(6) Using Precambrian Sediments as Palaeo-seawater Proxies 

Throughout much of the oceans, microbial life is not lacking for carbon, nitrogen, or oxygen; instead, it is the scarcity of essential trace nutrients such as phosphorus, iron, molybdenum, vanadium, zinc and nickel that limits microbial proliferation. This has likely been true since the dawn of life over 3.8 billion years ago, when it appears microbes began evolving elaborate metal scavenging strategies (e.g., iron-solubilising siderophores) and alternate versions of critical metallo-enzymes (e.g., V-Fe, Mo-Fe, and Fe-Fe nitrogenases) to cope with trace element limitation. The availability of trace elements in seawater is, in part, controlled by long-term geological processes, such as the gradual cooling of the upper mantle and the punctuated accumulation of atmospheric oxygen. It has also now been hypothesized that these events may have directed microbial evolution at the enzymatic level over billions of years. Accordingly, this aspect of my research programme is focused on developing a high-resolution sedimentary record of the history of marine trace element availability over deep geological time, and assessing how changing marine nutrient conditions may have directed microbial diversification, and ultimately (in the future) the rise of multicellular life. Moreover, as life evolved, so too did the Earth Surface System, so another key component to my research is understanding the interactions between the lithosphere-biosphere-hydrosphere-atmosphere through time. Specifically, I focus on two highly significant time periods in Earth’s history; (a) the evolution of marine plankton in the Eoarchean (4.0-3.7 Ga); and (b) the rise of cyanobacteria and aerobic respiration in Late Archean-Early Paleoproterozoic (2.7-2.3 Ga).

      The basis for this research is the integration of field and laboratory studies. The first component consists of the on-going collection and analyses of two contrasting marine sedimentary rocks, BIF and black shales. The BIF rock record is extensive, spanning every continent and encompassing sediments from as young as 0.5 Ga (in Uruguay) to as far back as Earth’s earliest known marine deposit (~3.85 Ga BIF in northern Quebec). Crucially, as pure authigenic chemical sediments (i.e., free of detrital contamination) that were sourced from marine hydrothermal inputs but oxidized and precipitated in the marine photic zone, BIF effectively captured the evolving elemental and isotopic signatures of bulk seawater. The black shale record, by contrast, comprise fine-grained clastic sediments with greater than 1% carbonaceous material, which accumulated under anoxic conditions. They often contain an abundance of trace metals that were sourced from continental weathering. The combination of both the BIF and black shale records, therefore, not only allows us to assess both hydrothermal and terrestrial inputs to Precambrian seawater, but it offers us a glimpse into the paleo-nutrient landscape that, as today, should have varied along an ocean transect.


(a) The Eoarchean

Relatively little is known about the environmental conditions of the oceans during the first billion (Ga) years after the formation of the Earth. This is primarily due to the scarcity of rocks older than ~ 3.5 Ga, while those that do exist are highly metamorphosed and lack fossils, hindering environmental reconstructions. There are only three well-preserved BIF whose age constraints place them firmly in (at least) the Eoarchean: Nuvvuagittuq Supracrustal Belt (northern Québec); Isua Supracrustal Belt (south western Greenland), and the Nulliak Association (northern Labrador). Most of our limited knowledge of Eoarchean seawater composition comes from the extensive study of a single formation, the Isua BIF. Recently, however, we were part of a collaborative study of the chemical sediments in the Nuvvuagittuq Supracrustal Belt in northern Quebec. This belt is at least 3.75 Ga years old, but may be as old as 4.28 Ga. Research led by my former PhD student (Aleksandra Mloszewska, now a PDF at the University of Toronto) has shown that there are two distinct chemical sedimentary units in this belt, an archetypical BIF unit, and a more silicate rich unit, the BSF (see Mloszewska et al., 2012Mloszewska et al., 2013). The precursor deposits were likely made up of layered amorphous silica and ferric oxyhydroxide gels, fine grained carbonate oozes and/or Fe-Ca-Mg rich silicate gels. Low Al2O3, TiO2, Zr, Hf and Th concentrations suggest that these units are detritus-free chemical sediments, and their REE and Y profiles suggest that they have retained their seawater-like composition despite metamorphic overprinting, with a ~0.1% contribution by high-temperature hydrothermal fluids, similar to the Isua BIF. The most significant trace element in the Nuvvuagittuq chemical sediments is Ni. Applying experimentally-derived partitioning coefficients for Ni to these absolute concentrations suggests that Earth’s earliest oceans had relatively high dissolved Ni concentrations (up to ~ 300 nM, compared to ~9 nM in modern seawater). These concentrations are sufficiently high that methane-producing bacteria (methanogens), which have high Ni requirements, could have thrived in the water column at that time. We have also begun working on the ca. 3.78 Ga Nulliak Association, a volcano-sedimentary sequence located in the Saglek Bay area of northern Labrador. 

