An SEM study of microfossils in the black shale of the Lower Cambrian Niutitang Formation, Southwest China: Implications for the polymetallic sulfide mineralization

Ore Geology Reviews 65 (2015) 811–820

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An SEM study of microfossils in the black shale of the Lower Cambrian Niutitang Formation, Southwest China: Implications for the polymetallic sulfide mineralization Jun Xu, Yi-Liang Li ⁎ Department of Earth Sciences, The University of Hong Kong, Pok Fu Lam Road, Hong Kong Special Administrative Region, China

a r t i c l e

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Article history: Received 7 March 2014 Received in revised form 28 June 2014 Accepted 4 July 2014 Available online 10 July 2014 Keywords: Biomineralization Ni–Mo–PGE–Au Sulfide Green algae Black shale

a b s t r a c t The black shale in the Lower Cambrian Niutitang Formation on the southeastern margin of the Yangtze Platform hosts a layer of polymetallic sulfide ores containing extremely high concentrations of Ni (up to 3.8 wt.%) and Mo (up to 7.5 wt.%). Abundant micrometer-sized microfossils were observed in the Ni–Mo sulfide enriched layer under scanning electron microscopy. The microfossils include vesicles with clear organic wall structures and permineralized internal contents. These structures resemble unicellular green algae. Both biomass-adsorbed transition metals and biological structural protein metals could be accumulated and mineralized from the blooming algae, followed by anoxic microbial reduction and immobilization. The biotic impact may be a substantial mechanism for the massive Ni- and Mo-sulfide deposition in a typical restricted ocean basin environment. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Black shales are widely distributed in the lower part of the Lower Cambrian Niutitang Formation on the southeastern margin of the Yangtze Platform, South China, and its basal unit hosts the wellknown Ni–Mo–PGE–Au polymetallic sulfide deposits (Jiang et al., 2007; Murowchick et al., 1994; Zhu et al., 2003). The ores contain up to 7.5 wt.% Mo sulfides and 3.8 wt.% Ni sulfides (Steiner et al., 2001), being the richest ores of this kind hosted in black shales around the world (Lott et al., 1999). The formation of polymetallic sulfide ores around the Cambrian explosion (circa 545–530 Ma, Baker, 2006) is noteworthy. Its precise dating may have important biological and geochemical indications for the Precambrian–Cambrian (P–C) transition. Cambrian stratigraphy has been refined in the recent years, and the age of the base of Cambrian is determined to be 541 Ma (Walker et al., 2013; Zhu et al., 2006). The ore layer bears a molybdenite Re–Os age of 541 ± 16 Ma (Mao et al., 2002), indicating that global ocean anoxia was related to the major biological changes at the P–C boundary. This age was subsequently corrected to be 521 ± 5 Ma (Xu et al., 2011). A volcanic ash bed in the basal Niutitang Formation just below the Ni–Mo sulfide ore layer contains zircon with a U–Pb age of 518 ± 5 Ma (Zhou et al., 2008) or

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http://dx.doi.org/10.1016/j.oregeorev.2014.07.004 0169-1368/© 2014 Elsevier B.V. All rights reserved.

532.3 ± 0.7 Ma (Jiang et al., 2009), therefore suggesting that the global ocean anoxic event might not be responsible for the major evolution changes at the P–C boundary. The Cambrian explosion is a tremendous biological and geological conundrum in the evolution history of life. Rich fossil preservations have been uncovered in Neoproterozoic to Cambrian strata in China and around the world (Zhu, 2010). Nevertheless, molecular clock estimates show that major animal clades diverged long before their first appearance in the fossil record (Erwin et al., 2011). Occurrence of the Burgess Shale-type Chengjiang biota (525–520 Ma, Zhang et al., 2007) in Yunnan Province of Southwest China provided evidence for the rapid emergence of animal and algae species in near-shore marine environments (Gabbott et al., 2004; Hou et al., 1991), followed by the emergence of the Kaili biota from neighboring Guizhou Province (Zhao et al., 2005) and the Burgess Shale fauna from British Columbia, Canada (Conway Morris, 1989). It is generally agreed that the formation of the Cambrian polymetallic sulfide ores required anoxic and reductive environments, and that hydrothermal activity provided part of the metal source, such as U and Ni (Pi et al., 2013; Steiner et al., 2001). Some elements like Mo are mainly originated from seawater (Orberger et al., 2007). However, genesis of the Ni–Mo sulfide enriched layer is still a matter of debate. Mechanism of polymetal enrichment, especially the co-existence of metals with distinct geochemical properties, such as redox-sensitive metals, heavy metals and others, still remains mysterious and can hardly be explained by known geochemical mechanisms (Pi et al., 2013).

