Hydrothermal vents and organic ligands sustained the Precambrian copper budget

The bioavailability of metals in the early ocean is a key parameter for understanding the evolution and expansion of Earth’s biosphere. Theoretical work suggested extremely low Zn and Cu levels in Precambrian seawater, but these predictions are not supported by recent geochemical data. One explanation for this discrepancy is a strong hydrothermal influx of metals and/or stabilisation in solution by organic ligands. Here new models are constructed to test this hypothesis for the solubility of Cu. The results show that hydrothermal vents constituted the major source of Cu to the Archean ocean, but higher ocean temperatures or higher levels of organic matter may have been needed to stabilise dissolved Cu in seawater. From the Proterozoic onwards, rivers contributed most of the marine Cu budget and concentrations were probably close to the modern range, even if the residence time of Cu in seawater was shorter than today. Biological Cu limitation was thus probably lifted in the Proterozoic, but the origin of Cu toxicity for cyanobacteria likely emerged in the Archean. The results provide a new interpretive framework for geochemical records.Publisher PDFPeer reviewe

An isotopically light nitrogen reservoir in the ocean : evidence from ferromanganese crusts

Funding: UK Nature Environment Research Council NERC (grant NE/V010824/1); Deutsche Forschungsgemeinschaft (DFG SPP1833 grant BA-2289/8-1).Ferromanganese (FeMn) oxide crusts and nodules in the deep ocean have been studied extensively in the context of critical metals and metal isotope mass balances; however, their role in the marine nitrogen cycle has been unexplored. Here we investigated a suite of hydrogenetic and diagenetic marine FeMn crusts and nodules from the Pacific to determine their isotopic signature and contribution as another N sink from the modern ocean. Our results reveal unusually low δ15N values down to −12 ‰ in some hydrogenetic crusts, paired with low δ13C values in carbonate associated with these crusts and nodules. This pattern is most parsimoniously explained by partial oxidation of ammonium (nitrification) derived from benthic biomass. Nitrification generates isotopically light nitrite, which may adhere to FeMn oxides by adsorption. In contrast, the diagenetic and hydrogenetic nodules are enriched in 15N/14N to up to +12 ‰, likely due to retention of ammonium in phyllosilicate minerals. Overall, we conclude that FeMn oxide crusts and nodules are a novel archive of microbial activity that may be preserved in the sedimentary record on Earth and possibly Mars.Publisher PDFPeer reviewe

Using modern low-oxygen marine ecosystems to understand the nitrogen cycle of the Paleo- and Mesoproterozoic oceans

CAF was funded by University of Maryland Horn Point Laboratory start-up funds.During the productive Paleoproterozoic (2.4–1.8 Ga) and less productive Mesoproterozoic (1.8–1.0 Ga), the ocean was suboxic to anoxic and multicellular organisms had not yet evolved. Here, we link geologic information about the Proterozoic ocean to microbial processes in modern low‐oxygen systems. High iron concentrations and rates of Fe cycling in the Proterozoic are the largest differences from modern oxygen‐deficient zones. In anoxic waters, which composed most of the Paleoproterozoic and ~40% of the Mesoproterozoic ocean, nitrogen cycling dominated. Rates of N2 production by denitrification and anammox were likely linked to sinking organic matter fluxes and in situ primary productivity under anoxic conditions. Additionally autotrophic denitrifiers could have used reduced iron or methane. 50% of the Mesoproterozoic ocean may have been suboxic, promoting nitrification and metal oxidation in the suboxic water and N2O and N2 production by partial and complete denitrification in anoxic zones in organic aggregates. Sulfidic conditions may have composed ~10% of the Mesoproterozoic ocean focused along continental margins. Due to low nitrate concentrations in offshore regions, anammox bacteria likely dominated N2 production immediately above sulfidic zones, but in coastal regions, higher nitrate concentrations probably promoted complete S‐oxidizing autotrophic denitrification at the sulfide interface.PostprintPeer reviewe

On-line chloride removal from ion chromatography for trace-level analyses of phosphite and other anions by coupled IC-ICPMS

This work was financially supported by a Natural Environment Research Council (NERC) Frontiers grant (NE/V010824/1) and by a Leverhulme Trust research grant (RPG-2022-313) to E.E.S.Rationale Ion chromatography (IC) combined with inductively coupled plasma mass spectrometry (ICPMS) is an ideal tool for measuring low concentrations of anionic species such as phosphite; however, the high concentration of chloride and other anions in natural solutions may negatively impact chromatographic separation and data quality. Method We developed an on-line mechanism of removing chloride from a sample within an ion chromatograph, using an additional valve and a separation column that transfers chloride to waste while phosphite and most other anions are retained. We installed this system in a coupled IC/ICPMS system (ICS6000 and Element 2 in medium-resolution mode) and determined linearity and detection limits. In addition, we measured phosphorus species by NMR for comparison as an alternative method for phosphite determination. Results Chloride was fully removed from the samples while phosphite was retained and could be analysed by IC/ICPMS. Concentrations could be measured down to 0.003 μmol/L and possibly less with good linearity over the explored range (up to 1.615 μmol/L; r2 = 0.999). In contrast, the detection limit by NMR was 6.46 μmol/L. Conclusions The on-line removal mechanism works well for simplifying sample matrices. It removes the need for costly pre-analytical sample treatment with OnGuard columns. We confirm that IC/ICPMS is the most powerful technique for quantifying phosphite in natural solutions. The new chloride-removal method may also be applicable to analyses of other anions.Publisher PDFPeer reviewe