      Coupled with fieldwork, my group has initiated microbiological and genetic experiments aimed at understanding the links between trace metal availability and the establishment of marine biogeochemical cycles. One of these projects involves the same marine cyanobacterium that we have titrated to assess surface chemical reactivity (Synechococcus sp. 7002). At present Aleksandra Mloszewska is growing sp. 7002 under high iron to test their viability; the tolerance of iron in cyanobacteria is a function of the expression of the RNA helicase gene, which occurs as a physiological adaptive response against environmental stress. She is also focusing on what role the addition of dissolved silica might play in terms of survivability at high Fe concentrations (Mloszewska et al., in review). This work is directly linked to a recent study by Dr. Elizabeth Swanner (now an Associate Professor at Iowa State) who also studied Synechococcus PCC 7002 and showed that Fe(II) is toxic to this cyanobacterium in the range of tens of µM, due to the production of damaging reactive oxygen species (ROS). The significance of this work for the Precambrian is that toxic Fe(II) concentrations were periodically supplied to the late Archean photic zone via upwelling from deep basins. She proposed that much early oxygen production occurred on platforms isolated from upwelling Fe(II) during sea-level regression (Swanner et al., 2015). Sea-level transgressions, initiated by the emplacement of large igneous provinces (LIP), drowned these “oxygen oases”. With Fe(II) toxicity as a modulating factor, the tempo of oxygen production was controlled by the growth of stable cratonic margins and the timing of plume-type volcanism.







In the late Archean, oxygen production was limited by toxic concentrations of Fe(II) in upwelling water, but semi-restricted carbonate platforms provided an oasis to cyanobacteria. (a) During a transgressive event, the redoxcline between Fe(II) and oxygen was shallow, limiting cyanobacteria to restricted waters and leading to herringbone carbonate precipitation in subtidal waters with dissolved Fe(II) concentrations >20 µM. (b) During a regression, oxygen produced by cyanobacteria living on the Fe(II)-free shelf deepened the redoxcline with Fe(II) along the slope, consistent with evidence for oxygen and higher organic carbon export in black shales. (c) Major transgressions associated with the emplacement of LIP that drowned the carbonate platforms in Fe(II) rich water, terminated carbonate deposition, and led to the deposition of oxide-facies IF. Fe(II), in water upwelling along the slope, could have been oxidized by molecular oxygen close to the platform or by the activity of Fe(II)-oxidizing anoxygenic phototrophs further away from the platform.


      A second project led by Aleksandra is focusing on the effects of ultraviolet radiation on the viability of those same cyanobacteria. In a previous study, we demonstrated that benthic cyanobacteria growing in solute-rich hydrothermal waters survived high influxes of UVC (at 254 nm) by precipitating their own biomineral sunscreen (Phoenix et al., 2001). With the design of an anaerobic ultraviolet chamber, we were able to experimentally test whether solute-rich Eoarchean seawater might similarly have protected ancient plankton (but using a broader range of wavelengths; 180-400 nm). We subsequently demonstrated that Fe(III)-Si nanoparticles and colloids, at concentrations relevant for the Archean ocean, absorb up to 73% of incoming UV-C (Mloszewska et al., in review). These aggregates would have formed within minutes of microbial or photochemical oxidation of Fe(II), and should have been abundant in seawater whenever Fe(II) was locally available. The shielding role of Archean seawater implies that vast majority of marine early marine phototrophs could have been free to be carried by currents to colonize the photic zone across the planet, as evidenced by the early fossil and geochemical rock records. In a related study, a recently graduated PhD student at Tubingen (Tina Gauger) studied whether the ferric oxyhydroxides precipitated by photoferrotrophic bacteria similarly acted as a UVC sunscreen. She found that both Rhodopseudomonas palustris TIE-1 and Rhodobacter ferrooxidans SW2 form nanometer-sized grains of ferrihydrite that are loosely attached to their cell surfaces (Gauger et al., 2015). These biogenic Fe(III) minerals were shown to protect the bacteria from UV-C irradiation, while cells grown in the absence of Fe(II) displayed diminished cell viability as a consequence of damage to their DNA. As in the previous study, this work implies that primitive Fe(II)-oxidizing bacteria would have been able to produce their own UV screen, enabling them to live in the shallow photic zone of the ancient oceans. Similarly, the nitrate-reducing Fe(II)-oxidizing microorganisms Acidovorax sp. strain BoFeN1 and strain 2AN, both common soil inhabitants, were protected from UV-C radiation by the ferrihydrite they produced during their metabolism (Gauger et al., 2016a). Interestingly, a potential second benefit for those bacteria might come from UV’s ability to photo-reduce Fe(III) to Fe(II), thereby regenerating the electron donor for nitrate-reducing (and other) Fe(II)-oxidizers.