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The paleogeographic setting of the Lower Cambrian continental margin of Yangtze Platform indicates local stagnant basin environment controlled by syn-sedimentary rifting, which allowed syn-sedimentary metal enrichment from seawater under anoxic, highly reduced conditions (Mao et al., 2002). Geochemical evidence of biological activities has been reported. For example, S isotopic ratios suggest bacteria accumulated metals from venting fluids (Lott et al., 1999). Black shales have similar C/N ratios to zooplankton kerogens from clay-rich Devonian–Carboniferous carbonates in South China, and the ores are crosscut by hydrothermal veins, suggesting the formation of biogenic MoSC in a hydrothermal environment (Orberger et al., 2007). The recent studies showed that the Ni–Mo rich mineralized bodies are remnant of phosphate- and sulfide-rich subaquatic hardground supplemented with organics from planktonic and benthic species together with algal/microbial oncolite-like bodies in disturbed shallow water (Kríbek et al., 2007). Pašava et al. (2008) further suggested that leaching footwall Neoproterozoic sequences may be an extra source of the polymetals in addition to hydrothermal enrichments. Abundant fauna fossils such as arthropods, sponges and shelly remains were found within the hosting black shale (Braun et al., 2007; Steiner et al., 2001; Zhou and Jiang, 2009). Fossils in the Lower Cambrian black shale are generally found above the Ni–Mo–PGE– Au ore layer, and animal fossils are generally absent in the ore layer (Zhu et al., 2003). Organic fossils (clots) were reported from thin sections of the ore layer (Cao et al., 2013; Pašava et al., 2008; Steiner et al., 2001). Nevertheless, there is still a lack of direct evidence that marine life participated in the formation of this ore layer. In this study, scanning electron microscopy (SEM) is employed to investigate the well-preserved algal-like microfossil structures of micrometer size. Our study indicates that algal mats might have

existed in the unique sulfide ores. Biogenic origin of the polymetallic sulfides is further discussed. 2. Materials and methods The fossiliferous polymetallic Ni–Mo stratum is embedded in carbonaceous black shale at the bottom of the Niutitang Formation (Fig. 1). A total of twelve ore samples were collected from the Huangjiawan mine (N27.69°, E106.67°) near Songlin town, Zunyi, Guizhou Province (Fig. 2). Thin-sectioned slices of the samples were prepared by routine method, and the mineralogy was examined with an optical microscope and a DXR Raman spectroscope (Thermo Fisher Scientific Inc., USA). In order to avoid contamination, fresh surfaces of samples were produced for immediate SEM observation. All the produced surfaces were observed only once. The samples were first examined with an S-3400N Variable Pressure SEM (Hitachi, Japan) equipped with INCAx-sight electron dispersive X-ray spectroscopy system (EDS) detectors (Oxford Instruments, UK) for imaging at backscatter electron (BSE) mode at 20 kV. The samples were further examined with an S-4800 FEG SEM (Hitachi, Japan) equipped with EDS (Horiba, Japan) to obtain fine structures and chemical composition at secondary electron mode at low voltage (3–5 kV). 3. Results 3.1. Petrologic features of the Ni–Mo sulfide enriched layer and the black shale wall-rock The thickness of the Ni–Mo sulfide enriched layer varies from 0.05 m to 2 m. Hand specimen appears to be grayish black ores

Fig. 1. Distribution of the Ni−Mo sulfide layer in South China (after Mao et al., 2002).

