Iron and phosphorus biochemical systems and the Cryogenian-Ediacaran transition, Jacadigo basin, Brazil: Implications for the Neoproterozoic oxygenation event

Journal Pre-proofs Iron and phosphorus biochemical systems and the Cryogenian-Ediacaran transition, Jacadigo basin, Brazil: Implications for the Neoproterozoic Oxygenation Event Eric E. Hiatt, Peir K. Pufahl, Leandro Guimarães da Silva PII: DOI: Reference:

S0301-9268(19)30400-0 https://doi.org/10.1016/j.precamres.2019.105533 PRECAM 105533

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Precambrian Research

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12 July 2019 11 November 2019 14 November 2019

Please cite this article as: E.E. Hiatt, P.K. Pufahl, L. Guimarães da Silva, Iron and phosphorus biochemical systems and the Cryogenian-Ediacaran transition, Jacadigo basin, Brazil: Implications for the Neoproterozoic Oxygenation Event, Precambrian Research (2019), doi: https://doi.org/10.1016/j.precamres.2019.105533

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IRON AND PHOSPHORUS BIOCHEMICAL SYSTEMS AND THE CRYOGENIANEDIACARAN TRANSITION, JACADIGO BASIN, BRAZIL: IMPLICATIONS FOR THE NEOPROTEROZOIC OXYGENATION EVENT Hiatt, Eric, E.1* [email protected] (920) 424-7001 FAX (920) 424-0240 Pufahl, Peir K.2 [email protected] Leandro Guimarães da Silva2,3 [email protected]

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Department of Geology, University of Wisconsin - Oshkosh Oshkosh, Wisconsin, 54901, USA

Department of Geological Sciences and Geological Engineering Queen's University, Kingston, ON K7L3N6, Canada 3

SGB-CPRM - Geological Survey of Brazil Brasilia DF, 70.040-904, Brazil

*

Corresponding Author

Key words: Neoproterozoic Oxygenation, Cryogenian, phosphorite, biogeochemical, iron formation

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Highlights 

Transition out of one of the most extreme global ice ages in Earth history

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Sub-sea ice microbial marine ecosystem on the cusp of oxygenation

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Short-term redox fluctuations allowed phosphate to precipitate on the seafloor

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Photosynthesis and oxygen limited by ice cover during the Marinoan Snowball Earth

Graphical abstract

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ABSTRACT Termination of the Marinoan Snowball Earth ice age (635 Ma) marked the transition to a greenhouse world. This climate change forever modified the biogeochemical cycling of iron and phosphorus, ended large-scale iron formation deposition, began accumulation of phosphorus on marine shelves, and led to the Ediacaran radiation of eukaryotes. The Jacadigo Basin, Brazil, contains a nearly complete record of this critical transition. Glaciomarine diamictites and iron formation accumulated during two Marinoan ice advances with hydrothermal input of iron delivered via ice-margin upwelling. Biochemically precipitated rhythmites of siderite, sedimentary apatite, and hematite represent microbially mediated, sub-sea ice precipitation. Siderite laminae preserve microbial textures and have a mean ∂13C = -8.80 ‰, PDB (+/-0.86‰) reflecting degradation of organic matter at the seafloor. These millimeter-scale rhythmites are a sensitive record of sub-ice dynamics because they formed in response to shortterm fluctuations of O2 due to seasonal sub-ice photosynthesis. They demonstrate the connection between ice cover, O2, and cycling of iron and nutrient elements such as phosphorus. These biochemical rhythmites suggest that Cryogenian sea ice limited oxygen production prior to the onset of the Neoproterozoic Oxygenation Event. O2 increased enough to concentrate bioavailable phosphorus at the seafloor, which was essential for later diversification of metazoans in the Ediacaran. Such sub-ice Cryogenian biochemical systems may provide Earthbased analogs for life on ice-covered worlds, such as Europa and Enceladus.

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1. INTRODUCTION The Neoproterozoic Cryogenian to Ediacaran transition (ca. 635 Ma) was a critical time in the evolution of the geosphere and biosphere with rising O2 levels, diversification of metazoans, and emergence from one of the most severe ice ages in Earth history, the Marinoan Snowball glaciation (Kirschvink, 1992; Hoffman et al., 1998; Kirschvink et al., 2000; Hoffman and Schrag, 2002). Associated with the Marinoan, and earlier Sturtian glaciation, was the return of iron formation deposition after a billion years’ hiatus (Klein, 2005; Hoffman et al., 2017). The connection between Neoproterozoic iron formation and glaciomarine deposition has long been recognized (Kirschvink et al., 2000) and is a cornerstone of the “Snowball Earth” model (Kirschvink, 1992; Kirschvink et al., 2000). Near-global sea-ice cover is presumed to have limited photosynthetic O2 production and exchange with the atmosphere, and with hydrothermal input of Fe, produced nutrient-rich, ferruginous seawater that was periodically tapped via upwelling to produce synglacial iron formation. What has not been adequately explored are the relationships between ice cover and sub-ice seafloor environments, including biochemical processes and changes in the cycling of nutrient elements such as iron (Fe) and phosphorus (P). The Cryogenian-Ediacaran transition is recorded around the world as a sharp stratigraphic change between Marinoan glaciogenic rocks and unconformable cap carbonates above (James et al., 2001; Jiang et al., 2011). The apparent rapidity of this environmental change is partially an artifact of the minimal accommodation that was available in the platformal settings where most of the studied cap carbonate successions accumulated, which makes the associated sea-level rise appear rapid (Myrow et al., 2018). In such settings, low initial sedimentary accommodation, combined with rapid sea-level rise and isostatic crustal adjustments, generally resulted in little or no sediment accumulation during the transition.

