Swett, K., 1994. Paleobiology of the Neoproterozoic Svanbergfjellet Formation, Spitsbergen. Lethaia 27, 76–76. Chen, J., 1983. A preliminary study on the geological evolution of Sino-Korea Paraplatform during middle to terminal Proterozoic. Geological Review 29 (in Chinese). Cohen, K.M., Finney, S.C., Gibbard, P.L., Fan, J.X., 2013. The ICS International Chronostratigraphic Chart. Episodes 36, 199–204. Cohen, P.A., Macdonald, F.A., 2015. The Proterozoic Record of Eukaryotes. Paleobiology 41, 610-632. Combaz, A., Lange, F.W., Pansart, J., 1967. Les “Leiofusidae” Eisenack, 1938. Review of Palaeobotany and Palynology 1, 291–307 (in French). Cotter, K.L., 1997. Neoproterozoic microfossils from the Officer Basin, Western Australia. Alcheringa: An Australasian Journal of Palaeontology 21, 247-270. Cotter, K.L., 1999. Microfossils from Neoproterozoic Supersequence 1 of the Officer Basin, Western Australia. Alcheringa: An Australasian Journal of Palaeontology 23, 63–86. Couëffé, R., Vecoli, M., 2011. New sedimentological and biostratigraphic data in the Kwahu Group (Meso- to Neo-Proterozoic), southern margin of the Volta Basin, Ghana: Stratigraphic constraints and implications on regional lithostratigraphic correlations. Precambrian Research 189, 155–175.

78

Dale, B., 1983. Dinoflagellate resting cysts, “benthic plankton”, in: Fryxell, G.A. (Ed.), Survival strategies of the algae. Cambridge University Press, Cambridge, pp. 69–136. Dale, B., 2001. The sedimentary record of dinoflagellate cysts: looking back into the future of phytoplankton blooms. Scientia Marina 65, 257–272. Dong, L., Xiao, S., Shen, B., Zhou, C., Li, G., Yao, J., 2009. Basal Cambrian microfossils from the Yangtze Gorges area (South China) and the Aksu area (Tarim Block, Northwestern China). Journal of Paleontology 83(1), 30–44. Douzery, E.J.P., Snell, E.A., Bapteste, E., Delsuc, F., Philippe, H., 2004. The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils? Proc Natl Acad Sci U S A 101, 15386–15391. Downie, C., Sarjeant, W.A.S., 1963. On the interpretation and status of some hystrichosphere genera. Palaeontology 6, 83–96. Du, R., 1982. The discovery of the fossils such as Chuaria in the Qingbaikou System in northwestern Hebei and their significance. Geological Review 28, 1–6 (in Chinese). Du, R., Li, P., Wu, Z., 1979. Sinian Suberathem in the Western Yanshan Ranges. Journal of Shijiazhuang University of Economics, 1–17 (in Chinese). Duan, C., Xing, Y., Du, R., Yin, J., Liu, G., 1985. Macroscopic fossil algae, in: Xing, Y., Duan, C., Liang, Y., Cao, R. (Eds.), Late Precambrian palaeontology of China. Geological Publishing House, Beijing, pp. 68–77 (in Chinese). Edwards, L.E., 1993. Dinoflagellates, in: Lipps, J.H. (Ed.). Fossil prokaryotes and protists. Blackwell Scientific Publications, Oxford, pp. 105–140. Eisenack, A., 1937. Neue Mikrofossilien des baltischen Silurs. IV. Paleonto-logisch Zeitschrift 19, 217–243 (in German).

79

Eisenack, A., 1955. Chitinozoen, Hystrichospharen un andere Mikrofossilien aus dem Beyrichia-Kalk. Senckenbergiana Lethaea 36, 157–188 (in German). Eisenack, A., 1958. Tasmanites Newton 1875 und Leiosphaeridia n. g. als Gattungen der Hystrichosphaeridea. Palaeontographica, Abteilung A. 110, 1–19 (in German). Eisenack, A. 1965. Mikrofossilien aus den Silur Gotlands. Hystrichospharen, Problematika. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 122(3), 257–274 (in German). Eisenack, A., 1976. Mikrofossilien aus dem Vaginatenkalk von Hälludden, Öland. Palaeontographica, Abteilung A. 154, 181–203 (in German). Eisenack, A., Cramer, F.H., Díez, M., 1979. Katalog der fossilen Dinoflagellaten, Hystrichosphären und verwandten Mikrofossilien. Band VI Acritarcha 3/2. E. Schweizerbart'sche Verlagsbuchhandlung, Stuttgart. Eme, L., Sharpe, S.C., Brown, M.W., Roger, A.J., 2014. On the age of eukaryotes: evaluating evidence from fossils and molecular clocks, Cold Spring Harbor perspectives in biology. Evitt, W.R., 1985. Sporopollenin dinoflagellate cysts. Their morphology and interpretations. American Association of Stratigraphic Palynologists Foundation, College Station, Texas. Fatka, O., Brocke, R., 2008. Morphological variability and method of opening of the Devonian acritarch Navifusa bacilla (Deunff, 1955) Playford, 1977. Review of Palaeobotany and Palynology 148, 108–123. Fensome, R.A., Williams, G.L., Barss, J.M., Freeman, J.M., Hill, J.M., 1990. Acritarchs and fossil prasinophytes: An index to genera, species and