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with intercalated layers of shiny metal enrichment (Fig. 3A–B). Minerals were briefly identified by morphology and characteristic Raman shifts, as also shown in optical microscope images (Fig. 3C–F). Organic matters are amorphous, dark and sometimes yellowish. Quartz is finely mixed with organic matters. Mo-sulfide seems to be closely associated with organic matters in amorphous form, bearing a yellowish color. Pyrite and millerite appear as bright aggregates or bands. Apatite is grayish, sometimes mixed with the carbonaceous molybdenite. For SEM observation, pyrite exists as layered crystals or framboidal aggregates (2–10 μm in diameter). The size of a single pyrite crystal is ~ 0.5–3 μm (Fig. 4A). Other minerals include millerite, molybdenite, dolomite and calcite. There are also occasionally bornite, gypsum and sphalerite (Fig. 4B–F). Trace amounts of barite, gersdorffite and chalcopyrite are present. Mo is always bound to C and S (Fig. 5A) in a so-called MoSC phase (Kríbek et al., 2007), but the C content can be highly variable in this mineral (~ 20–75 at.%). In contrast, millerite is associated with either organic C (Fig. 5B) or not (Fig. 5C), with a highest C content of ~ 30 at.%. As the wall-rock of the Ni–Mo sulfide layer, the black shale is largely carboniferous silt composed of hydromica, illite, sericite, quartz, calcite, pyrite, barite and apatite (Jiang et al., 2007; this study).

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3.2. Morphology of microfossils Micrometer-scale coccoid vesicles are preserved three-dimensionally in the Ni–Mo sulfide layer (Fig. 6) with an average diameter of 2.4 ± 0.7 μm. It appears that most of these vesicles have undergone compression, probably because of sedimentation and/or solidification. Some of them have laevigate envelopes and trilete morphologies (Fig. 6A–D) and appear similar to the microfossils from the Late Precambrian Bitter Springs Formation (Schopf and Blacic, 1971); others have partly mineralized surfaces (Fig. 6E– G). Some vesicle remains are disintegrated (Fig. 6H–I). Small spherical grains with an average diameter of 1.1 ± 0.3 μm occur either adjacent to (Fig. 7A, C) or encapsulated by organic vesicles (arrowed in Fig. 7B–E). The in situ preservation of these small grains within the envelopes is notable. There are accompanying euhedral gypsum rods, possibly as a result of oxidizing hydrothermal fluids (Orberger et al., 2007) (Fig. 7B–E). All excystment openings are simple ruptures (Fig. 7B–F). All the vesicles have smooth (organic) external surface with little ornament and mineralized internal content (Fig. 7B–F), suggesting that the fossils have experienced permineralization. Chemical composition of the vesicles was measured by EDS. The external surfaces have organic C (~ 50 wt.%), siliceous materials (~ 10 wt.%), and metal sulfides (3–4 wt.%). The organic nature of the vesicles indicates that they are soft membrane structures rather than rigid cell walls. The internal surfaces (Fig. 7E–F) contain more metal sulfides (~30 wt.%) but less C (~20 wt.%). Unlike the organic vesicles, the small grains observed were largely mineralized to metal sulfides, being gersdorffite or pyrite. They are apparently different from adjacent metal sulfides both in morphology and structure. These grains might not be authentic biological structures; rather, they were probably mineralized during diagenesis, forming small sulfide spherules with extraordinarily intricate surfaces. It is noteworthy that these coarse grains are not present independently, but they are always closely associated with organic vesicle structures (Fig. 7B–E). Many of the microfossils have experienced varied degrees of deformation and became less identifiable, as compiled in Fig. 8. Some have preserved intact shapes with partly mineralized external surface (Fig. 8A–H). Some have partly broken surfaces and higher degree of mineralization of internal structures (Fig. 8I–L). Some of them only have envelope without internal contents (Fig. 8M–Q). Internal structures were completely mineralized in two of the fossils (Fig. 8R–S). One fossil was completely mineralized, with part of the internal contents leaking out of the envelope (Fig. 8T). 4. Discussion 4.1. Classification of microfossils

Fig. 2. Stratigraphic diagram of the Ni−Mo sulfide layer in the Niutitang Formation, Zunyi, Guizhou Province, Southwest China (after Steiner et al., 2001).

Pašava et al. (2008) suggested that elliptical organic matter in the polymetallic ore layer had undergone diagenetic alteration to form sulfides, with pyrite, MoSC, and other organic matter debris present in the inner parts of organic matter ellipses, so the organic matter was probably sourced from bacteria and algae, which could readily be replaced by sulfides. In our study, the organic vesicles and spore-like bodies were uniquely found in the Ni–Mo enriched layer, but not in the host black shale. Contamination is excluded because all sample surfaces were freshly opened and many of the fossils appear to be closely associated with minerals. Though they are bacteriomorph-sized, bacteria seldom form spores and can hardly fossilize since they lack compounds to build shape and resist diagenesis. It seems that the fossils do not have cyanobacterial affinities because no colonial existence could be observed.