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To more completely understand the nature of this important transition we investigated the Neoproterozoic Jacadigo Basin, Brazil (Fig. 1; Angerer et al., 2016). Supergene weathering that is pervasive in outcrop exposures of Brazil resulted in complete dissolution of siderite, phosphate minerals, partial removal of dolomite and clay minerals, and quartz, which obscures details in depositional and diagenetic fabrics and textures. Previous studies have been based on outcrop and mine subcrop exposures (all intensely altered), and to a very limited extent, drill cores (e.g. Freitas et al., 2011), which has led to a very incomplete understanding of the CryogenianEdiacaran transition in this region. Our study is based on recently drilled high-quality diamond drill cores through the lower Ediacaran to Cryogenian section in the Jacadigo Basin. The Jacadigo Basin is an aulacogen filled with iron formation of the Santa Cruz Formation that is interbedded with glaciomarine diamictite of the Marinoan Puga Formation (ca. 635 Ma; Babinski et al., 2013), an important marker throughout the region (Fig. 2). Sedimentation in this rift basin produced a nearly complete sedimentologic record through the Cryogenian-Ediacaran transition, which preserved a transitional section between the Cryogenian and the regional carbonate platform of the Ediacaran. This high-resolution window provides new insights into the nature of this critical boundary.

2. GEOLOGIC SETTING The Neoproterozoic of Brazil is characterized by rifting, glaciation, and periods of stability that were punctuated by convergence of the Amazon, São Franciscan, and Rio de La Plata cratons during the Brasiliano orogeny (Trompette et al., 1998; Gaucher et al., 2003; Freitas et al., 2011; Fig. 3). Breakup of Rodinia, and the early-stage assembly of West Gondwana led to deposition of sediments that comprise the Santa Cruz Formation in the Neoproterozoic Jacadigo

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Basin. The Jacadigo Basin is an aulacogen (Fig. 1; Trompette et al., 1998; Fuck et al., 2008; Angerer et al., 2016) between the Amazonian, Rio de La Plata, and São Francisco cratons (Fig. 3). It dissects the Rio Apa block, a crustal outlier (Trompette et al., 1998), which is either an allochthonous crustal fragment or the southern extension of the Amazon Craton (Cordani et a., 2010). In the Neoproterozoic, the Amazon Craton and Rio Apa block were rotated ca. 180° and located at 30-40°S (Trindade et al., 2003; Tohver et al., 2006; Trindade & Macouin, 2007). The Urucum and Santa Cruz formations together make up the Jacadigo Group (Fig. 2; Almeida, 1945; Dorr, 1945; Piacentini et al., 2007; Walde and Hagemann, 2007). The Urucum Formation, which overlies Mesoproterozoic granite and gneiss of the Rio Apa Complex, is composed mostly of conglomeratic and sandy braided stream deposits (Fig. 2). The change from the Urucum Formation to marine conditions of the overlying Santa Cruz Formation is marked by shoreface sandstone with reworked hematitic, silt- to pebble-sized mud rip-up clasts. Ice-rafted dropstones first appear in the lower portion of the Santa Cruz Formation (Urban et al., 1992; Gaucher et al., 2015). The upwelling-related iron formation of the Santa Cruz Formation is interbedded and overlain by pebble to boulder glacial diamictite of the Puga Formation (Almeida, 1945; Dorr, 1945; Karfunkel and Hoppe, 1988). Shallow marine deposits and coarsegrained braided river deposits rest conformably above the uppermost Puga diamictite and unconformably below the Corumbá Group (Gaucher et al. 2003). At its base, the carbonate rich Corumbá Group contains glacial outwash conglomerates of the Cadiueus Formation, which are overlain by marine sandstone and biochemical rhythmites of the Cerradinho Formation (Figs. 2 & 4), the focus of research herein. The Cadiueus and Cerradinho are included in the Corumbá Group (Almeida, 1965; Trompette et al., 1998; Gaucher et al., 2003), and assumed to be Ediacaran, but geochronology or biostratigraphic control is lacking. Sedimentologically, the

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outwash and dropstone-rich shallow marine facies of the Cerradinho would be more logically included in the Cryogenian Jacadigo Group. Regionally, the Corumbá Group is dominated by dolostones of the stromatolite-rich Bocaina Formation and mixed carbonate to siliciclastic, deeper-water facies of Tamengo Formation, which together represent the evolution of an extensive carbonate platform across the Paraguay Fold Belt and São Franciscan craton (Alvarenga et al., 2011). Ancient glacial deposits in Brazil have been recognized for over 120 years (Karfunkel and Hoppe, 1988 and references therein). Striated and facetted clasts, outsized clasts, scoured bedrock surfaces, as well as esker deposits, varved facies have long been recognized (e.g. Karfunkel and Hoppe, 1988 and references therein); Neoproterozoic glacial deposits in the Paraguay fold belt were first documented by Maciel (1959). Interpreted environments include “tillites” that pass laterally into crudely bedded to cross-bedded cobble to boulder-rich diamictite intervals and represent a wide spectrum of glacial environments from terrestrial ice-contact to glaciomarine (Karfunkel and Hoppe, 1988). In the Jacadigo Basin, Puga diamictites are sand-dominated and in mine outcrops, have large-scale crossbedding with foresets that can be traced 3-4 meters, suggesting a glaciomarine origin. In the southern Paraguay fold belt, beds contain striated and faceted clasts in a clay-rich matrix and represent ice-contact glacial till. Detrital zircon ages indicate an Amazon craton provenance, which records equatorward glacial transport with the Gondwana continental fragments rotated back to their Neoproterozoic paleo-positions (Trindade et al., 2003; Tohver et al., 2006; Trindade & Macouin, 2007). Further south in the Serra do Bodoquena (southern Paraguay fold belt; Fig. 1), detrital zircons suggest derivation from the Rio Apa Block and indicate transport from the paleo-W-SW (Babinski et al., 2013). The youngest detrital zircon U-

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Pb date is 706  9 Ma, which precludes a Sturtian (ca. 720 Ma) age and supports Puga Formation deposition in the Marinoan (ca. 635 Ma; Babinski et al., 2013; Rooney et al., 2015). The intercalation of Puga diamictite with iron formation of the underlying Santa Cruz Formation confirms that these biochemical sedimentary rocks are the youngest major iron formation (Piacentini et al., 2007; Walde and Hagemann, 2007; Babinski et al., 2013; Hoffman et al., 2017).