80

infraspecific taxa. American Association of Stratigraphic Palynologists, Contributions Series 25, 1–771. Gao, L., Zhang, C., Liu, P., Tang, F., Song, B., Ding, X., 2009. Reclassification of the Meso- and Neoproterozoic Chronostratigraphy of North China by SHRIMP Zircon Ages. Acta Geologica Sinica – English Edition 83, 1074–1084. Gao, L., Zhang, C., Shi, X., Song, B., Wang, Z., Liu, Y., 2008a. Mesoproterozoic age for Xiamaling Formation in North China Plate indicated by zircon SHRIMP dating. Chinese Science Bulletin 53, 2665–2671. Gao, L., Zhang, C., Yin, C., Shi, X., Wang, Z., Liu, Y., Liu, P., Tang, F., Song, B., 2008b. SHRIMP zircon ages: basis for refining the Chronostraigraphic Classification of the Meso- and Neoproterozoic Strata in North China Old Land. Acta Geoscientica Sinica 29, 366–376 (in Chinese). Golovenok, V.K., Belova, M.Y., 1984. Riphean microbiota in cherts of the Billyakh Group on the Anabar Uplift. Palentological Journal 4, 20–30. Golovenok, V.K., Belova, M.Y., 1986. The Riphean microflora in the cherts from the Malgin Formation in the Yudoma-Maya basin. Paleontological Journal 2, 85– 90. Golubkova, E.Y., Raevskaya, E.G., Kuznetsov, A.B., 2010. Lower Vendian microfossil assemblages of East Siberia: Significance for solving regional stratigraphic problems. Stratigraphy and Geological Correlation 18, 353–375. Graham, L.E., Graham, J.M., Wilcox, L.W., 2009. Algae. 2 nd ed. Benjamin Cummings, San Francisco. Grey, K., 2005. Ediacaran palynology of Australia. Memoirs of the Association of Australiasian Palaeontologists 31, 1–439.

81

Grey, K., Willman, S., 2009. Taphonomy of Ediacaran acritarchs from Australia: significance for taxonomy and biostratigraphy. Palaios 24(3/4), 239–256. Guy-Ohlson, D., 1996. Prasinophycean algae, in: Jansonius, J., McGregor, D.C. (Eds.). Palynology: principles and Applications. Volume 1. American Association of Stratigraphic Palynologists Foundation, Salt Lake City, pp. 181–189. Han, T.-M., Runnegar, B., 1992. Megascopic Eukaryotic Algae from the 2.1-BillionYear-Old Negaunee Iron-Formation, Michigan. Science 257, 232–235. He, T., Zhou, Y., Vermeesch, P., Rittner, M., Miao, L., Zhu, M., Carter, A., Pogge von Strandmann, P.A.E., Shields, G.A., 2017. Measuring the ‘Great Unconformity’ on the North China Craton using new detrital zircon age data. Geological Society, London, Special Publications 448, 145–159. He, Y., Zhao, G., Sun, M., Xia, X., 2009. SHRIMP and LA-ICP-MS zircon geochronology of the Xiong’er volcanic rocks: Implications for the PaleoMesoproterozoic evolution of the southern margin of the North China Craton. Precambrian Research 168, 213–222. He, Z., Niu, B., Zhang, X., Zhao, L., Liu, R., 2011. Discovery of the paleo-weathered mantle of the rapakivi granite covered by the Proterozoic Changzhougou Formation in the Miyun area, Beijing and their detrital zircon dating. Geological Bulletin of China 30(5), 798–802 (in Chinese). Hedges, S.B., Blair, J.E., Venturi, M.L., Shoe, J.L., 2004. A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evolutionary Biology 4, 2.

82

Hofmann, H.J., Chen, J., 1981. Carbonaceous megafossils from the Precambrian (1800Ma) near Jixian, northern China. Canadian Journal of Earth Sciences 18, 443–447. Hofmann, H.J., Jackson, G.D., 1991. Shelf-facies microfossils from the Uluksan Group (Proterozoic Bylot Supergroup), Baffin Island, Canada. Journal of Paleontology 65, 361–382. Hofmann, H.J., Jackson, G.D., 1994. Shale-Facies Microfossils from the Proterozoic Bylot Supergroup, Baffin Island, Canada. Memoir (The Paleontological Society) 37, 1–39. Horodyski, R.J., 1980. Middle Proterozoic Shale-Facies Microbiota from the Lower Belt Supergroup, Little Belt Mountains, Montana. Journal of Paleontology 54, 649–663. Horodyski, R.J., Allan Donaldson, J., 1980. Microfossils from the Middle Proterozoic Dismal Lakes Groups, Arctic Canada. Precambrian Research 11, 125–159. Hu, G., Zhao, T., Zhou, Y., 2014. Depositional age, provenance and tectonic setting of the Proterozoic Ruyang Group, southern margin of the North China Craton. Precambrian Research 246, 296–318. Hu, Y., Fu, J., 1982. Micropalaeoflora from the Gaoshanhe Formation of late Precambrian of Luonan, Shaanxi and its stratigraphic significance. Bulletin of the Xi'an Institute of Geology and Mineral Resources, Chinese Academy of Geological Science 4, 102–113 (in Chinese). Inouye, I., Hori, T., Chihara, M., 1990. Absolute configuration of the flagellar apparatus of Pterosperma cristatum (Prasinophyceae) and consideration of its phylogenetic position. Journal of Phycology 26, 329–344.

83

Jackson, M.J., Southgate, P.N., Page, R.W., 2000. Gamma-Ray Logs and U-Pb Zircon Geochronology—Essential Tools to Constrain Lithofacies Interpretation of Paleoproterozoic Depositional Systems, in: Grotzinger, J.P., James, N.P. (Eds.). SEPM Society for Sedimentary Geology. Jankauskas, T.V., 1979a. The Lower Riphean microbiota of the southern Urals. Proceedings of the USSR Academy of Sciences 247, 1465–1467 (in Russian). Jankauskas, T.V., 1979b. Middle Riphean microbiota from the southern Urals and the Bashkirian Urals. Proceedings of the USSR Academy of Sciences 248, 190– 193 (in Russian). Jankauskas, T.V., 1980. Shishenyakaya microbiota of the upper Riphean of the southern Urals. Proceedings of the USSR Academy of Sciences 251, 190–192 (in Russian). Jankauskas, T.V., 1982. Microfossils of the Riphean of the Southern Urals, in: Keller, B.M. (Ed.), Stratotype of the Riphean: Paleontology and Paleomagnetics. Nauka, Moscow, pp. 84–120 (in Russian). Jankauskas, T.V., Mikhailova, N.S., German, T.N., Sergeev, V.N., Abduazimova, Z.M., Belova, M.Y., Burzin, M.B., Veis, A.F., Volkova, N.A., Golovionok, V.K., Grigorijeva, A.Y., Kirjanov, V.V., Kozlova, Y.V., Kolosov, P.N., Kraskov, L.N., Krylov, I.N., Luchinina, V.A., Medvedeva, A.M., Oqurizova, R.N., Paskiavichene, L.T., Piatiletov, V.G., Rudavskaya, V.A., Siverizeva, I.A., Stanevich, A.M., Treshchetenkova, A.A., Faizulina, Z.K., Chepikova, I.K., Shenfil, V.Yu., Shepeleva, E.D., Yakshin M.S., 1989. Precambrian Microfossils of the USSR. Nauka, Leningrad (in Russian).