(Left Figure) Scanning electron micrograph of the nitrate-reducing Fe(II)-oxidizing bacteria Acidovorax sp. strain BoFeN1 at the end of oxidation of ca. 8 mM Fe(II). The biomineralized cells show spiky needle or broccoli-like biomineral structures on the cell surfaces. Cells that are not fully encrusted are also present in both cultures. (Right Figure) Fe(II) oxidation (left) and NO3- reduction (right) over time by the nitrate-educing Fe(II)-oxidizer Acidovorax sp. strain BoFeN1 in cultures with acetate/nitrate/Fe(II) inoculated with inoculum that was either UV-treated (1’ UV) or non-UV-treated (no UV). The inoculum stemmed from cultures that were grown with acetate/nitrate in the absence of Fe(II) (non-encrusted) (a, d); grown with acetate/nitrate/Fe(II) (encrusted) (b, e); or grown with acetate/nitrate without Fe(II) but with added abiogenic ferrihydrite (fh) (c, f). Open symbols show data for non-UV-treated inoculum, filled symbols for 1 min UV-treated inoculum. From Gauger et al. (2016b).

(b) The Late Archean - Early Paleoproterozoic

A number of recent studies have focused on the trace element composition of BIF between 2.7 and 2.3 Ga as a means of better understanding Earth’s transition from a largely anoxic planet to one that became increasingly oxygenated (see Robbins et al., 2016 for review). The premise for this work is based on the concept originally championed by Frausto da Silva and Williams (2001) who suggested that the trace elements utilized in metalloenzymes today reflect, to some degree, the availability of trace elements in ancient seawater when those metalloenzymes first evolved. And, why BIF are ideal for this work is that many of them are almost pure chemical sediments (i.e., low detrital contamination) and thus they can track seawater composition at the time they were precipitated. The chemical archive preserved in BIF can then be exploited using the predictable nature of adsorption reactions occurring at the surface of the authigenic hydrous ferric oxides (HFO), such as ferrihydrite, that would have originally precipitated from, and equilibrated with, contemporaneous seawater. In natural systems, where trace element sequestration by HFO results from a continuum of adsorption and co-precipitation reactions, lumped-process distribution coefficient models can be used to relate the concentration of an element in the precipitate to the dissolved concentration present at the time of precipitation. In fact, this predictive aspect of HFO sorption reactions has been used to better understand the BIF record with respect to limitations on Precambrian primary productivity that may have arisen via HFO sequestration of bio-essential nutrients. Four examples are provided below.


      My initial interests in BIF as paleo-seawater proxies was based on the pioneering work of Bjerrum and Canfield (2002) who proposed that low phosphorous (P) concentrations in Archean and Paleoproterozoic BIF reflected limited marine phosphorous availability at that time, which would have reduced levels of photosynthesis and carbon burial, thereby inhibiting long-term oxygen production on the early Earth. However, a re-evaluation of the P content in BIF, that took into account the preferred sorption of Si (relative to P) to BIF precursor iron phases (e.g., ferrihydrite), demonstrated that high concentrations of dissolved Si in the Archean oceans would have decreased the amount of P sorption to BIF precursor minerals (Konhauser et al., 2007b). Indeed, Planavsky et al. (2010) demonstrated, based on P content in BIF and Phanerozoic ferrginous depists, that P concentrations appear to have been elevated in Precambrian oceans. Interestingly, a more recent evaluation of the P content in shales through time shows a different pattern, one of relatively low authigenic phosphorous burial in mud-rich depositional environments until about 800 to 700 million years ago (Reinhard et al., 2017). The most parsimonious way to reconcile these different results (based on different lithologies) is that phosphorous was in fact limited for much of the Precambrian, but due to phosphorous scavenging in anoxic, iron-rich waters, i.e., as solid phase iron phosphate minerals such as vivianite - the so-called deep-sea P trap - but not as a result on BIF depsition, as previously suggested.