Exploring the effects of residence time on the utility of stable isotopes and S/C ratios as proxies for ocean connectivity

Funding: UK Natural Environment Research Council - NE/V010824/1.Various geochemical proxies have been developed to determine if ancient sedimentary strata were deposited in marine or nonmarine environments. A critical parameter for proxy reliability is the residence time of aqueous species in seawater, which is rarely considered for proxies relying on stable isotopes and elemental abundance ratios. Differences in residence time may affect our ability to track geologically short-lived alternations between marine and nonmarine conditions. To test this effect for sulfur and nitrogen isotopes and sulfur/carbon ratios, we investigated a stratigraphic section in the Miocene Oberpullendorf Basin in Austria. Here, previous work revealed typical seawater-like rare earth element and yttrium (REY) systematics transitioning to nonmarine-like systematics. This shift was interpreted as a brief transition from an open marine depositional setting to a restricted embayment with a reduced level of exchange with the open ocean and possibly freshwater influence. Our isotopic results show no discernible response in carbonate-associated sulfate sulfur isotopes and carbon/sulfur abundance ratios during the interval of marine restriction inferred from the REY data, but nitrogen isotopes show a decrease by several permil. This observation is consistent with the much longer residence time of sulfate in seawater compared with REY and nitrate. Hence, this case study illustrates that the residence time is a key factor for the utility of seawater proxies. In some cases, it may make geochemical parameters more sensitive to marine water influx than paleontological observations, as in the Oberpullendorf Basin. Particular care is warranted in deep time, when marine residence times likely differ markedly from the modern.Publisher PDFPeer reviewe

Hydrothermal regeneration of ammonium as a basin-scale driver of primary productivity

Funding: This study was financially supported by a NERC research grant (NE/V010824/1), and Estonian Science Agency project PRG447 to K.KHydrothermal vents are important targets in the search for life on other planets due to their potential to generate key catalytic surfaces and organic compounds for biogenesis. Less well studied, however, is the role of hydrothermal circulation in maintaining a biosphere beyond its origin. Here we explored this question with analyses of organic carbon, nitrogen abundances, and isotopic ratios from the Paleoproterozoic Zaonega Formation (2.0 Ga), NW Russia, which is composed of interbedded sedimentary and mafic igneous rocks. Previous studies have documented mobilization of hydrocarbons, likely associated with magmatic intrusions into unconsolidated sediments. The igneous bodies are extensively hydrothermally altered. Our data reveal strong nitrogen enrichments of up to 0.6 wt.% in these altered igneous rocks, suggesting that the hydrothermal fluids carried ammonium concentrations in the millimolar range, which is consistent with some modern hydrothermal vents. Further, large isotopic offsets of approximately 10 ‰ between organic-bound and silicate-bound nitrogen are most parsimoniously explained by partial biological uptake of ammonium from the vent fluid. Our results, therefore, show that hydrothermal activity in ancient marine basins can provide a locally high flux of recycled nitrogen. Hydrothermal nutrient recycling may thus be an important mechanism for maintaining a large biosphere on anoxic worlds.PostprintPeer reviewe

Contrasting nutrient availability between marine and brackish waters in the late Mesoproterozoic : evidence from the Paranoá Group, Brazil

Funding: Natural Environment Research Council (Grant Number(s): NE/V010824/1).Understanding the delayed rise of eukaryotic life on Earth is one of the most fundamental questions about biological evolution. Numerous studies have presented evidence for oxygen and nutrient limitations in seawater during the Mesoproterozoic era, indicating that open marine settings may not have been able to sustain a eukaryotic biosphere with complex, multicellular organisms. However, many of these data sets represent restricted marine basins, which may bias our view of habitability. Furthermore, it remains untested whether rivers could have supplied significant nutrient fluxes to coastal habitats. To better characterize the sources of the major nutrients nitrogen and phosphorus, we turned to the late Mesoproterozoic Paranoá Group in Brazil (~1.1 Ga), which was deposited on a passive margin of the São Francisco craton. We present carbon, nitrogen and sulphur isotope data from an open shelf setting (Fazenda Funil) and from a brackish-water environment with significant riverine input (São Gabriel). Our results show that waters were well-oxygenated and nitrate was bioavailable in the open ocean setting at Fazenda Funil; the redoxcline appears to have been deeper and further offshore compared to restricted marine basins elsewhere in the Mesoproterozoic. In contrast, the brackish site at São Gabriel received only limited input of marine nitrate and sulphate. Nevertheless, previous reports of acritarchs reveal that this brackish-water setting was habitable to eukaryotic life. Paired with previously published cadmium isotope data, which can be used as a proxy for phosphorus cycling, our results suggest that complex organisms were perhaps not strictly dependent on marine nutrient supplies. Riverine influxes of P and possibly other nutrients likely rendered coastal waters perhaps equally habitable to the Mesoproterozoic open ocean. This conclusion supports the notion that eukaryotic organisms may have thrived in brackish or perhaps even freshwater environments.Publisher PDFPeer reviewe