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Fig. 3. Photographs of Ni−Mo sulfide ores from the Niutitang Formation. A−B: images of the hand specimen. C−F: optical microscope images of the Ni−Mo sulfide ores (reflection mode). Minerals were identified by Raman spectroscopy. om: organic matters; ap: apatite; f: framboidal pyrite; m: millerite; mo: molybdenite; qz: quartz.

Some tetrahedral spores with bigger sheath were introduced as red or green algae from late Precambrian strata (Schopf and Blacic, 1971). Xiao et al. (2004) discovered phosphatized red algae in the Neoproterozoic Doushantuo Formation of South China (580 Ma), which is slightly older than the Niutitang Formation (e.g., Jiang et al., 2009; Mao et al., 2002) and within 100 km distance from the Huangjiawan mine site. Red and brown algal fossils were reported in the adjacent Kaili biota (Zhao et al., 2005). Steiner et al. (2001) and Pašava et al. (2008) identified phosphatized elliptical organic matter in the polymetal sulfide ores as lower algae and bacteria (e.g., cyanobacteria), whereas Cao et al. (2013) interpreted organic clots (200–600 μm) in the ores as rhodophyte cystocarps. Fossils in this observation have a much smaller size than red algal cells which are usually about 3–15 μm in diameter (Bare et al., 1975), making them unlikely to be red algal remains. Some eukaryotic algal species such as heterotrophic flagellates are indeed as

small as 1 μm in diameter or even smaller (Massana et al., 2006). Andreoli et al. (1978) reported a green alga, Chlorella nana sp. nov., of a prominently reduced size (1.5–3 μm). This range seems to be comparable to our observation. Green algae is one of the four algal phyla that produce spores (Maggs and Callow, 2002), which might explain the small spore-like objects within organic vesicles observed in this study. Therefore we suggest that these microfossils probably have ancient green algal affinities. However, more observations are still needed to determine the taxonomy and confirm its connection with polymetal sulfide mineralization in other ore deposits. 4.2. Metal accumulation and mineralization The coexistence of organic matters and metal sulfides within black shales has been widely reported. For example, a good positive

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Fig. 4. Mineralogy of the Ni −Mo sulfide ores (SEM images). Minerals were identified by EDS. p: pyrite; f: framboidal pyrite; g: gypsum; cl: clay minerals; d: dolomite; b: bornite; m: millerite; mo: molybdenite.

linear correlation between organic C and S in pyrite has been established for normal marine shale of all ages (Raiswell and Berner, 1986). Mo abundance can be a proxy for organic C in black shales (Wilde et al., 2004). Although a strong link between phytoplanktonic fossils and Ni–Mo sulfide precipitation is still not well established, the close association of sulfide minerals with organic contents in the Ni–Mo sulfide layer implies that marine algae may have played a crucial role in the formation of this polymetal deposit. Based on its locality on the passive continental margin of the Yangtze Platform, paleogeographic site as stagnant ocean basin has been suggested to be a suitable environment for the deposition of the Ni–Mo sulfide layer (Mao et al., 2002; Murowchick et al., 1994; Wang et al., 2005). Zhu et al. (2003) argued that the reasonable condition for the Ni–Mo ore formation is off-shore basin to slope. We propose a tentative paleoenvironment model (Fig. 9). Photosynthesis was supported in the photic zone in the upper water column, where phytoplanktons and macroalgae

proliferate. Denitrifying redox condition was present in the bottom water (below approximately 150 m depth) of the basin (Piper and Link, 2002). Abundant red bedding planes and trace fossils suggest the presence of seafloor microbial mats (Dornbos et al., 2004). High sedimentation rates of organic matters onto the sea floor contributed to the accumulation of phosphate (Li et al., 2013), chert, black shale, mudstone and absorbed trace metals (Piper and Link, 2002). Huge amounts of decayed organic accumulation can be produced upon long-term deposition, as indicated by extensive existence of framboidal pyrite as well as high C contents in the polymetallic sulfide layer. Proteins make up 37–50% of the cell wall in algae (Schiewer and Volesky, 2000). Nickel is utilized in several enzyme systems by micro-organisms (Kaluarachchi et al., 2010). Molybdenum forms the catalytic center of a large variety of enzymes (Schwarz et al., 2009). Substantial environmental studies have demonstrated that the biomass of marine algae, including green, red and brown