(Left Figure) P/Fe molar ratios through time in iron-oxide-rich distal hydrothermal sediments and iron formations with low amounts of siliciclastic input. Open squares are individual samples; filled circles are formation averages. The P/Fe ratio reflects the size of the marine phosphate reservoir; phosphate sorption onto ferric oxyhydroxides follows a distribution coefficient (KD) relationship. The ratio is also influenced by the concentration of dissolved silica, because phosphate and silica hydroxides compete for sorption sites on ferric oxyhydroxides. Our compilation of P/Fe data suggests that there were elevated seawater phosphate concentrations in the Precambrian and a peak in phosphate levels associated with the Neoproterozoic snowball Earth glaciations. From Planavsky et al. (2010). (Right Figure) P content of fine-grained, marine siliciclastic sedimentary rocks through time. (a) Sedimentary phosphorite occurrences through time, as compiled in ref. (b) P concentrations through time for pre-Cryogenian (blue) and post-Tonian (red) samples. From Reinhard et al. (2017).


      Second, we showed that the nickel (Ni) content in BIF has changed dramatically over time, with a significant decline in molar nickel to iron ratios at 2.7 billion years ago, which we attribute to a reduced flux of Ni to the oceans as a consequence of cooling upper-mantle temperatures and decreased eruption of Ni-rich ultramafic rocks at the time. We then measured Ni partition coefficients between simulated Precambrian sea water and diverse iron hydroxides, and subsequently determined that dissolved Ni concentrations may have reached 400 nM throughout much of the Archaean eon, but dropped below 200 nM by 2.5 Ga and to modern day values (9 nM) by 550 Ma. The drop in Ni availability in the oceans around 2.7 Ga would have had profound consequences for microorganisms that depended on it, that being methane-producing bacteria called methanogens (Konhauser et al., 2009; Konhauser et al., 2015). These bacteria have a unique Ni requirement for their methane-producing enzymes, and crucially, these bacteria have been implicated in controlling oxygen levels on the ancient Earth as the methane they produced was reactive with oxygen and kept atmospheric oxygen levels low. It is possible that a Ni famine eventually led to a cascade of events that began with reduced methane production, the expansion of cyanobacteria into shallow-water settings previously occupied by methanogens, and ultimately increased oxygenic photosynthesis that tipped the atmospheric balance in favour of oxygen, the so-called Great Oxidation Event (GOE) at around 2.5 Ga.

      One possibility that we did not consider in our earlier manuscript was the potential influence of microbially-derived organic material, even though it is widely believed that bacterial phytoplankton was involved in Fe(II) oxidation and the deposition of BIF primary minerals. Accordingly, work by a former PhD student at Tubingen (Merle Eickhoff) studied the sorption of Ni to, and co-precipitation of Ni with, both biogenic ferrihydrite precipitated by the freshwater photoferrotroph Rhodobacter ferrooxidans SW2 and the marine photoferrotroph Rhodovulum iodosum, as well as chemically synthesized ferrihydrite. She observed a two- to threefold lower Ni/Fe ratio in biogenic as compared to abiogenic ferrihydrite, a pattern likely due tocompetition between Ni and organic matter for sorption sites on the mineral surface (Eickhoff et al., 2014). Based on this new data, we conclude that, if the Fe(III) minerals deposited in BIFs were – at least to some extent – biological, then the Ni concentrations in the early ocean would have been higher than previously suggested.

















(Left Figure) Molar Ni to Fe ratios in iron formation through time. This dataset has most recently been updated by Konhauser et al. (2015), who nearly doubled the points available since its initial presentation in Konhauser et al. (2009). A unidirectional decline in molar Ni/Fe is stark and robust. (Right Figure) Maximum dissolved Ni concentrations in sea water through time. Values were extrapolated from solid-phase BIF Ni/Fe data using experimentally determined Ni distribution coefficients. The three coloured areas represent maximum aqueous Ni concentrations at dissolved silica concentrations of 2.20 mM (yellow), 0.67 mM (orange) and 0 mM (red) to simulate plausible Archean seawaterconcentrations. The solid black line represents the average dissolved Ni value from time-averaged Ni/Fe ratios. The modern mean oceanic Ni concentration (9 nM) is plotted as a line. From Konhauser et al. (2009).