Timing the evolution of phosphorus-cycling enzymes through geological time using phylogenomics

Phosphorus plays a crucial role in controlling biological productivity, but geological estimates of phosphate concentrations in the Precambrian ocean, during life’s origin and early evolution, vary over several orders of magnitude. While reduced phosphorus species may have served as alternative substrates to phosphate, their bioavailability on the early Earth remains unknown. Here, we reconstruct the phylogenomic record of life on Earth and find that phosphate transporting genes (pnas) evolved in the Paleoarchean (ca. 3.6-3.2 Ga) and are consistent with phosphate concentrations above modern levels ( > 3 µM). The first gene optimized for low phosphate levels (pstS; <1 µM) appeared around the same time or in the Mesoarchean depending on the reconstruction method. Most enzymatic pathways for metabolising reduced phosphorus emerged and expanded across the tree of life later. This includes phosphonate-catabolising CP-lyases, phosphite-oxidising pathways and hypophosphite-oxidising pathways. CP-lyases are particularly abundant in dissolved phosphate concentrations below 0.1 µM. Our results thus indicate at least local regions of declining phosphate levels through the Archean, possibly linked to phosphate-scavenging Fe(III), which may have limited productivity. However, reduced phosphorus species did not become widely used until after the Paleoproterozoic Great Oxidation Event (2.3 Ga), possibly linked to expansion of the biosphere at that time.Peer reviewe

The evolution of Earth’s biogeochemical nitrogen cycle

Financial support during the compilation of this manuscript was provided by the NASA postdoctoral program (EES), the NSF Graduate Research Fellowship Program (MAK), the Agouron Institute (MCK, RB) and the NSF FESD program (grant number 1338810, subcontract to RB).Nitrogen is an essential nutrient for all life on Earth and it acts as a major control on biological productivity in the modern ocean. Accurate reconstructions of the evolution of life over the course of the last four billion years therefore demand a better understanding of nitrogen bioavailability and speciation through time. The biogeochemical nitrogen cycle has evidently been closely tied to the redox state of the ocean and atmosphere. Multiple lines of evidence indicate that the Earth’s surface has passed in a non-linear fashion from an anoxic state in the Hadean to an oxic state in the later Phanerozoic. It is therefore likely that the nitrogen cycle has changed markedly over time, with potentially severe implications for the productivity and evolution of the biosphere. Here we compile nitrogen isotope data from the literature and review our current understanding of the evolution of the nitrogen cycle, with particular emphasis on the Precambrian. Combined with recent work on redox conditions, trace metal availability, sulfur and iron cycling on the early Earth, we then use the nitrogen isotope record as a platform to test existing and new hypotheses about biogeochemical pathways that may have controlled nitrogen availability through time. Among other things, we conclude that (a) abiotic nitrogen sources were likely insufficient to sustain a large biosphere, thus favoring an early origin of biological N2 fixation, (b) evidence of nitrate in the Neoarchean and Paleoproterozoic confirm current views of increasing surface oxygen levels at those times, (c) abundant ferrous iron and sulfide in the mid-Precambrian ocean may have affected the speciation and size of the fixed nitrogen reservoir, and (d) nitrate availability alone was not a major driver of eukaryotic evolution.PostprintPeer reviewe

Biomass recycling and Earth's early phosphorus cycle

This work was supported by NSF Graduate Research Fellowship DGE-1256082 to M.A.K., a NASA Postdoctoral Fellowship to E.E.S., NASA Exobiology grant NNX16AI37G, and NASA Astrobiology Institute grant NNA13AA93A.Phosphorus sets the pace of marine biological productivity on geological time scales. Recent estimates of Precambrian phosphorus levels suggest a severe deficit of this macronutrient, with the depletion attributed to scavenging by iron minerals. We propose that the size of the marine phosphorus reservoir was instead constrained by muted liberation of phosphorus during the remineralization of biomass. In the modern ocean, most biomass-bound phosphorus gets aerobically recycled; but a dearth of oxidizing power in Earth’s early oceans would have limited the stoichiometric capacity for remineralization, particularly during the Archean. The resulting low phosphorus concentrations would have substantially hampered primary productivity, contributing to the delayed rise of atmospheric oxygen.Publisher PDFPeer reviewe