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venting activities could be the source of Ni (Pi et al., 2013; Steiner et al., 2001). Large quantities of algal remnants could have accumulated enough metals which were reduced and fixed through bacterial activities. SRB plays an important role in the mineralization of organic C in seabed (Jørgensen, 1982). SRB activity in this Ni–Mo rich layer was confirmed by typical S isotopic compositions of sulfides (Murowchick et al., 1994). The existence of substantive pyrite framboids in the Ni–Mo enriched layer (Fig. 4A) was also attributed to SRB colonization (Kohn et al., 1998). It is conceivable that SRB is involved in the reduction of high-valent metals and sulfide generation in submarine anoxic and reductive environments, whereas organic algal residues serve as effective substrate and C source for bacterial proliferation. The coupled metal reduction in turn may co-precipitate as sulfides with isotopic biosignatures. Huge amounts of algal biomass could be a prerequisite for the formation of polymetal ores through rapid growth in a time window of, for example, 100,000 years. Carbon isotope record shows that the Upper Neoproterozoic and Lower Cambrian black shales in the Yangtze Platform were probably formed in upwelling systems with high organic productivities (Li et al., 1999). Passive continental margin during the maximal transgression in Early Cambrian could have greatly enhanced biological propagation in shallow waters (Pu et al., 1992). Increased atmospheric and ocean oxidation in late Neoproterozoic may have changed the bioavailability of nitrate and trace elements (Knoll and Xiao, 2003). Different types of algae have shown high ability of Ni biosorption (Holan and Volesky, 1994). The amount of annual production of green algae could be as high as 48.9 kg·m − 2 in photic zone (Xu and He, 2006), which in turn may yield at least 3.23 million tons of nickel storage in a period of 100,000 years in a shallow marine environment of 20 km 2 . This calculated yield is one order of magnitude higher than the estimated nickel storage of 0.15 million tons in the mining reserve of this area (Mao et al., 2002). Considering the fact that metal source could be a possible limit of algal growth (Morel et al., 1991), the calculated amount of metal mineralization is more than enough for the whole depositional area. 5. Conclusions The unusual Ni–Mo sulfide enriched ore layer of Lower Cambrian black shales in the Yangtze Platform contains a considerable amount of microfossils. Morphological and mineralogical records indicate that these well-preserved microfossils may have green algal origins. They might have played important roles in the formation of the polymetallic ore layer. We tentatively suggest that algae bloom and consequent accumulation of remnant biomass in restricted basins provided strong absorbent for collecting multiple transition metals, and bacterial sulfate reduction fixed these metals into sulfides. Fig. 5. Semi-quantitative EDS spectra of the Mo- and Ni-rich minerals measured by S-4800 SEM. A: Mo associated with C and S; B: millerite associated with C content; C: millerite without C content. Inner ring denotes the range of electron beam. Outer ring denotes the range of signal collection. Note S (K line) and Mo (L line) have overlapping peaks at ~2.3 keV.

algae, has great potential in the sorption of heavy metal ions, such as Cu2 +, Zn2 +, Ni2 +, Cd2 +, Pb2 + and Hg2 + (e.g., Doshi et al., 2006; Holan and Volesky, 1994; Prasher et al., 2004; Shanab et al., 2012). Mo-sulfide in the black shales is suggested to be a result of dissimilatory sulfate reducing bacterial (SRB) metabolism and selective enrichment of Mo in paleo-seawater (Biswas et al., 2009). There is plenty of dissolved molybdate in seawater, but hydrothermal

Acknowledgments We would like to thank Prof. Lizeng Bian (Nanjing University) and Prof. Leiming Yin (Nanjing Institute of Geology and Paleontology, CAS) for their kind advice. Dr. Sanyuan Zhu, Mr. Frankie Chan and Ms. Amy Wong are acknowledged for their assistance in electron microscope operations. This study was supported by Hong Kong Research Grants Council (HKU703412P). References Andreoli, C., Rascio, N., Casadoro, G., 1978. Chlorella nana sp. nov. (Chlorophyceae): a New Marine Chlorella. Bot. Mar. 21, 253–256. Baker, M.E., 2006. The genetic response to Snowball Earth: role of HSP90 in the Cambrian explosion. Geobiology 4, 11–14.

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Fig. 6. SEM images of the algae-like microfossils. A−G: vesicles with trilete appearance; H−I: heavily squeezed vesicles.