84

Javaux, E.J., 2007. The Early Eukaryotic Fossil Record, in: Jékely, G. (Ed.), Eukaryotic Membranes and Cytoskeleton: Origins and Evolution. Springer New York, New York, NY, pp. 1–19. Javaux, E.J., Knoll, A.H., 2017. Micropaleontology of the lower Mesoproterozoic Roper Group, Australia, and implications for early eukaryotic evolution. Journal of Paleontology 91, 199–229. Javaux, E.J., Knoll, A.H., Walter, M.R., 2001. Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412, 66–69. Javaux, E.J., Knoll, A.H., Walter, M. R., 2003. Recognizing and Interpreting the Fossils of Early Eukaryotes. Origins of life and evolution of the biosphere 33, 75–94. Javaux, E.J., Knoll, A.H., Walter, M. R., 2004. TEM evidence for eukaryotic diversity in mid-Proterozoic oceans. Geobiology 2(3), 121–132. Javaux, E.J., Lepot, K., 2018. The Paleoproterozoic fossil record: Implications for the evolution of the biosphere during Earth's middle-age. Earth-Science Reviews 176, 68–86. Javaux, E.J., Marshall, C.P., Bekker, A., 2010. Organic-walled microfossils in 3.2billion-year-old shallow-marine siliciclastic deposits. Nature 463, 934-938. Kaźmierczak, J., 1979. The eukaryotic nature of Eosphaera-like ferriferous structures from the Precambrian Gunflint Iron Formation, Canada: A comparative study. Precambrian Research 9, 1–22. Khabarov, E.M., Ponomarchuk, V.A., Morozova, I.P., 2002. Strontium isotopic evidence for supercontinental breakup and formation in the Riphean: Western margin of the Siberian craton. Russian Journal of Earth Sciences 4, 259–269.

85

Knoll, A.H., 2014. Paleobiological Perspectives on Early Eukaryotic Evolution. Cold Spring Harbor Perspectives in Biology 6. Knoll, A.H., Javaux, E.J., Hewitt, D., Cohen, P., 2006. Eukaryotic Organisms in Proterozoic Oceans. Philosophical Transactions: Biological Sciences 361, 1023–1038. Knoll, A.H., Walter, M.R., Narbonne, G.M., Christie-Blick, N., 2004. A New Period for the Geologic Time Scale. Science 305, 621–622. Kuznetsov, A.B., Ovchinnikova, G.V., Semikhatov, M.A., Gorokhov, I.M., Kaurova, O.K., Krupenin, M.T., Vasil’eva, I.M., Gorokhovskii, B.M., Maslov, A.V., 2008. The Sr isotopic characterization and Pb-Pb age of carbonate rocks from the Satka formation, the Lower Riphean Burzyan Group of the southern Urals. Stratigraphy and Geological Correlation 16, 120–137. Laflamme, M., Darroch, S.A.F., Tweedt, S.M., Peterson, K.J., Erwin, D.H., 2013. The end of the Ediacara biota: Extinction, biotic replacement, or Cheshire Cat? Gondwana Research 23, 558–573. Lamb, D.M., Awramik, S.M., Chapman, D.J., Zhu, S., 2009. Evidence for eukaryotic diversification in the ∼1800 million-year-old Changzhougou Formation, North China. Precambrian Research 173, 93–104. Lamb, D.M., Awramik, S.M., Zhu, S., 2007. Paleoproterozoic compression-like structures from the Changzhougou Formation, China: Eukaryotes or clasts? Precambrian Research 154, 236–247. Lan, Z., Li, X., Chen, Z.-Q., Li, Q., Hofmann, A., Zhang, Y., Zhong, Y., Liu, Y., Tang, G., Ling, X., Li, J., 2014. Diagenetic xenotime age constraints on the Sanjiaotang Formation, Luoyu Group, southern margin of the North China

86

Craton: Implications for regional stratigraphic correlation and early evolution of eukaryotes. Precambrian Research 251, 21–32. Lenton, T.M., Watson, A.J., 2011. Revolutions that made the Earth. Oxford University Press. Li, H., Lu, S., Su, W., Xiang, Z., Zhou, H., Zhang, Y., 2013. Recent advances in the study of the Mesoproterozoic geochronology in the North China Craton. Journal of Asian Earth Sciences 72, 216–227. Li, H., Su, W., Zhou, H., Geng, J., Xiang, Z., Cui, Y., Liu, w., Lu, S., 2011. The base age of the Changchengian System at the northern North China Craton should be younger than 1670 Ma: constraints from zircon U-Pb LA-MC-ICP-MS dating of a granite-porphyry dike in Miyun County, Beijing. Earth Science Frontiers 18, 108–120 (in Chinese). Li, H., Su, W., Zhou, H., Xiang, Z., Tian, H., Yang, L., Huff, W.D., Ettensohn, F.R., 2014. The first precise age constraints on the Jixian System of the Meso- to Neoproterozoic Standard Section of China: SHRIMP zircon U-Pb dating of bentonites from the Wumishan and Tieling formations in the Jixian Section, North China Craton. Acta Petrologica Sinica 30, 2999–3012 (in Chinese). Li, H., Zhu, S., Xiang, Z., Su, W., Lu, S., Zhou, H., Geng, J., Li, S., Yang, F., 2010. Zircon U-Pb dating on tuff bed from Gaoyuzhuang Formation in Yanqing, Beijing: Further constraints on the new subdivision of the Mesoproterozoic stratigraphy in the northern North China Craton. Acta Petrologica Sinica 26, 2131–2140 (in Chinese). Liu, Y., Kuang, H., Meng, X., Ge, M., Cai, G., 2005. The Neoproterozoic stratigraphic correlation framework in the Jilin-Liaoning-Xuzhou-Huaiyang area. Journal of Stratigraphy 29, 387–396+404 (in Chinese).