3. METHODS Lithology, sedimentary structures, stratigraphic changes, and diagenetic features were interpreted from drill cores logged at a centimeter-scale. One hundred and twenty-five polished thin sections through the Cryogenian-Ediacaran transition interval were examined. Photomicrographs were taken with a Leitz Ortholux II POL-BK petrographic microscope equipped with transmitted and reflected light and a Canon EOS Rebel T4i digital SLR camera. The mineralogy of all samples was determined by X-Ray diffraction using a Rigaku D/Max2000T X-Ray Diffractometer at the University of Wisconsin-Oshkosh. The diffractometer was operated at 40 KV and 40 mA, using a Cu Kα target, and scans run from 10 to 60 degrees twotheta. Microbeam analyses of selected samples were completed at the University of Canterbury and Argonne National Laboratory. Polished thin sections were carbon coated in an Emitech K975X coater. At the University of Canterbury, analyses were performed using a JEOL JSM6100 scanning electron microscope (SEM) equipped with an Oxford Instruments Oxford Instruments X-MaxN Silicon Drift electron backscattered detector (EDS) with a working distance of 15 mm and 20 KV operating voltage. Elemental concentration maps were created using Oxford Instrument’s AZtec large area element mapping software. At Argonne National 8

Laboratory, analyses were performed on a Hitachi S-4700-II Field emission SEM equipped with a Bruker XFlash 6160 EDS detector. A precision bench dental drill equipped with a 0.5 mm diameter tungsten bur was used to produce samples analyzed for ∂18O and ∂13C. Siderite mineralogy of all samples was confirmed using XRD prior to analysis. 200 to 500 µg samples were analyzed at 72 °C on a Gasbench 2 and Thermo Delta V Advantage mass spectrometer in the Department of Earth Sciences at Oxford University. The oxygen-isotope acid fractionation factor of Rosenbaum and Sheppard (1986; 1.00964) was utilized for the siderite samples and that of Kim et al. (2015; 1.00865) for NBS-18 and NBS-19. Reproducibilities were +/- 0.06 ‰ for ∂13C and +/- 0.14 ‰ for ∂18O, at one standard deviation based 41 analyses of the BGS Ivitut siderite standard.

4. RESULTS & DISCUSSION We examined, described, sampled, and logged fourteen new high-quality diamond drill cores through the Santa Cruz Formation and a few outcrop exposures. Some of the drill cores capture a sedimentary sequence above the Santa Cruz and Puga Formations. From this transitional interval we focused on the initial marine sedimentation above the uppermost Puga diamictite, an interval which is only preserved in drill core (Figs. 2 & 4). This stratigraphic section consists of shallow marine sandstone and mudstone facies with francolite (marine highly substituted carbonate fluor-apatite) glacial dropstones and biochemical rhythmites composed of millimeter-scale, microbially laminated, authigenic siderite, francolite, and hematite. Transmitted- and reflected-light petrography, elemental maps and secondary electron photomicrographs reveal diastem (sedimentary hiatus) surfaces on siderite (FeCO3) laminae,

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francolite on these surfaces, and hematite (Fe2O3) and francolite, as well as replacement textures (iron oxide phases in siderite laminae).

4.1 Sedimentology and Depositional Environments The Corumbá Group overlies the uppermost diamictite of the Puga Formation and previous to this study was thought to consist solely of the stromatolite-rich Bocaina which represents a regionally extensive shallow-water carbonate platform and overlying Tamengo formations in the Jacadigo Basin. In drill core, the top of the Puga diamictite is marked by an intensely pyritized and chloritized erosional surface; pyritization and chloritization are paragenetically late events associated with burial diagenesis. An 18-meter thick interval of light grey intraclast-bearing, granitic-gneiss-pebble to cobble conglomerate that is pervasively trough-cross-bedded overlies the Puga. The Cadiueus Formation has previously only been described in the Serra do Bodoquena where it has been interpreted as alluvial fan to braided stream deposits (Gaucher et al., 2003). Given the stratigraphic succession, sedimentary structures, and composition this interval is interpreted to represent a melt-water outwash deposit (Gaucher et al., 2003).

A sharp non-erosional contact separates the Cadiueus from the overlying 60-meter-thick dark-grey to black, thinly bedded, chlorite-rich, feldspathic sandstones and interbedded black laminated siltstone of the Cerradinho Formation (Fig. 4). The sandstones are ripple-crosslaminated, punctuated by pebble-sized granitic to gneissic dropped stones, and contain francolite peloids and flaser bedding (Fig. 5). The Cerradinho Formation has also previously only been described in the Serra do Bodoquena from the southernmost portions of the Paraguay fold belt

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and has been interpreted as representing shallow marine environments (Almeida, 1965; Gaucher et al., 2003).