Bare, W.F.R., Jones, N.B., Middlebrooks, E.J., 1975. Algae removal using dissolved air flotation. J. Water Pollut. Control Fed. 47, 153–169. Biswas, K., Woodards, N., Xu, H., Barton, L., 2009. Reduction of molybdate by sulfatereducing bacteria. BioMetals 22, 131–139. Braun, A., Chen, J.Y., Waloszek, D., Maas, A., 2007. Siliceous microfossils and biosiliceous sedimentation in the lowermost Cambrian of China. Geol. Soc. Lond., Spec. Publ. 286, 423–424. Cao, J., Hu, K., Zhou, J., Shi, C.H., Bian, L.Z., Yao, S.P., 2013. Organic clots and their differential accumulation of Ni and Mo within early Cambrian black-shale-hosted polymetallic Ni–Mo deposits, Zunyi, South China. J. Asian Earth Sci. 62, 531–536. Conway Morris, S., 1989. Burgess shale faunas and the Cambrian Explosion. Science 246, 339–346. Dornbos, S., Bottjer, D., Chen, J.Y., 2004. Evidence for seafloor microbial mats and associated metazoan lifestyles in Lower Cambrian phosphorites of Southwest China. Lethaia 37, 127–137. Doshi, H., Ray, A., Kothari, I.L., Gami, B., 2006. Spectroscopic and scanning electron microscopy studies of bioaccumulation of pollutants by algae. Curr. Microbiol. 53, 148–157. Erwin, D.H., Laflamme, M., Tweedt, S.M., Sperling, E.A., Pisani, D., Peterson, K.J., 2011. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334, 1091–1097. Gabbott, S.E., Hou, X., Norry, M.J., Siveter, D.J., 2004. Preservation of Early Cambrian animals of the Chengjiang biota. Geology 32, 901–904. Holan, Z.R., Volesky, B., 1994. Biosorption of lead and nickel by biomass of marine algae. Biotechnol. Bioeng. 43, 1001–1009. Hou, X.G., Ramskold, L., Bergstrom, J., 1991. Composition and preservation of the Chengjiang fauna — a Lower Cambrian soft-bodied biota. Zool. Scr. 20, 395–411. Jiang, S.Y., Yang, J.H., Ling, H.F., Chen, Y.Q., Feng, H.Z., Zhao, K.D., Ni, P., 2007. Extreme enrichment of polymetallic Ni–Mo–PGE–Au in lower Cambrian black shales of South China: an Os isotope and PGE geochemical investigation. Palaeogeogr. Palaeoclimatol. Palaeoecol. 254, 217–228. Jiang, S.Y., Pi, D.H., Heubeck, C., Frimmel, H., Liu, Y.P., Deng, H.L., Ling, H.F., Yang, J.H., 2009. Early Cambrian ocean anoxia in South China. Nature 459, E5–E6. Jørgensen, B.B., 1982. Mineralization of organic matter in the sea bed — the role of sulphate reduction. Nature 296, 643–645. Kaluarachchi, H., Chan Chung, K.C., Zamble, D.B., 2010. Microbial nickel proteins. Nat. Prod. Rep. 27, 681–694.