87

Loron, C., Moczydłowska, M., 2017. Tonian (Neoproterozoic) eukaryotic and prokaryotic organic-walled microfossils from the upper Visingsö Group, Sweden. Palynology, 1–35. Luo, Q., Zhang, Y., Sun, S., 1985. The eukaryotes in the basal Changcheng System of Yanshan Ranges. Acta Geologica Sinica, 12–16 (in Chinese). Luo, Q., Zhang, Y., Sun, S., 1986. Research on the Middle-Late Proterozoic microplants in Kuancheng area, Hebei Province. Precambrian Geology, 457– 476 (in Chinese). Lyons, T.W., Reinhard, C.T., Planavsky, N.J., 2014. The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506, 307. Ma, K., Hu, S., Wang, T., Zhang, B., Qin, S., Shi, S., Wang, K., Huang, Q., 2017. Sedimentary environments and mechanisms of organic matter enrichment in the Mesoproterozoic Hongshuizhuang Formation of northern China. Palaeogeography, Palaeoclimatology, Palaeoecology 475, 176–187. Margulis, L., Corliss, J.O., Melkonian, M., Chapman, D.J., 1989. Handbook of Protoctista. Jones and Bartlett Publishers, Boston. Mendelson, C.V., Schopf, J.W., 1992. Proterozoic and selected early Cambrian microfossils and microfossil-like objects, in: Schopf, J.W., Klein, C. (Eds.), The Proterozoic biosphere. Cambridge University Press, Cambridge, pp. 865– 952. Mikhailova, N.S., 1986. New finds of the microfossils from the Upper Riphean deposits of the Krasnoyarsk region, in: Sokolov, B.S. (Ed.), Current Problems of Modern Paleoalgology. Nauka, Kiev, pp. 31–37 (in Russian). Moczydłowska, M., 2008a. The Ediacaran microbiota and the survival of Snowball Earth conditions. Precambrian Research 167, 1–15.

88

Moczydłowska, M., 2008b. New records of late Ediacaran microbiota from Poland. Precambrian Research 167, 71–92. Moczydłowska, M., 2015. Algal affinities of Ediacaran and Cambrian organic-walled microfossils with internal reproductive bodies: Tanarium and other morphotypes, Palynology, DOI: 10.1080/01916122.2015.1006341 Moczydłowska, M., Landing, E.D., Zang, W., Palacios, T., 2011. Proterozoic phytoplankton and timing of Chlorophyte algae origins. Palaeontology 54, 721–733. Moczydłowska, M., Pease, V., Willman, S., Wickström, L., Agić, H., 2017. A Tonian age for the Visingsö Group in Sweden constrained by detrital zircon dating and biochronology: implications for evolutionary events. Geological Magazine, 1–15. Moczydłowska, M., Schopf, J.W., Willman, S., 2010. Micro- and nano-scale ultrastructure of cell walls in Cryogenian microfossils: revealing their biological affinity. Lethaia 43, 129–136. Moczydłowska, M., Willman, S., 2009. Ultrastructure of cell walls in ancient microfossils as a proxy to their biological affinities. Precambrian Research 173, 27–38. Muir, M.D., 1976. Proterozoic microfossils from the Amelia dolomite, Mcarthur Basin, Northern Territory. Alcheringa: An Australasian Journal of Palaeontology 1(2), 143–158. Nagovitsin, K., 2009. Tappania-bearing association of the Siberian platform: Biodiversity, stratigraphic position and geochronological constraints. Precambrian Research 173, 137–145.

89

Nagovitsin, K.E., Kochnev, B.B., 2015. Microfossils and biofacies of the Vendian fossil biota in the southern Siberian Platform. Russian Geology and Geophysics 56, 584–593. Nagy, R.M., Porter, S.M., Dehler, C.M., Shen, Y., 2009. Biotic turnover driven by eutrophication before the Sturtian low-latitude glaciation. Nature Geosci 2, 415–418. Oehler, D.Z., 1978. Microflora of the middle Proterozoic Balbirini Dolomite (McArthur Group) of Australia. Alcheringa: An Australasian Journal of Palaeontology 2, 269–309. Pang, K., Tang, Q., Yuan, X., Wan, B., Xiao, S., 2015. A biomechanical analysis of the early eukaryotic fossil Valeria and new occurrence of organic-walled microfossils from the Paleo-Mesoproterozoic Ruyang Group. Palaeoworld 24, 251–262. Parfrey, L.W., Lahr, D.J.G., Knoll, A.H., Katz, L.A., 2011. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci U S A 108, 13624–13629. Pavlov, V.E., Gallet, Y., Petrov, P.U., Zhuravlev, D.Z., Shatsillo, A.V., 2002. The Ui Group and Late Riphean Sills in the Uchur–Maya Area: Isotope and Paleomagnetic Data and the Problem of the Rodinia Supercontinent. Geotectonics 36, 278–292. Peat, C.J., Muir, M.D., Plumb, K.A., McKirdy, D.M., Norvick, M.S., 1978. Proterozoic microfossils from the Roper Group, Northern Territory, Australia. BMR Journal of Australian Geology and Geophysics 3, 1–17.