Drill core through the Cerradinho Formation preserves three easily decimeter- to meterthick intervals of biochemical rhythmite consisting of siderite, francolite, and hematite in mmthick laminae (Figs. 4 & 6). These rhythmite intervals are not preserved in outcrop because the siderite and francolite weather rapidly (years to decades). Drill core reveal that the rhythmite laminae are devoid of siliciclastic sediment except for rare individual medium sand- to granulesized lone stones (Fig. 6A). The lower contacts of the rhythmite intervals are sharp but nonerosional, but the tops are erosional with ripped-up clasts of the rhythmite included in the overlying coarse-grained feldspathic sandstone units (Fig. 6C). The siderite-rich laminae readily oxidize a few days after cutting drill core; this rapid oxidative breakdown is why they are not preserved in outcrop. Ripple marks, flaser bedding, and rip-up clasts, in combination with francolite grains, suggest that sandstone units were deposited by tidal currents and wave action in a marine setting. The dropstones that punctuate the entire Cerradinho Formation (Figs. 5 & 6) additionally indicate that sea ice was present at least seasonally in this temperate latitude setting, and likely limited siliciclastic input along the shoreline. The stratigraphic evolution upward from diamictite of the Puga Formation to high-energy outwash braided streams of the Cadiueus Formation, followed by tidally influenced marine sediment of the Cerradinho Formation represents the initial marine transgression that flooded the late stage of this rift basin (Gaucher et al., 2003; Alvarenga et al., 2011). The succession provides insights into the transition from the Marinoan Snowball ice age to widespread carbonate platform development (Bocaina Formation) in the Early Ediacaran.

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4.2 Biochemical Rhythmites The biochemical rhythmites are composed of laminated siderite, francolite, and hematite that contain a detailed record of fluctuating O2 levels (Fig. 6). Siderite layers (1 to 10 mm-thick) form rhythmite bases; when present, francolite laminae (<1 to 5 mm) formed on diastems atop underlying siderite laminae (Figs. 7 & 8). These contacts can be marked by microstylolites, but we chose examples for analysis that have no evidence of pressure solution at any scale. The surfaces are overlain by sand and silt-sized eroded siderite from the underlying laminae, and francolite is found as delicate crinkly crusts and formed authigenically in fenestral-like pores in the underlying siderite laminae (Figs. 7 & 8). Hematite layers (1-mm to 1-cm thick) commonly form cycle tops, although hematite, or its Fe-(oxyhydr)oxide precursor, infilled fenestral-like pores in the underlying siderite laminae where, through burial diagenesis, it became well crystallized hematite (Fig. 8). Microbial laminae and peloids occur in all layers but are well developed in siderite (Figs. 7 & 8). Key to the precipitation of these discrete layers was elimination of diluting terrigenous clastics. Except for rare lone clasts of medium- to granule-sized siliciclastic grains, siliciclastic sediment is conspicuously absent in the iron-rich rhythmite intervals (Figs. 6, 7, 8) suggesting periods of ice cover in which either clastic sediment remained frozen in the overlying ice or the ice was devoid of sediment. Throughout Earth history, deposition of iron formation and francolite usually form in environments with little or no siliciclastic sediment; this commonly occurs offshore of deserts where upwelling of either P- or Fe-rich waters takes place (Simonson, 1985; Klein, 2005; Pufahl, 2010; Bekker et al., 2010; Pufahl and Groat, 2017). In general, sedimentation rate estimates for the Cryogenian were unusually low (Partin and Sadler, 2016) and sea ice is thought to have extended to low latitudes (Hoffman et al., 1998).

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These rhythmites may represent an extreme, albeit short-lived, end member wherein virtually all terrestrial sedimentation was halted, and sub-ice, marine biochemical processes dominated.

4.2.1 Siderite Siderite is a minor, but common, syndepositional carbonate mineral that forms under microaerobic to anoxic reducing conditions often in association with methanogenesis (Berner, 1981; Walker, 1984; Mozley et al., 1992). Although an important phase in some hematite and magnetite-rich facies of Archean and Paleoproterozoic iron formation (Klein, 2005, Walker, 1984; Beukes et al., 1990), siderite has not been previously reported in Cryogenian iron deposits. In Paleoproterozoic iron formation, siderite is interpreted to have formed authigenically on and just beneath the seafloor and diagenetically during burial when microbial breakdown of sedimentary organic matter led to elevated alkalinity of pore water enriched in ferrous iron (Walker, 1984; Beukes et al., 1990; Beukes and Gutzmer, 2008). Under anoxic to microaerobic (ca. 1.0 nmol to 2.5 µmol O2/kg) conditions, siderite is thermodynamically stable and insoluble, but precipitates slowly (Jensen et al., 2002). The abundance of siderite at the transition out of the Marionan Snowball Earth ice age confirms Tziperman et al.’s (2011) prediction that anoxic deep oceans during the Neoproterozoic were key to creating conditions for microbial iron reduction, increased alkalinity, and widespread precipitation of siderite. Sea ice cover may have amplified the alkalinity of the Jacadigo Basin by restricting the diffusion of CO2 out of seawater (Hoffman et al., 1998; Le Heron et al., 2013). As in Archean and Paleoproterozoic iron formation, exchange with atmospheric CO2, bacterial respiration of organic carbon, and upwelling of hydrothermally modified water masses all were factors in controlling seawater alkalinity (Beukes et al., 1990; Fischer et al., 2009; Konhauser et al. 2017).

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The regular occurrence of micro-peloidal texture, crinkly microbial laminae, and microstromatolites in rhythmite layers (Figs. 7 & 8) support the bacteria-associated precipitation of siderite from alkaline pore water (a-d below).

(a) C6H12O6  3CO2 + 3CH4 (methanogenesis) (b) CO2(aq) + H2O  H2CO3 (c) H2CO3  HCO3- + H+ (d) Fe+2 + 2HCO3−1  FeCO3(SIDERITE) + CO2 + H2O

∂13C values of siderite from the rhythmite units (Fig. 9; Table 1) range from -9.76 to 7.74, with a mean of -9.21 +/-0.69‰ relative to PDB, which suggests a significant organic matter carbon contribution to the siderite and supports the chemical model outlined in equations a-d above. These results are consistent with siderite formed in suboxic to anoxic marine environments (Mozley and Wersin, 1992). The siderite from laminae in two upper shoreface sandstone samples have slightly more positive ∂13Cvalues with a mean of -7.86 +/-0.23‰ and, based on their more variable ∂18O values, are likely more affected by burial diagenesis. These ∂13C values fill a gap in the ∂13C chemostratigraphy and are consistent with the trends in light ∂13C values that preceded and immediately followed the Marinoan ice age (-5 to -7 ‰ Halverson et al., 2010). Many of the siderite grains contain small clusters of crystals and paragenetically later subhedral to euhedral siderite overgrowths extend into micropores (Fig. 10). Marine siderite is typically Mg- and Ca-rich with up to 41 and 15 mole %, respectively (Mozley, 1989). Small clusters of calcium-rich siderite crystallites suggest low-temperature precipitation in seawater