Knoll, A.H., Xiao, S.H., 2003. Algae and the Late Neoproterozoic evolution of macroscopic multicellularity. GSA Annual Meeting Abstracts with Programs, 35 (6). Kohn, M.J., Riciputi, L.R., Stakes, D., Orange, D.L., 1998. Sulfur isotope variability in biogenic pyrite: reflections of heterogeneous bacterial colonization? Am. Mineral. 83, 1454–1468. Kríbek, B., Sýkorová, I., Pasava, J., Machovic, V., 2007. Organic geochemistry and petrology of barren and Mo–Ni–PGE mineralized marine black shales of the Lower Cambrian Niutitang Formation (South China). Int. J. Coal Geol. 72, 240–256. Li, R.W., Lu, J.L., Zhang, S.K., Lei, J.J., 1999. Organic carbon isotopes of the Sinian and Early Cambrian black shales on Yangtze Platform, China. Sci. China Ser. D Earth Sci. 42, 595–603. Li, Y.L., Sun, S., Chan, L.S., 2013. Phosphogenesis in the 2460 and 2728 million-year-old banded iron formations as evidence for biological cycling of phosphate in the early biosphere. Ecol. Evol. 3, 115–125. Lott, D.A., Coveney, R.M., Murowchick, J.B., Grauch, R.I., 1999. Sedimentary exhalative nickel-molybdenum ores in South China. Econ. Geol. 94, 1051–1066. Maggs, C.A., Callow, M.E., 2002. Algal spores. Encyclopedia of Life Sciences. Macmillan Publishers Ltd, London, pp. 1–6. Mao, J.W., Lehmann, B., Du, A.D., Zhang, G.D., Ma, D.S., Wang, Y.T., Zeng, M.G., Kerrich, R., 2002. Re−Os dating of polymetallic Ni−Mo −PGE −Au mineralization in Lower Cambrian black shales of South China and its geologic significance. Econ. Geol. 97, 1051–1061. Massana, R., Terrado, R., Forn, I., Lovejoy, C., Pedrós-Alió, C., 2006. Distribution and abundance of uncultured heterotrophic flagellates in the world oceans. Environ. Microbiol. 8, 1515–1522. Morel, F.M.M., Hudson, R.J.M., Price, N.M., 1991. Limitation of productivity by trace metals in the sea. Limnol. Oceanogr. 36, 1742–1755. Murowchick, J.B., Coveney Jr., R.M., Grauch, R.I., Eldridge, C.S., Shelton, K.L., 1994. Cyclic variations of sulfur isotopes in Cambrian stratabound Ni−Mo−(PGE−Au) ores of southern China. Geochim. Cosmochim. Acta 58, 1813–1823. Orberger, B., Vymazalova, A., Wagner, C., Fialin, M., Gallien, J.P., Wirth, R., Pasava, J., Montagnac, G., 2007. Biogenic origin of intergrown Mo-sulphide- and carbonaceous matter in Lower Cambrian black shales (Zunyi Formation, southern China). Chem. Geol. 238, 213–231. Pašava, J., Kříbek, B., Vymazalová, A., Sýkorová, I., Žák, K., Orberger, B., 2008. Multiple sources of metals of mineralization in Lower Cambrian black shales of South China: evidence from geochemical and petrographic study. Resour. Geol. 58, 25–42.

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Fig. 7. SEM images of the microfossils with permineralized contents. A: a rugged sulfide spherule (ss) and gypsum rods (gr); B−C: vesicles encapsulating and releasing rugged spherules, with gypsum rods; D: an unbroken vesicle, with a protruding gypsum rod and a sulfide spherule; E−F: broken vesicles with and without rugged spherules.

Pi, D.H., Liu, C.Q., Shields-Zhou, G.A., Jiang, S.Y., 2013. Trace and rare earth element geochemistry of black shale and kerogen in the early Cambrian Niutitang Formation in Guizhou province, South China: constraints for redox environments and origin of metal enrichments. Precambrian Res. 225, 218–229. Piper, D.Z., Link, P.K., 2002. An upwelling model for the Phosphoria sea: a Permian, oceanmargin sea in the northwest United States. AAPG Bull. 86, 1217–1235. Prasher, S.O., Beaugeard, M., Hawari, J., Bera, P., Patel, R.M., Kim, S.H., 2004. Biosorption of heavy metals by red algae (Palmaria palmata). Environ. Technol. 25, 1097–1106. Pu, X.C., Zhou, H.D., Wang, X.L., 1992. Cambrian Lithofacies, Paleogeography and Mineralization in South China (in Chinese). Geological Publishing House, Beijing. Raiswell, R., Berner, R.A., 1986. Pyrite and organic matter in Phanerozoic normal marine shales. Geochim. Cosmochim. Acta 50, 1967–1976. Schiewer, S., Volesky, B., 2000. Biosorption by marine algae. In: Valdes, J.J. (Ed.), Bioremediation. Kluwer, Dordrecht, the Netherlands, pp. 139–169. Schopf, J.W., Blacic, J.M., 1971. New microorganisms from the Bitter Springs Formation (Late Precambrian) of the North-Central Amadeus Basin, Australia. J. Paleontol. 45, 925–960. Schwarz, G., Mendel, R.R., Ribbe, M.W., 2009. Molybdenum cofactors, enzymes and pathways. Nature 460, 839–847. Shanab, S., Essa, A., Shalaby, E., 2012. Bioremoval capacity of three heavy metals by some microalgae species (Egyptian Isolates). Plant Signal. Behav. 7, 392–399. Steiner, M., Wallis, E., Erdtmann, B.-D., Zhao, Y., Yang, R., 2001. Submarine-hydrothermal exhalative ore layers in black shales from South China and associated fossils — insights into a Lower Cambrian facies and bio-evolution. Palaeogeogr. Palaeoclimatol. Palaeoecol. 169, 165–191.