90

Peng, P., Liu, F., Zhai, M., Guo, J., 2012. Age of the Miyun dyke swarm: Constraints on the maximum depositional age of the Changcheng System. Chinese Science Bulletin 57, 105–110. Peng, Y., Bao, H., Yuan, X., 2009. New morphological observations for Paleoproterozoic acritarchs from the Chuanlinggou Formation, North China. Precambrian Research 168, 223–232. Pietrzak-Renaud, N., Davis, D., 2014. U–pb geochronology of baddeleyite from the Belleview metadiabase: Age and geotectonic implications for the Negaunee Iron Formation, Michigan. Precambrian Research 250(3), 1–5. Planavsky, N.J., Asael, D., Hofmann, A., Reinhard, C.T., Lalonde, S.V., Knudsen, A., Wang, X., Ossa Ossa, F., Pecoits, E., Smith, A.J.B., Beukes, N.J., Bekker, A., Johnson, T.M., Konhauser, K.O., Lyons, T.W., Rouxel, O.J., 2014. Evidence for oxygenic photosynthesis half a billion years before the Great Oxidation Event. Nature Geoscience 7, 283. Porter, S.M., Riedman, L.A., 2016. Systematics of organic-walled microfossils from the ca. 780–740 Ma Chuar Group, Grand Canyon, Arizona. Journal of Paleontology 90, 815–853. Poulton, S.W., Fralick, P.W., Canfield, D.E., 2010. Spatial variability in oceanic redox structure 1.8 billion years ago. Nature Geoscience 3, 486. Prasad, B., Uniyal, S.N., Asher, R., 2005. Organic-walled microfossils from the Proterozoic Vindhyan Supergroup of Son Valley, Madhya Pradesh, India. The Palaeobotanist 54, 13–60. Pyatiletov, V.G., 1980a. Mikrofossilii iz pozdnedokembriyskikh otlozheniy, vskrytykh Vanavarskoy skvazhnoy (zapadnaya chast' Sibirskoy platformy), in: Khomentovskiy, V.V., Pyatiletov, V.G., Karlova, G.A. (Eds.), N ovye

91

dannyep o stratigrafipi ozdnegod okembriya zapada Sibirskoy platformy i ee skladchatogo obramleniya. Sbornik Nauchnykh Trudov, Akademiya Nauk SSSR, Sibirskoe Otdeleniye, Novosibirsk, pp. 71–76 (in Russian). Pyatiletov, V.G., 1980b. On finds of microfossils of the genus Navifusa in the Lakhanda Formation. Palaeontological Journal 180, 143–145 (in Russian). Rasmussen, B., Bose, P.K., Sarkar, S., Banerjee, S., Fletcher, I.R., McNaughton, N.J., 2002. 1.6 Ga U-Pb zircon age for the Chorhat Sandstone, lower Vindhyan, India: Possible implications for early evolution of animals. Geology 30, 103– 106. Raven, P.H., Evert, R.F., Eichhorn, S.E., 2005. Biology of plants. W.H. Freeman and Company Publishers, New York. Ray, J.S., Martin, M.W., Veizer, J.n., Bowring, S.A., 2002. U-Pb zircon dating and Sr isotope systematics of the Vindhyan Supergroup, India. Geology 30, 131–134. Retallack, G.J., 2015. Acritarch Evidence for an Ediacaran Adaptive Radiation of Fungi. Botanica Pacifica: a journal of plant science and conservation 4, 19-33. Riedman, L.A., Porter, S., 2016. Organic-walled microfossils of the midNeoproterozoic Alinya Formation, Officer Basin, Australia. Journal of Paleontology 90, 854–887. Riedman, L.A., Sadler, P.M., 2017. Global species richness record and biostratigraphic potential of early to middle Neoproterozoic eukaryote fossils. Precambrian Research. Runnegar, B., 1994. Proterozoic eukaryotes: evidence frombiology and geology, in: Bengtson, S. (Ed.). Early life on Earth. Nobel Symposium No. 84. Columbia University Press, New York, pp. 287–297.

92

Samuelsson, J., 1997. Biostratigraphy and palaeobiology of early Neoproterozoic strata of the Kola Peninsula, Northwest Russia. Norsk Geologisk Tidsskrift 77, 165. Samuelsson, J., Dawes, P.R., Vidal, G., 1999. Organic-walled microfossils from the Proterozoic Thule Supergroup, Northwest Greenland. Precambrian Research 96, 1–23. Sánchez-Baracaldo, P., Raven, J.A., Pisani, D., Knoll, A.H., 2017. Early photosynthetic eukaryotes inhabited low-salinity habitats. Proceedings of the National Academy of Sciences 114, E7737–E7745. Sarangi, S., Gopalan, K., Kumar, S., 2004. Pb–Pb age of earliest megascopic, eukaryotic alga bearing Rohtas Formation, Vindhyan Supergroup, India: implications for Precambrian atmospheric oxygen evolution. Precambrian Research 132, 107–121. Schopf, J.W., 1968. Microflora of the Bitter Springs Formation, Late Precambrian, Central Australia. Journal of Paleontology 42, 651–688. Schopf, J.W., 1970. Electron Microscopy of Organically Preserved Precambrian Microorganisms. Journal of Paleontology 44, 1–6. Schopf, J.W., Klein, C., 1992. The Proterozoic Biosphere: A Multidisciplinary Study. Cambridge University Press, Cambridge. Semikhatov, M.A., Kuznetsov, A.B., Chumakov, N.M., 2015. Isotope age of boundaries between the general stratigraphic subdivisions of the Upper Proterozoic (Riphean and Vendian) in Russia: The evolution of opinions and the current estimate. Stratigraphy and Geological Correlation 23, 568–579. Semikhatov, M.A., Ovchinnikova, G.V., Gorokhov, I., Kuznetsov, A.B., Vasil'eva, I.M., Gorokhovskii, B.M., Podkovyrov, V.N., 2000. Isotope Age of the