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(Carothers et al., 1988; Mozley, 1989) and the overgrowths are Mg-rich, which is consistent with siderite formed in seawater (Fig. 10; Mozley, 1989). Precipitation also required a sustained source of ferrous iron (reaction d), which was likely delivered through hydrothermal activity in the Jacadigo rift. A hydrothermal signature in Neoproterozoic seawater is well documented throughout the Ediacaran and was the result of relatively low oxygen levels and extensive mid-ocean-ridge activity (Huang et al., 2011). The thick Mn and Fe-rich banded iron formation of the underlying Santa Cruz Formation (Walde and Hageman, 2007) also points to an intra-rift basin hydrothermal source. Fe-redox pumping (Heggie et al., 1990; Pufahl, 2010) is another likely source of dissolved iron. Glacial and coastal erosion of exposed underlying Santa Cruz Formation iron formation would have provided an excellent source of fine-grained iron oxide and iron (oxyhydr)oxide sediment. Such detrital iron could have easily dissolved under anoxic to microaerobic water (<2.5 µmol O2/kg ; Lovely, 1991; Picardal et al., 1993; Nealson et al., 2002), especially in the presence of organic matter and would have resulted in large-scale reduction of solid Fe-(oxyhydr)oxide particles to produce dissolved ferrous iron in pore water (net reaction e). The abundant microbial microstructures found in the rhythmite units are consistent with the presence of chemosynthetic bacteria, which could further facilitate iron reduction at the seafloor (Bailey et al., 2013). Modern chemosynthetic bacteria such as Shewanella sp. produce ferrous iron at the sediment-water interface by using ferric iron in Fe-(oxyhydr)oxides as an electron acceptor to facilitate the heterotrophic breakdown of sedimentary organic matter (Lovely, 1991; Nealson et al., 2002; Bonneville et al., 2006). (e) CH2O(ORG.) + 4Fe(OH)3(S)  4Fe+2 + HCO3− + 7OH− + 3H2O

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(f) 4Fe+2 + O2 + 10H2O  4Fe(OH)3(S) + 8H+

4.2.2 Phosphate Phosphate occurs as the highly-substituted form of carbonate fluorapatite, francolite {Ca10 − a – bNaaMgb(PO4)6 − x(CO3)x − y − z(CO3,F)y(SO4)z(F2)} (Nathan, 1984). Francolite is concentrated as crinkly layers on diastem surfaces, as pore-filling cement, and as peloids (Figs. 7 & 8). Siderite and francolite are also found in irregular microbial laminae in shallow, sandy tidally influenced upper shoreface deposits throughout the Cerradinho Formation (Figs. 4 & 5). Microbially laminated francolite reflects a redox change that terminated siderite precipitation (Fig. 8). Francolite requires a higher Eh (greater O2) to form relative to siderite. Decreased methanogenesis with associated lower alkalinity likely occurred with phosphatization of the top contact of siderite layers. Francolite formed in microbial films on these surfaces, and it penetrates downward and partially filled pores in the underlying siderite (Fig. 8). This small-scale francolite accumulation contrasts to economic Neoproterozoic sedimentary phosphate occurrences such as the Sete Lagoas and Nova America formations, Brazil (Drummond et al., 2015; Caird et al., 2017), and the Doushantou Formation, China (Jiang et al., 2011). The potential for abundant fine-grained detrital iron oxide suspended sediment in the water column makes iron-redox pumping a likely transport mechanism of phosphate. Phosphate readily adsorbs onto Fe-(oxyhydr)oxide particles (Berner, 1973) and is released as these dissolve in microaerobic to anoxic water (Wallman, 2003). Through this process, iron-redox pumping probably increased pore water phosphate saturation (Heggie et al., 1990; Nelson et al., 2010; Pufahl and Groat, 2017) and supplied phosphate to chemosynthetic sulfur bacteria (Hiatt et al.,

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2015; Caird et al., 2017). Sulfur bacteria facilitate phosphogenesis (Jørgensen and Revsbech, 1983; Larkin and Strohl, 1983; Fossing et al., 1995; Arning et al., 2009; Bailey et al., 2009; Bailey et al., 2013). Limited oxidative chemical weathering in the Cryogenian (McFadden et al., 2008; Ries et al., 2009, Huang et al., 2017) would have produced seawater sulfate concentrations that were on the order of <30% of modern values (Kah et al, 2004). Nevertheless, sulfate levels may have been periodically elevated in periglacial coastal environments because sea ice formation would have created cold, sulfate-rich brines that bathed the seafloor to support communities of phosphate-concentrating, sulfur-bacteria. Chemosynthetic bacterial ecosystems were, and continue to be, critical players in the global phosphorus cycle and drive phosphate mineralization that is the hallmark of the economic phosphorite giants of the last 620 Ma (Schulz and Schulz, 2005; Bailey et al., 2013; Hiatt et al., 2015). An oxic to dysoxic water column and reducing conditions in the sediment would have favored such sulfur bacteria (similar to Beggiatoa sp., Thioploca sp.), which could have concentrated phosphate and led to francolite precipitation below the sediment-water interface (Arning et al., 2009; Froelich et al., 1988). Pyrite framboids are present in the Cerradinho Formation (Fig. 11), suggesting an authigenic microbial origin (Popa et al., 2004) and the association with francolite supports a chemosynthetic origin. It is likely that similar phosphatemineralizing chemosynthetic systems operated on seafloor environments around the world as the Snowball Earth ice ages waxed and waned.