Walker, J.D., Geissman, J.W., Bowring, S.A., Babcock, L.E., 2013. The Geological Society of America Geologic Time Scale. Geol. Soc. Am. Bull. 125, 259–272. Wang, M., Sun, X.M., Ma, M.Y., 2005. Microthermometric measurement of fluid inclusions and its constraints on genesis of PGE-polymetallic deposits in Lower Cambrian black rock series, southern China. Chin. J. Geochem. 24, 297–305. Wilde, P., Lyons, T.W., Quinby-Hunt, M.S., 2004. Organic carbon proxies in black shales: molybdenum. Chem. Geol. 206, 167–176. Xiao, S.H., Knoll, A.H., Yuan, X.L., Pueschel, C.M., 2004. Phosphatized multicellular algae in the Neoproterozoic Doushantuo Formation, China, and the early evolution of florideophyte red algae. Am. J. Bot. 91, 214–227. Xu, S.N., He, P.M., 2006. Analysis of phenomena for frequent occurrences of red tides and bioremediation by seaweed cultivation. J. Fish. China 30, 554–561 (in Chinese with English abstract). Xu, L.G., Lehmann, B., Mao, J.W., Qu, W.J., Du, A.D., 2011. Re − Os age of polymetallic Ni −Mo −PGE − Au mineralization in Early Cambrian black shales of South China — a reassessment. Econ. Geol. 106, 511–522. Zhang, Z.F., Shu, D.G., Emig, C., Zhang, X.L., Han, J., Liu, J.N., Li, Y., Guo, J.F., 2007. Rhynchonelliformean brachiopods with soft-tissue preservation from the early Cambrian Chengjiang Lagerstätte of South China. Palaeontology 50, 1391–1402. Zhao, Y.L., Zhu, M.Y., Babcock, L.E., Yuan, J.L., Parsley, R.L., Peng, J., Yang, X.L., Wang, Y., 2005. Kaili Biota: a taphonomic window on diversification of metazoans from the basal Middle Cambrian: Guizhou, China. Acta Geol. Sin. Engl. 79, 751–765. Zhou, C.M., Jiang, S.Y., 2009. Palaeoceanographic redox environments for the lower Cambrian Hetang Formation in South China: evidence from pyrite framboids, redox

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Fig. 8. SEM images of the less identifiable microfossils. These fossils experienced different degrees of deformation and mineralization.

Open Ocean photic zone phytoplankton

O2

macroalgae

Restricted Basin oxic suboxic/anoxic

Algal mat Framboidal pyrite

Black shale

Carbonaceous Ni-Mo sulfide layer

Fig. 9. Schematic diagram of a restricted basin environment at continental margin. Redox status changes with water depth. Biological activities on the seabed are evidenced by stable S isotope signatures and high organic C background.

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sensitive trace elements, and sponge biota occurrence. Palaeogeogr. Palaeoclimatol. Palaeoecol. 271, 279–286. Zhou, M.Z., Luo, T.Y., Li, Z.X., Zhao, H., Long, H.S., Yang, Y., 2008. SHRIMP U−Pb zircon age of tuff at the bottom of the Lower Cambrian Niutitang Formation, Zunyi, South China. Chin. Sci. Bull. 53, 576–583. Zhu, M.Y., 2010. The origin and Cambrian explosion of animals: fossil evidences from China. Acta Palaeontol. Sin. 49, 269–287 (in Chinese with English abstract).

Zhu, M.Y., Zhang, J.M., Steiner, M., Yang, A.H., Li, G.X., Erdtmann, B.D., 2003. Sinian− Cambrian stratigraphic framework for shallow- to deep-water environments of the Yangtze Platform: an integrated approach. Prog. Nat. Sci. 13, 951–960. Zhu, M.Y., Babcock, L.E., Peng, S.C., 2006. Advances in Cambrian stratigraphy and paleontology: integrating correlation techniques, paleobiology, taphonomy and paleoenvironmental reconstruction. Palaeoworld 15, 217–222.