      The most recognized biochemical role of cobalt (Co) is its participation as a cofactor in cobalamin (vitamin B12), which is essential for a number of metalloenzymes. In previous modeling work, researchers have pointed to the antiquity of the cobalamin cofactor, suggesting that its origin somewhere between 3.5 and 2.7 Ga is consistentwith the evolution of cyanobacteria in a Co-rich ocean (Saito et al., 2003). An examination of Co concentrations in BIF (and shales, pyrite) through time suggested an expansion of the paleomarine Co reservoir between 2.8 and 1.8 Ga (Swanner et al., 2014). This conclusion is indicated by a large increase in Co/Ti ratios in BIF, euxinic shales, and pyrite relative to the evolving continental crust, with a peak in Co/Ti values observed at ~2.4 Ga. The expansion of the Co reservoir between 2.8 and 1.8 Ga may be coincident with increased mantle plume activity and associated hydrothermal inputs, and such conditions may simultaneously have allowed for the establishment of the ferruginous conditions necessary for BIF precipitation and an increase in the amount of Co introduced to the ocean. Pervasive anoxic conditions would help keep Co in solution, and as such the residence time of Co would be higher in more anoxic oceans compared to modern, well-oxygenated oceans.








(Left Figure) The Co/Ti of IF (symbols) and of evolving continental crust. Data points are from bulk (squares) and laser-ablation (circles) analyses of Precambrian Superior-type BIF (red) and Algoma-type BIF (black). Also included are Phanerozoic shallow-marine ironstones (blue) and hydrothermal and exhalative deposits (green). (Right Figure) Cobalt concentrations in pyrite (circles) from modern (open) and ancient (filled) euxinic shales, and bulk euxinic shales (squares). From Swanner et al.,(2014).


      Zinc (Zn) is amongst the most biologically important trace metals, particularly for eukaryotes, and is a component in a wide variety of metallo-peptides and polymerases. Prior to compilations of Zn data from the sedimentary proxy record, the only estimates for Zn concentrations and bioavailability came from geochemical modeling (e.g., Saito et al., 2003). This modeling work was consistent with the emergence of eukaryotic metalloenzymes and rapid diversification of eukaryotes in the Neoproterozoic following a transition from a widely anoxic ocean with expanded euxinia to a well-oxygenated ocean. This view provided a possible explanation for the delay in eukaryotic diversification. Recently, however, two studies have re-evaluated paleomarine Zn concentrations through time, and thereby its bioavailability, using the sedimentary rock record. Scott et al. (2013) focused on black shales, building from the observation that Zn/Al ratios in sediments from modern euxinic basins are positively correlated with dissolved Zn concentrations in bottom waters. Scott et al. (2013) found there was no evidence in the Precambrian black shale record to infer a depleted paleomarine Zn reservoir — because the average Zn concentration in Precambrian and Phanerozoic euxinic shales are not significantly different. Accordingly, they suggested that seawater Zn levels remained broadly uniform throughout time at near modern levels and several orders of magnitude above concentrations that would be biolimiting. This finding was bolstered by Robbins et al. (2013) who examined Zn concentrations and Zn/Fe ratios in BIF and found generally constant Zn enrichments through time. When viewed alongside updated geochemical models for Zn speciation, and considering hypothesized partitioning scenarios for Zn and Fe co-precipitation, Robbins et al. (2013) estimated a paleomarine Zn reservoir on the order of 10 nM. This value is several orders of magnitude above the ~10E−13 M concentration considered as biolimiting and is in excellent agreement with the black shale record (Scott et al., 2013). The updated view of a relatively static paleomarine Zn reservoir contradicts the findings of earlier geochemical models that linked (1) the low Zn requirements of cyanobacteria to the predicted low levels of total Zn in the Precambrian oceans, and also (2) the proliferation of eukaryotes to an increase in total Zn during the Phanerozoic. Instead, Robbins et al. (2013) suggested that the late proliferation of Zn in eukaryotic metallomes may be better linked to biologically intrinsic evolutionary factors, i.e., zinc‘s geochemical and biological evolution may be decoupled and viewed as a function of increasing need for genome regulation and diversification of Zn-binding transcription factors.