4.2.3 Hematite Deposition of hematite laminae at the tops of rhythmite cycles records progressive water column oxygenation (Figs. 6 & 7). A rise in the concentration of photosynthetic O2 during

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deposition of single-rhythmite cycles would have resulted in increased iron precipitated as Fe(oxyhydr)oxide. The millimeter-scale changes in mineralogy that characterize the rhythmites are the products of short-term redox changes (Figs. 6 & 7).

4.3 Role of Sea Ice in Nutrient Cycling The end of iron formation deposition and appearance of francolite in the Cerradinho Formation highlights the link between the biogeochemical cycling of iron and phosphorus and oxygenation of shelf environments. Because of the very small-scale (from a few hundred microns in thickness) and the regularity of the redox changes represented by their mineralogy, these rhythmite laminae could represent biochemical varves (Fig. 6). Varves are layers deposited in an annual period (De Geer, 1912; Zolitschka et al., 2015), and can form in lakes, deep marine basins, and in evaporative basins (Kirkland, 2003; Baumgartner et al., 2013). Recent examples of glacio-lacustrine and glacio-marine varves provide a strong case for annual periodicity, whereas ancient examples of chemical varves are interpreted to represent annual cycles of inferred seasonal oceanographic changes (aridity and evaporation) (Anderson et al. 1972), with each varve consisting of two to three mineralogically distinct individual laminae (Kirkland, 2003). It is possible that these laminae represent seasonal changes in oxygen due to intensity of sunlight in a sub-ice environment. Marine phytoplankton remain productive under sea ice in the modern, albeit at lower levels, and with diminished O2 ocean-atmosphere exchange (Gosselin et al., 1997).

Although it is becoming increasingly clear that the oceans were at least partially oxygenated by the mid- to late Ediacaran during the Neoproterozoic oxygenation event (NOE; ca. 580 Ma; Canfield et al., 2008; Ochs and Shields-Zhou, 2012; Johnston et al., 2012; Kendall et

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al., 2015), it is not clear how the transition occurred. Did it occur in one major pulse following the end-Cryogenian Snowball Earth, and thus corresponded to “cap carbonate” deposition (Sahoo et al., 2012), did oxygen increase slowly throughout the Cryogenian (Cheng et al., 2018), or did it occur in a stepwise fashion as the ice sheets of the Marinoan ice age waxed and waned during the Cryogenian? The answers to these questions have profound implications for the evolution of metazoans through changes, not only in oxygen levels, but in phosphorus cycling.

Siderite likely formed in microaerobic to anoxic conditions due to limited photosynthesis under sea ice (Fig. 12; Gosselin et al., 1997); organic matter accumulation and absence of O2 may have led to methanogenesis in the sediment. Photosynthetic O2 production would have been minimal in the winter and allowed phosphate to diffuse from the sediment into the overlying water. This would have stimulated further microbial productivity and methanogenesis that likely further helped to drive siderite precipitation. Below the seafloor, microbial breakdown of organic matter in reducing porewater led to further upward diffusion of phosphate to the sediment-water interface (Froelich et al., 1988). With increased oxygen levels and suspension settling of Fe(oxyhydr)oxide mud, phosphate was trapped and fixed as francolite in microbial mats and in the sediment (Fig. 12B; Heggie et al., 1990; Reimers et al., 1996; Pufahl and Hiatt, 2012). Hematite mud layers could represent suspension settling of Fe-(oxyhydr)oxide particles on the seafloor. These layers probably represent the most intense periods of sub-ice photosynthesis and watercolumn O2 production, which may have occurred during summer (Fig. 12A). Sea ice cover would have limited photosynthesis, diminished CO2 and O2 exchange with the atmosphere, and preserved in these biochemical rhythmites. Ice cover created stable, persistent seafloor environments in which redox-driven biochemical sediments could accumulate. The resulting redox-driven rhythmites suggest that shallow benthic seafloor

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environments were on the verge of oxygenation, that phosphorus was concentrated at the seafloor, and supports the hypothesis that Cryogenian sea ice was key to limiting O2 production (Hoffman et al., 1998; Kirschvink et al., 2000; Hoffman et al., 2017). Because of the intimate connection between oxygen and the accumulation of P, the Neoproterozoic was a pivotal time for the global P-cycle (Papineau, 2010; Pufahl, 2010; Drummond et al., 2015; Caird et al., 2017). Throughout most of the Precambrian, phosphorus concentrations in marine sediments remained low compared to the those of the Phanerozoic (Planavsky et al., 2010; Reinhard et al., 2016). This changed in the Neoproterozoic as indicated by increased phosphorus concentrations measured in fine-grained marine clastic rocks (Planavsky et al., 2010; Reinhard et al., 2016), and with the first, although very rare, appearance of phosphate-biomineralized skeletal elements in the Cryogenian (Cohen et al., 2011). This is physical evidence of the evolving phosphorus and O2 cycles that led to the diversification of life including appearance of metazoans. This sub-ice Cryogenian biochemical system could serve as an analog for those envisioned elsewhere in the solar system. Sub-ice biochemical systems on Enceladus and Europa, and under the recently discovered sub-glacial water under Mars’ polar ice caps are emerging frontiers in the search for extraterrestrial life in our solar system (Orosei et al., 2018). Enceladus and Europa are “snowball worlds” that have global oceans beneath their ice-shrouded surfaces (Jia et al., 2018; Postberg et al., 2018). Recent discoveries of water vapor, salt compounds, and organic molecules in the cryo-volcanic ejecta in space surrounding Saturn’s icecovered moon Enceladus point to a biochemical origin. These discoveries raise the possibility that chemosynthetic microbes are living in the ocean underneath Enceladus’ solid ice outer shell (Postberg et al., 2018). Likewise, Jupiter’s moon Europa emits water-vapor plumes into space

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from its global sub-ice ocean that may contain information about the ocean’s composition (Jia et al., 2018). The Cryogenian sub-ice, biochemical system of the Cerradinho Formation could provide an important analog for such extraterrestrial systems as NASA and other agencies plan for multiple missions to these moons and Mars. Additionally, this intersection between the cryosphere, biosphere and geosphere holds great potential for understanding conditions that led to diversification of eukaryotes and specifically, metazoans in the Ediacaran.