93

Middle-Upper Riphean Boundary: Pb-Pb Geochronology of the Lakhanda Group Carbonates, Eastern Siberia. Doklady Earth Sciences 372, 625–629. Semikhatov, M.A., Shurkin, K.A., Aksenov, Y.M., Bekker, Y.R., Bibikova, Y.V., Duk, V.L., Yesipchuk, K.Y., Karsakov, L.P., Kiselev, V.V., Kozlov, V.L., Lobach-Zhuchenko, S.B., Negrutsa, V.Z., Robonen, V.I., Sez'ko, A.I., Filatova, L.I., Khomentovskiy, V.V., Shemyakin, V.M., Shul' diner, V.I., 1991. A new stratigraphic scale for the Precambrian of the USSR. International Geology Review 33, 413–422. Sergeev, V.N., Knoll, A.H., Vorob’eva, N.G., 2011. Ediacaran Microfossils from the Ura Formation, Baikal-Patom Uplift, Siberia: Taxonomy and Biostratigraphic Significance. Journal of Paleontology 85, 987–1011. Sergeev, V.N., Knoll, A.H., Vorob’eva, N.G., Sergeeva, N.D., 2016. Microfossils from the lower Mesoproterozoic Kaltasy Formation, East European Platform. Precambrian Research 278, 87–107. Sergeev, V.N., Vorob’eva, N.G., Yu. Petrov, P., 2017. The biostratigraphic conundrum of Siberia: Do true Tonian–Cryogenian microfossils occur in Mesoproterozoic rocks? Precambrian Research 299, 282–302. Sharma, M., Shukla, Y., 2009. Taxonomy and affinity of Early Mesoproterozoic megascopic helically coiled and related fossils from the Rohtas Formation, the Vindhyan Supergroup, India. Precambrian Research 173, 105–122. Shi, M., Feng, Q., Khan, M.Z., Awramik, S., Zhu, S., 2017a. Silicified microbiota from the Paleoproterozoic Dahongyu Formation, Tianjin, China. Journal of Paleontology 91, 369–392.

94

Shi, M., Feng, Q., Khan, M.Z., Zhu, S., 2017b. An eukaryote-bearing microbiota from the early mesoproterozoic Gaoyuzhuang Formation, Tianjin, China and its significance. Precambrian Research 303, 709–726. Singh, V.K., Sharma, M., 2014. Morphologically complex organic-walled microfossils (OWM) from the late Palaeoproterozoic-early Mesoproterozoic Chitrakut Formation, Vindhyan Supergroup, central India and their implications on the antiquity of eukaryotes. Journal of the Palaeontological Society of India 59, 89–102. Staplin, F.L., Jansonius, J., Pocock, S.A.J., 1965. Evaluation of some acritarchous hystrichosphere genera. Neues Jahrbuch für Geologie und Paläeontologie Abhandlungen 123, 167–201. Strother, P.K., Wellman, C.H., 2016. Palaeoecology of a billion-year-old non-marine cyanobacterium from the Torridon Group and Nonesuch Formation. Palaeontology 59, 89–108. Sun, S., 1989. Microflora of lower series of the Changcheng System in Kuancheng County, Hebei Province, China. Scientia Geologica Sinica 3, 235–243 (in Chinese). Sun, S., 2006. Microplants of the Mesoproterozic-Neoproterozoic Erathem in Jixian, China. Geological Publishing House, Beijing (in Chinese). Tang, Q., Hughes, N.C., McKenzie, N.R., Myrow, P.M., Xiao, S., 2017. Late Mesoproterozoic – early Neoproterozoic organic-walled microfossils from the Madhubani Group of the Ganga Valley, northern India. Palaeontology 60, 869–891.

95

Tang, Q., Pang, K., Yuan, X., Wan, B., Xiao, S., 2015. Organic-walled microfossils from the Tonian Gouhou Formation, Huaibei region, North China Craton, and their biostratigraphic implications. Precambrian Research 266, 296–318. Tappan, H., 1980. The paleobiology of plant protists. WH Freeman, San Francisco, California. Tian, S., Zhai, Z., 1996. Stratigraphy (Lithostratic) of the municipality of Tianjin. China University of Geosciences Press, Wuhan (in Chinese). Tien, C., 1923. Stratigraphy and Palaeontology of the Sinian Rocks of Nankou. Bulletin of the Geological Society of China 2, 105–109. Timofeev, B.V., 1959. The oldest flora of the Baltic region and its stratigraphic significance. Trudy VNIGRI, Leningrad (in Russian). Timofeev, B.V., 1966. Micropaleophytological investigation into ancient formations. Nauka, Moscow (in Russian). Timofeev, B.V., 1969. Proterozoic spheromorphida. Nauka, Leningrad. Timofeev, B.V., Hermann, T.N., Mikhailova, N.S., 1976. Plant Microfossils of the Precambrian, Cambrian, and Ordovician. Nauka, Leningrad (in Russian). Turner, R.E., 1984. Acritarchs from the type area of the Ordovician Caradoc Series, Shropshire, England. Palaeontolgraphica, Abteilung B 190, 87–157. Vidal, G., 1988. A Palynological Preparation Method. Palynology 12, 215–220. Vidal, G., Ford, T.D., 1985. Microbiotas from the late Proterozoic Chuar Group (northern Arizona) and Uinta Mountain Group (Utah) and their chronostratigraphic implications. Precambrian Research 28, 349–389. Vidal, G., Moczydłowska, M., Rudavskaya, V.A., 1993. Biostratigraphical implications of a Chuaria-Tawuia assemblage and associated acritarchs from the Neoproterozoic of Yakutia. Palaeontology 36, 387–402.