(Left Figure) Concentrations of Zn in BIF through time This version includes all available BIF data and is plotted without the removal of samples indicating detrital contamination (i.e., >1% Al2O3 or >0.1% TiO2). Even when the all samples are included, Zn/Fe ratios in BIF tend to fall in a field that spans 2–3 orders of magnitude and is relatively consistent through time. From Robbins et al. (2013). (Right Figure) Zn enrichments in euxinic black shales through time. From Scott et al. (2013).


      Evidence for the redox evolution associated with the GOE can also be borne out of BIF trace metal record, specifcally our recent work on chromium (Cr), uranium (U) and copper (Cu). For instance, a recent compilation of Cr enrichment in BIF shows a profound enrichment (as expressed by the molar Cr/Ti ratio) beginning at 2.45 Ga in the Weeli Wolli Formation (Australia), as well as the similarly aged Cauê Iron Formation (Brazil), was followed by a spike in Cr enrichment in oolitic and pisolitic ironstone associated with the ca. 2.32 Ga Timeball Hill Formation (Australia). Cr enrichment in the face of muted Cr isotope fractionation at this time points to a supply mechanism that involved predominately the reduced Cr(III) form (Konhauser et al., 2011). Given the insolubility of Cr minerals, its mobilisation and incorporation into BIF indicates enhanced chemical weathering at that time. We suggest that only the oxidation of an abundant and previously stable crustal pyrite reservoir by aerobic-respiring, chemolithoautotrophic bacteria could have generated the degree of acidity required to solubilise Cr(III) from ultramafic source rocks and residual soils [reaction 1].

[1]     FeS2 + 14Fe3+ + 8H2O                15Fe2+ + 2SO42− + 16H+

Such an acid-generated attack would have enhanced in-situ dissolution of Cr-bearing crustal minerals (including soils) that previously retained Cr under anoxic, but pH-neutral conditions, leading to increased continental Cr(III) supply to the oceans; this process would also have led to an increased supply of dissolved sulphate and sulphide-hosted trace elements to the oceans around that time. Accordingly, it has been suggested that the Cr enrichment beginning at ca. 2.45 Ga reflects Earth's first acidic continental rock drainage, whereby acidity was generated with rising O2 at unprecedented scales via the oxidation of a previously untapped terrestrial pyrite reservoir. This process continued perhaps for 150–200 m.y. – the crustal half-life - until the volume of easily oxidisable pyrite in the weathered crust was diminished. Interestingly, not all BIF in this time window display elevated Cr enrichments (e.g., Dales Gorge and Joffre members of the Brockman Iron Formation, Australia). Considering the low solubility of Cr(III) at marine pH levels, the rapid reduction of Cr(VI) by aqueous Fe(II), and near-instantaneous co-precipitation of Cr(III) with Fe(III)-oxyhydroxide, dissolved Cr dispersal would be limited upon delivery to the oceans. In this regard, proximity of the depositional site to shore played a strong role in determining which BIF would record a continental Cr input. Indeed, BIF having some of the highest Cr values, such as the Cauê and Timeball Hill formations, show evidence of sediment reworking and grade into granular iron formations (GIF), indicative of shallow-water deposition.

















(Left Figure) Authigenic Cr enrichments in the IF record. Squares denote bulk analyses, circles are laser ablation analyses, black represents Algoma-type iron formations intimately related to submarine volcanism, red denotes Superior-type iron formations that formed in continental shelf environments, blue indicates Proterozoic oolitic iron formations and Phanerozoic ironstones that formed in shallow marine waters, and green represents Phanerozoic hydrothermal and exhalative deposits. Increased Cr concentrations and authigenic enrichments between 2.48 and 2.32 Gyr ago are related to increased Cr(III) inputs to sea water, and correspond to intense acidity generated by oxidative weathering of an untapped crustal pyrite reservoir. From Konhauser et al. (2011). (Left Figure) River/marine mixing model, indicating alteration pH necessary to supply sufficient Cr to account for Cr enrichment in the Timeball Hill Formation. The model is conservatively based on the lower end of Cr enrichment reported for the Timeball Hill Formation, specifically mean Cr (197 ppm) and Fe (47 wt%) values. Black lines, mixing trajectories for Fe-bearing marine waters contributing a total of 10 ppm Fe, and river water bearing different proportions of Cr leachate, in which Cr concentration is limited as a function of pH by amorphous Cr(OH)9  solubility. Light blue shaded area, plausible leachate contributions and mixing ratios that are realistic for the deposition of Timeball Hill Formation. The green to yellow transition indicates the dependence of inorganic pyrite oxidation on pH, and the approximate pH threshold below which aerobic microbial Fe(II) oxidation is required to sustain pyrite oxidation. The mixing model confirms that aerobic microbial Fe(II) oxidation was required to account for the low alteration pH and Cr mobilisation even for Timeball Hill Formation samples with the lowest degrees of Cr enrichment. From Konhauser et al. (2011).