5. CONCLUSIONS The end Marinoan Snowball Earth succession of southwestern Brazil records one of the most significant climate change events in Earth history. Dropstones in marine facies of the lower Corumbá Group suggest periods of sea-ice during the waning of the Cryogenian ice age and associated marine transgression. The succession records glacial melting, outwash sedimentation, sea-level rise, and marine-shelf deposition that was punctuated by ice cover prior to the development of a widespread carbonate platform (Bocaina Formation). The Cerradinho Formation is a shallow-water shelf deposit marked by dropstones, except in intervals of biochemical rhythmite. Periods of ice cover limited siliciclastic sedimentation, limited photosynthetic O2 production, and gave rise to the redox-driven microbial ecosystem that formed the rhythmite intervals. Such sub-ice depositional systems are under-appreciated facets of the Snowball Earth ice ages. The presence of francolite in the Cerradinho Formation suggests that, for the first time in Earth history, phosphate-trapping redox reactions shifted to subtidal sediments (under sea ice and in open water, shallow shelf facies). Until this transition out of the Cryogenian, phosphate had

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only been mineralized as francolite in oxygen oases that marked many Precambrian tidal flat systems. The millimeter-scale mineralogic changes in the rhythmites are interpreted to reflect short-term redox cycles in this system. It was ice cover that limited photosynthetic oxygen production, and that resulted in changes in the biogeochemical cycling of iron and phosphorus. The biochemical rhythmites suggest that O2 levels fluctuated on short time scales and that concentration of phosphorus at the seafloor preceded both the globally correlative cap carbonates of the basal Ediacaran and the later diversification of eukaryotes and metazoans. This ancient biochemical system provides an analog for ice-covered worlds in our solar system, such as Europa and Enceladus, that may host sub-ice chemosynthetic microbial life.

ACKNOWLEDGEMENTS:

We thank Vetria Ltd. for their support and access to drill cores. Rafael Henson and Fernañda Claus provided valuable help and shared their knowledge. We are grateful to Maisa B. Abram and Claudio G. Porto for thoughtful discussions that led to this synthesis, Pam Frail for making thin sections, and Brooke Vander Pas and Max Schwid for help drafting figures. Rachel Koritala made our work with the FEG-SEM at Argonne National Laboratory possible. Two anonymous reviewers provided insightful critiques that resulted in a much-improved manuscript. Funding for this project was provided by a Fulbright Fellowship, a UW-Oshkosh Faculty Development Research Grant, an Acadia University Harrison McCain fellowship, and an Argonne Center for Nanoscale Materials collaborative award to EEH; and a NSERC Discovery Grant to PKP.

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TABLES Table 1. Isotope data for individual micro-sampled siderite laminae in the Cerradinho Formation. Facies 1 samples are from ripple-cross laminated francolite peloid-bearing marine sandstone (Fig. 5). Facies 2 samples are from multiple siderite laminae within the three biochemical rhythmite units (Figs. 4 & 6).

FIGURES Figure 1. Simplified geologic map with Brazil inset. Black box on inset map encloses the area of the geologic map. Jacadigo Basin shown by diagonal ruled line area. NP = North Paraguay fold belt, SP = South Paraguay fold belt, which is coincident with the Serra do Bodoquena. Modified from Jones (1985). Figure 2. Stratigraphic relationships for the Jacadigo Basin, Corumbá area and general tectonic changes. The Cadiueus and Cerradinho are included in the Corumbá Group, and assumed to be Ediacaran, but there is no geochronology or biostratigraphic evidence. Sedimentologically, the outwash and dropstone-rich shallow-marine facies of the Cerradinho would be more logically included in the Cryogenian Jacadigo Group. Wavy red lines represent stratigraphic breaks and interpreted unconformities. Regionally, the contact between the underlying Puga Formation, and overlying units is unconformable (Freitas et al, 2011), The Puga-Cadiueus contact is well exposed in two drill cores and is marked by a surface that could reflect weathering, but the contact between the Cerradinho and Bocaina is not exposed in either outcrop of drill core and can only be inferred based on exposures in the Serra do Bodoquena region. Modified from Piacentini et al. (2007) and Babcock et al. (2005). Figure 3. Paleogeographic reconstruction for 635 Ma. Green box shows the study area. Tm = Tarim, NA = Northern Australia, SA = Southern Australia, EAnt = East Antarctica, Kal = Kalahari, Om = Oman, P = Rio de La Plata, SF = São Francisco, WAfr = West Africa, Ca = Central Asian Fold Belt, Av = Avalonia, ESv = East Svalbard, Kaz – Kazakhstan, Sib = Siberia. Modified from Hoffman et al (2017).

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Figure 4. Stratigraphic section showing details of the Cryogenian to Early Ediacaran (Bocaina Formation) transition. Based on observations we made in drill core and in regional outcrop exposures, we interpret the contact between the Jacadigo and Corumbá groups and the contact between the Cerradinho and overlying Bocaina Formation as unconformities (wavy red lines). C = clay, S = silt, Ms = medium sand, Cs = coarse sand, G = granule, P = pebble, C = cobble, and B = boulder.