96

Vidal, G., Moczydłowska-Vidal, M., 1997. Biodiversity, Speciation, and Extinction Trends of Proterozoic and Cambrian Phytoplankton. Paleobiology 23, 230– 246. Vidal, G., Siedlecka, A., 1983. Planktonic, acid-resistant microfossils from the upper Proterozoic strata of the Barents Sea region of Varanger Peninsula, East Finnmark, northern Norway. Norges Geologiske Undersøkelse Bulletin 382, 45. Volkova, N.A., 1981. Akritarkh verkhnego Dokembriia iugovostochnoi Sibiri (Ustkirbinskaia svita). Biulleten Moskovskogo Obshchestva Ispytatelei Prirody Otdel Geologicheskii 56, 66–75 (in Russian). Vorob’eva, N.G., Sergeev, V.N., Knoll, A.H., 2009. Neoproterozoic Microfossils from the Northeastern Margin of the East European Platform. Journal of Paleontology 83, 161–196. Vorob’eva, N.G., Sergeev, V.N., Petrov, P.Y., 2015. Kotuikan Formation assemblage: A diverse organic-walled microbiota in the Mesoproterozoic Anabar succession, northern Siberia. Precambrian Research 256, 201–222. Vorob’eva, N.G., Sergeev, V.N., Semikhatov, M.A., 2006. Unique lower Vendian Kel’tma microbiota, Timan ridge: New evidence for the paleontological essence and global significance of the Vendian system. Doklady Earth Sciences 410, 1038–1043. Walter, M.R., Oehler, J.H., Oehler, D.Z., 1976. Megascopic Algae 1300 Million Years Old from the Belt Supergroup, Montana: A Reinterpretation of Walcott's Helminthoidichnites. Journal of Paleontology 50, 872–881.

97

Wang, C., Liu, P., Zhang, S., Shang, X., 2015a. Discussion on the relationship between the Ediacaran Schizofusa and Leiosphaeridia (acritarchs). Acta Micropalaeontologica Sinica 32, 75–82 (in Chinese). Wang, F., Zhang, X., Guo, R., 1983. The Sinian microfossils from Jinning, Yunnan, south west China. Precambrian Research 23(2), 133–175. Wang, J., Wang, X., Deng, S., Lu, X., Tian, Y., Xu, H., Li, X., Li, S., Chen, Y., Yang, Y., Zhang, C., Xu, J., 1996. Stratigraphy (Lithostratic) of Hebei Province. China University of Geosciences Press, Wuhan (in Chinese). Wang, W., Liu, S., Santosh, M., Deng, Z., Guo, B., Zhao, Y., Zhang, S., Yang, P., Bai, X., Guo, R., 2015b. Late Paleoproterozoic geodynamics of the North China Craton: Geochemical and zircon U-Pb-Hf records from a volcanic suite in the Yanliao rift. Gondwana Research 27, 300–325. Wang, Y., Wang, Y., Du, W., 2016. The long-ranging macroalga Grypania spiralis from the Ediacaran Doushantuo Formation, Guizhou, South China. Alcheringa: An Australasian Journal of Palaeontology 40, 303–312. Waterbury, J.B., Stanier, R.Y., 1978. Patterns of growth and development in pleurocapsalean cyanobacteria. Microbiol Rev 42, 2–44. Wicander, R., 2007. Acritarchs and Prasinophyte Phycomata. Short Course, CIMP Lisbon' 07, Joint Meeting of Spore/Pollen and Acritarch Subcommissions, Lisbon (Portugal): INETI. Xiao, S., Knoll, A.H., Kaufman, A.J., Yin, L., Zhang, Y., 1997. Neoproterozoic fossils in Mesoproterozoic rocks? Chemostratigraphic resolution of a biostratigraphic conundrum from the North China Platform. Precambrian Research 84, 197–220.

98

Xiao, S., Narbonne, G.M., Zhou, C., Laflamme, M., Grazhdankin, D.V., Moczydłowska-Vidal, M., Cui, H., 2016. Towards an Ediacaran time scale: problems, protocols, and prospects. Episodes 39, 540–555. Xiao, S., Shen, B., Tang, Q., Kaufman, A.J., Yuan, X., Li, J., Qian, M., 2014. Biostratigraphic and chemostratigraphic constraints on the age of early Neoproterozoic carbonate successions in North China. Precambrian Research 246, 208–225. Xing, Y., Duan, C., Liang, Y., Cao, R., 1985. Late Precambrian palaeontology of China. Geological Publishing House, Beijiing (in Chinese). Xing, Y., Liu, G., 1973. On Sinian micro-flora in Yenliao region of China and its geological significance. Acta Geologica Sinica, 1–64 (in Chinese). Xing, Y., Liu, G., 1982. Late Precambrian microflora of China and its stratigraphical significance. Bulletin of Chinese Academy of Geological Society 4, 55–67 (in Chinese). Yan, Y., 1982. Schizofusa from the Chuanlinggou Formation of Changcheng System in Jixian County. Bulletin of the Tianjin Institute of Geology and Mineral Resources 6, 1–7 (in Chinese). Yan, Y., 1985. Preliminary research on microflora from Chuanlinggou Formation of Changcheng System in Jixian County. Bulletin of the Tianjin Institute of Geology and Mineral Resources 12, 137–168 (in Chinese). Yan, Y., 1989. Shale-facies algal filaments from Chuanlinggou Formation in Jixian County. Bulletin of the Tianjin Institute of Geology and Mineral Resources 21, 149–165 (in Chinese).