      Evidence for increased oxidative weathering of the continents is also supported by recent compilations of Cu and U in Precambrian marine sediments. Although the Cu concentration record presented by Chi Fru et al. (2016) for BIF and shales is relatively constant in terms of abundance – reminiscent of the Zn record – there is a clear trend in the stable isotopes values of Cu that appears to be due to variations in Cu sinks and sources. Before the GOE, the preferential sequestration of 65Cu by Fe(III)-oxyhydroxides during BIF precipitation likely enriched seawater in residual 63Cu, which would have been incorporated into planktonic biomass and ultimately deposited into black shales depleted in 65Cu. After the GOE, oxidative continental weathering of sulfides should have increased the supply of dissolved Cu(II) and delivered more 65Cu–rich runoff to the oceans, while at the same time the isotopically light sink associated with Fe(III)-oxyhydroxides waned. As a result, Cu isotopes in black shales became progressively heavier. This evolution towards heavy δ65Cu values coincides with a shift to negative sedimentary δ56Fe values and increased marine sulfate after the GOE, and is traceable through Phanerozoic black shales to modern marine settings, where marine dissolved and sedimentary δ65Cu values are universally positive.















(A) Box and whisker isotopic plot of δ65Cu showing a transition to heavier values with the onset of the GOE. (B) Copper distribution in BIF throughout Earth history. 



      In a similar manner, temporal changes in U abundances in the BIF and black shale datasets provide highly complementary records that document the rise and accumulation of O2 associated with the GOE and yield insights into post-GOE oxygen dynamics (Partin et al., 2013a; Partin et al., 2013b). An increase in U concentration and U/Fe ratios is observed in the BIF record around 2.47–2.43 Ga and appears to mark the onset of the GOE—corroborated by a peak in both BIF and black shale U concentrations by 2.32 Ga. Following this initial peak, U and U/Fe ratios in the BF record return to low levels during the late Paleoproterozoic (post 2.05 Ga), until an increase is observed in Neoproterozoic IF and Phanerozoic ironstones. In contrast to conventional models predicting a unidirectional oxygen rise, the U record demonstrates rises and falls, tracking a more complex redox fabric in the Proterozoic atmosphere-ocean system.

(Left Figure) Secular variations in U content as recorded by BIF, reflecting the evolution of the marine U cycle. Data for all samples passing compositional filters, grouped based on iron formation classification (Algoma-type, Superior-type, Ironstone, and Phanerozoic hydrothermal) as well as analysis type (bulk—squares; laser ablation—circles). Samples failing filters relative to metamorphic grade or association with VMS deposits are highlighted with yellow stars. From Partin et al. (2013a). (Left Figure) U enrichments in organic-rich shales through time. Green bar at the base of the figure indicates average continental crust value (2.7 ppm). The U shale record suggests that the redox history of the Precambrian atmosphere–ocean system is characterized by both increases and decreases in atmospheric oxygen level linked to the burial of organic carbon, as shown by the secular variation in carbon isotope composition of carbonates (gray band, modified from Karhu (1999)). From Partin et al. (2013b).

      Lastly, the complexity in O2 dynamics is perhaps most clearly displayed in a study that compared the differing redox behaviour of Mo and Cr. By coupling a large database of sedimentary enrichments to a mass balance approach that includes a first-order description of spatially variant metal burial rates, Reinhard et al. (2013) found that the Mo and Cr record necessitates a Proterozoic ocean that was pervasively anoxic relative to the Phanerozoic (at a minimum of ~40-50% of modern seafloor area and potentially much more) but was characterised by a relatively small extent of euxinic seafloor (less than ~1-10% of modern seafloor area). His model also suggests that the oceanic Mo reservoir is extremely sensitive to very small perturbations in the extent of sulphidic seafloor and that the record of Mo and Cr enrichments through time is fully consistent with the possibility of a Mo co-limited marine biosphere during many periods of Earth’s history, including the mid-Proterozoic.