Figure 5. A. Coarse-grained feldspathic arenite overlain by black siltstone typical of the unweathered Cerradinho Formation. Small dropped pebbles (Ds) and dropped diamictite (tillite) clasts (Dd), ripple cross-laminae (Rxl) are found throughout the Cerradinho, and flaser bedding (Fb) is common. On outcrop, the Cerradinho is red-brown and only the more resistant sandstone layers are preserved. B. Chloritized pebble-sized granitic (Ds) and diamictite (tillite) (Dd) dropped stones. Millimeter to centimeter-scale lamina are deformed under the large dropstone. C. Siderite-rich microbial laminae in black siltstone to fine-grained sandstone with a single dropped granitic pebble (Ds). D. Chloritized pebble-sized granitic dropped stones (Ds) in siderite (Sid) and inter-laminated siltstone-sandstone of the Cerradinho Formation. Note the deformed laminae under the large drop stone and draping ones above. Scale bars are in centimeters.

Figure 6. A. Biochemical laminae consisting of siderite (creme to light grey), hematite (brick red), and francolite (brown-tan), microbial laminae. A few coarse- to very coarse-sand-sized dropped stones (Ds) are found on a single horizon. B. Rhythmite laminae with thicker layers. Lower portion of the sample contains siderite with microbial textures similar to those seen in Figure 5C. C. Millimeter-thick microbially laminated siderite overlying ripple-cross-laminated coarse-grained feldspathic sandstone facies of the Cerradinho. This laminated siderite intervals grade upward into siderite-francolite-hematite rhythmite. Scale bars are in centimeters.

Figure 7. A. Siderite (grey), francolite (P; brown, hematite-stained dark grey) and hematite (H; red). Microbial build-up (MS) in, and on, siderite lamina (light-medium grey layers). Incidentreflected light. Scale bar = 250 µm. B. Francolite (P) occurs on the upper surfaces of the siderite

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layers (Sid) and penetrates downward from small-scale diastem surfaces. Plane-polarized transmitted light. Scale bar = 100 µm. C. Microbial build up over a diastem surface encased in siderite (Sid) with micro-peloidal texture. Crystal casts (arrows) may represent dissolved gypsum crystals. Plane-polarized transmitted light. Scale bar = 300 µm. D. Same field of view as in C, but in cross-polarized light.

Figure 8. A. Crinkly francolite (P) lamina on erosional upper surface (double arrow) on peloidal, microbially laminated siderite lamina (Sid). Opaque hematite and transparent fluoroapatite cement crystals fill fenestral porosity throughout the siderite. Area marked by white box in B. Plane-polarized light. Scale bar = 100 µm. B. EDS element map showing francolite (P) (bight green; Ca & PO4) concentrated with organic matter on the upper eroded surface of the siderite (Sid) lamina. Because calcium substitutes for iron in siderite formed in seawater (Mozley, 1989), and due to the carbonate crystal matrix, siderite appears mottled blue-green-red in this EDS image. Siderite mineralogy was confirmed with XRD. Francolite extends down from this diastem surface into pores and micro-pores and forms a sharp contact with the overlying siderite layer due to an abrupt break in the redox condition. Diagenetic hematite (H) also fills micropores (red; Fe). Scale bar = 250 µm.

Figure 9. Cerradinho Formation siderite carbon and oxygen isotope variation. Siderite laminae in biochemical rhythmites have an ca. 2 ‰ lower carbon isotopic signature due to carbon contribution from organic matter and possible methanogenesis. Isotopic values from siderite laminae in sandstone lithofacies reflect greater addition of siderite cement overgrowths formed during burial.

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Figure 10. Paragenetic relationships in biochemical rhythmite of the Cerradinho Formation. A. SEM photomicrograph using secondary electrons showing paragenetically early siderite (calcium-iron siderite; Fs) overlain by Mg-rich siderite overgrowths (Ms), apatite (A), paragenetically late quartz (Q), and pore spaces (P). B. EDS element distribution map of the same field of view as A. Scale bars = 10 µm.

Figure 11. Pyrite framboid (Pf) surrounded by chlorite in the upper shoreface facies of the Cerradinho Formation. Note paragenetically late prismatic francolite (A) crystals. SEM photomicrograph using secondary electrons. Scale bar = 10 µm.

Figure 12. Model for sub-ice deposition of the biochemical rhythmite units in the transition out of the Marinoan ice age in the Cerradinho Formation. A. Winter deposition when sea ice was thickest, sunlight and photosynthesis were at a minimum, oxygen levels were at a minimum (microaerobic to anoxic), methanogenesis occurred below the seafloor, and microbially laminated siderite formed. B. Phosphogenesis on diastem surfaces occurred as oxygen levels rose and a redox gradient was established at the seafloor and chemosynthetic bacterial mats covered the seafloor. C. Summer sea ice at a minimum, sunlight most intense, oxygen maximum concentration, with Fe-(oxyhydr)oxide particles formed by oxygenation of hydrothermally derived Fe+2. Melting of ice carrying iron-rich sediment derived from glacial erosion of the Santa Cruz Formation iron formation. Fe-(oxyhydr)oxide particles settled to the seafloor resulting in hematite mud laminae.

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Siderite Sample 4824-41.0a 4824-42.7a 4824-42.7b 4824-49.95a 4824-49.95b 4824-49.95c 4824-53.6a 4824-53.6b 4824-53.6c 4824-56.8a

Facies 1 1 1 2 2 2 2 2 2 2

δ13C (PDB) -8.13 -7.75 -7.71 -9.21 -9.23 -9.24 -9.61 -9.64 -9.76 -7.74 Mean = -8.80 +/- 0.86

δ18O (PDB) -9.84 -4.16 -4.12 -5.57 -5.35 -5.12 -5.70 -6.17 -5.39 -4.15 Mean = -5.56 +/- 1.67

Table 1. Isotope data for individual micro-sampled siderite laminae in the Cerradinho Formation. Facies 1 samples are from ripple-cross laminated francolite peloid-bearing marine sandstone (Fig. 5). Facies 2 samples are from multiple siderite laminae within the three biochemical rhythmite units (Figs. 4 & 6).

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