99

Yan, Y., 1991. Shale-facies microflora from the Changzhougou Formation (Changcheng System) in Pangjiabu region, Hebei, China. Acta Micropalaeontological Sinica 8, 183–195 (in Chinese). Yan, Y., 1995. Shale facies microfloras from lower Changcheng System in Kuancheng, Hebei and comparison with those of Neighbouring areas. Acta Micropalaeontological Sinica 12, 349–373 (in Chinese). Yan, Y., Liu, Z., 1993. Significance of eucaryotic organisms in the microfossil flora of Changcheng System. Acta Micropalaeontologica Sinica 10, 167–180 (in Chinese). Yan, Y., Zhu, S., 1992. Discovery of acanthomorphic acritarchs from the Baicaoping Formation in Yongji, Shanxi and its geological significance. Acta Micropalaeontologica Sinica 9(3), 267–282 (in Chinese). Ye, Q., Tong, J., Xiao, S., Zhu, S., An, Z., Tian, L., Hu, J., 2015. The survival of benthic macroscopic phototrophs on a Neoproterozoic snowball Earth. Geology 43, 507–510. Yin, L., 1987. Microbiotas of Latest Precambrian Sequences in China, in: Nanjing Institute of Geology and Palaeontology, A.S. (Ed.), Stratigraphy and Palaeontology of Systemic Boundaries in China: Precambrian–Cambrian Boundary (1). Nanjing University Publishing House, Nanjing, pp. 415–523. Yin, L., 1997. Acanthomorphic acritarchs from Meso-Neoproterozoic shales of the Ruyang Group, Shanxi, China. Review of Palaeobotany and Palynology 98, 15–25. Yin, L., Guan, B., 1999. Organic-walled microfossils of Neoproterozoic Dongjia Formation, Lushan County, Henan Province, North China. Precambrian Research 94, 121–137.

100

Yin, L., Yuan, X., 2007. Radiation of Meso-Neoproterozoic and Early Cambrian protists inferred from the microfossil record of China. Palaeogeography, Palaeoclimatology, Palaeoecology 254, 350–361. Yin, L., Yuan, X., Meng, F., Hu, J., 2005. Protists of the Upper Mesoproterozoic Ruyang Group in Shanxi Province, China. Precambrian Research 141, 49–66. Zang, W., 1995. Early Neoproterozoic sequence stratigraphy and acritarch biostratigraphy, eastern Officer Basin, South Australia. Precambrian Research 74, 119–175. Zang, W., Walter, M.R., 1992. Late Proterozoic and Early Cambrian microfossils and biostratigraphy, northern Anhui and Jiangsu, central-eastern China. Precambrian Research 57, 243–323. Zhang, J., Tian, H., Li H., Su, W., Zhou, H., Xiang, Z., Geng, J., Yang, L., 2015a. Age, geochemistry and zircon Hf isotope of the alkaline basaltic rocks in the middle section of the Yan-Liao aulacogen along the northern margin of the North China Craton: New evidence for the breakup of the Columbia Supercontinent. Acta Petrologica Sinica 31(10), 3129–3146 (in Chinese). Zhang, S., Zhao, Y., Ye, H., Hu, G., 2016. Early Neoproterozoic emplacement of the diabase sill swarms in the Liaodong Peninsula and pre-magmatic uplift of the southeastern North China Craton. Precambrian Research 272, 203–225. Zhang, S., Zhao, Y., Ye, H., Hu, J., 2013. New constraints on ages of the Chuanlinggou and Tuanshanzi formations of the Changcheng System in the Yan-Liao area in the northern North China Craton. Acta Petrologica Sinica 29, 2481–2490 (in Chinese).

101

Zhang, Y., 1981. Proterozoic stromatolite microfloras of the Gaoyuzhuang Formation (Early Sinian: Riphean), Hebei, China. Journal of Paleontology 55(3), 485– 506. Zhang, Y., 1985. Stromatolitic microbiota from the middle Proterozoic Wumishan Formation (Jixian Group) of the Ming Tombs, Beijing, China. Precambrian Research 30, 277–302. Zhang, Y., Li, Q., Lan, Z., Wu, F., Li, X., Yang, J., Zhai, M., 2015b. Diagenetic xenotime dating to constrain the initial depositional time of the Yan-Liao Rift. Precambrian Research 271, 20–32. Zhang, Z., 1986. Clastic facies microfossils from the Chuanlinggou Formation (1800 Ma) near Jixian, North China. Journal of Micropalaeontology 5, 9–16. Zhu, S., Chen, H., 1995. Megascopic Multicellular Organisms from the 1700-MillionYear-Old Tuanshanzi Formation in the Jixian Area, North China. Science 270, 620. Zhu, S., Huang, X., Sun, S., 2005. New progress in the research of the Mesoproterozoic Changcheng System (1800–1400 Ma) in the Yanshan Range, North China. Journal of Stratigraphy S1, 437–449 (in Chinese). Zhu, S., Liu, H., Jun, H., 2012. On the disintegration of the Neoproterozoic Qingbaikouan System in Yanshan Range, North China. Geological Survey and Research 22(22), 5594–5607 (in Chinese). Zhu, S., Sun, S., Huang, X., He, Y., Zhu, G., Sun, L., Zhang, K., 2000. Discovery of carbonaceous compressions and their multicellular tissues from the Changzhougou formation (1800 Ma) in the Yanshan range, North China. Chinese Science Bulletin 45, 841–847.

102

Zhu, S., Xing, Y., Zhang, P., 1994. Biostratigraphic sequence of the middle-upper Proterozoic on North China Platform. Geological Publishing House, Beijing (in Chinese). Zhu, S., Zhu, M., Knoll, A.H., Yin, Z., Zhao, F., Sun, S., Qu, Y., Shi, M., Liu, H., 2016. Decimetre-scale multicellular eukaryotes from the 1.56-billion-year-old Gaoyuzhuang Formation in North China. Nature communications, 7: 11500.

103

Highlights: 1. We report the late Paleoproterozoic organic-walled microfossils from North China. 2. In total, 15 species (2 new species) including 6 unambiguous and 4 probable eukaryotic taxa are described. 3. The microfossils represent one of the earliest records of eukaryotes in the world. 4. Diversity of early eukaryotes reached moderate level by the late Paleoproterozoic.

104