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

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

Hydrothermal recycling of sedimentary ammonium into oceanic crust and the Archean ocean at 3.24 Ga

Funding was provided by a Natural Environment Research Council studentship (grant NE/R012253/1) to T.J. Boocock, and a National Science Foundation grant (grant EARPF 1725784) and an American Philosophical Society Lewis and Clark Grant, both to B.W. Johnson.The Archean ocean supported a diverse microbial ecosystem, yet studies suggest that seawater was largely depleted in many essential nutrients, including fixed nitrogen. This depletion was in part a consequence of inefficient nutrient recycling under anoxic conditions. Here, we show how hydrothermal fluids acted as a recycling mechanism for ammonium (NH4+) in the Archean ocean. We present elemental and stable isotope data for carbon, nitrogen, and sulfur from shales and hydrothermally altered volcanic rocks from the 3.24 Ga Panorama district in Western Australia. This suite documents the transfer of NH4+ from organic-rich sedimentary rocks into underlying sericitized dacite, similar to what is seen in hydrothermal systems today. On modern Earth, hydrothermal fluids that circulate through sediment packages are enriched in NH4+ to millimolar concentrations because they efficiently recycle organic-bound N. Our data show that a similar hydrothermal recycling process dates back to at least 3.24 Ga, and it may have resulted in localized centers of enhanced biological productivity around hydrothermal vents. Last, our data provide evidence that altered oceanic crust at 3.24 Ga was enriched in nitrogen, and, when subducted, it satisfies the elemental and isotopic source requirements for a low-N, but 15N-enriched, deep mantle nitrogen reservoir as sampled by mantle plumes.PostprintPeer reviewe

Nitrates as a potential N Supply for microbial ecosystems in a hyperarid Mars analog system

This research was funded by European Research Council (ERC) under the European Union’s Horizon 2020 Research and Innovation Programme (Grant Agreement 678812) (to M.W.C.). J.S. also acknowledges support from the China Scholarship Council (CSC).Nitrate is common in Mars sediments owing to long-term atmospheric photolysis, oxidation, and potentially, impact shock heating. The Atacama Desert in Chile, which is the driest region on Earth and rich in nitrate deposits, is used as a Mars analog in this study to explore the potential effects of high nitrate levels on growth of extremophilic ecosystems. Seven study sites sampled across an aridity gradient in the Atacama Desert were categorized into 3 clusters—hyperarid, middle, and arid sites—as defined by essential soil physical and chemical properties. Intriguingly, the distribution of nitrate concentrations in the shallow subsurface suggests that the buildup of nitrate is not solely controlled by precipitation. Correlations of nitrate with SiO2/Al2O3 and grain sizes suggest that sedimentation rates may also be important in controlling nitrate distribution. At arid sites receiving more than 10 mm/yr precipitation, rainfall shows a stronger impact on biomass than nitrate does. However, high nitrate to organic carbon ratios are generally beneficial to N assimilation, as evidenced both by soil geochemistry and enriched culturing experiments. This study suggests that even in the absence of precipitation, nitrate levels on a more recent, hyperarid Mars could be sufficiently high to benefit potentially extant Martian microorganisms.Publisher PDFPeer reviewe

Differential metamorphic effects on nitrogen isotopes in kerogen extracts and bulk rocks

This work was financially supported by a NASA Exobiology grant to RB (# NNX16AI37G), an NSF graduate student research fellowship to JZ, and a NASA postdoctoral fellowship to EES.The last decade has seen a steady rise in the number of publications on nitrogen isotopes in sedimentary rocks, which have become an established tool for investigating the evolution of life and environmental conditions. Nitrogen is contained in sedimentary rocks in two different phases: bound to kerogen or substituted in potassic minerals (mostly K-bearing phyllosilicates and feldspars). Isotopic measurements and interpretations typically focus either on kerogen extracts alone or on bulk rocks that include both phases. The community is split about which sample type more accurately captures the original composition of the biomass. To address this question, we combined nitrogen isotopes and carbon-to-nitrogen ratios with carbon-to-hydrogen ratios which act as an independent proxy for metamorphic alteration. Our results reveal that metamorphism drives kerogen-bound nitrogen isotopically lighter while silicate-bound nitrogen becomes heavier. For rocks up to greenschist facies, the isotopic effect of this internal partitioning (up to 3-4‰) is larger than the isotopic effect of metamorphic nitrogen loss from the system (up to 1-2‰). The opposite may be true for higher metamorphic grades. We conclude that for low-grade sedimentary rocks with more than 60% of their total nitrogen residing in the silicate phase the primary isotopic composition of the biomass is best approximated by the bulk rock measurement, whereas for high-grade rocks the kerogen extract may be the more accurate proxy. The isotopic difference between nitrogen phases can thus serve as a rough indicator of the degree of metamorphic alteration.PostprintPeer reviewe

Geochemical fingerprints of seawater in the Late Mesoproterozoic Midcontinent Rift, North America : life at the marine-land divide

The 1.1 Ga Midcontinent Rift (MCR) is a thick volcanic-sedimentary succession that forms a curvilinear belt through central North America and crops out along its northern apex around Lake Superior. Sedimentary units of the MCR have been long interpreted as fluvial-lacustrine and invited a number of studies on the early evolution of life in non-marine habitats. One of the key units is the siliciclastic Nonesuch Formation, thought to record deposition in a large lake. However, recent sedimentological observations indicate the presence of marine incursions. To further test this interpretation, we analysed trace element abundances in a broad suite of samples from multiple drill cores through the Nonesuch Formation. We aimed to differentiate geochemical influences of sediment provenance from post-depositional hydrothermal overprint and thereby identify authigenic enrichments in fluid-mobile elements that are indicators of primary environmental conditions. Our results reveal discrete enrichments in Mo and U in organic- and sulphide-rich horizons, which are most parsimoniously interpreted as marine signatures. This conclusion is supported by Sr/Ba ratios, which suggest mixing between freshwater and saltwater, and by rare cm-thick gypsum in the upper Copper Harbor Formation immediately below the Nonesuch rocks. The gypsum displays δ34S values of +25.9 ± 0.6‰, consistent with input of marine sulphate at least during parts of the basin's history. Collectively, our geochemical data support the sedimentological interpretation that this portion of the MCR archives a marine-influenced estuarine system. Although this conclusion rules out that microbial life documented from the MCR was living in exclusively freshwater habitats, the Nonesuch Fm and associated rocks still hold important clues about organisms that were capable of withstanding salinity gradients and bridging the gap between the marine and non-marine environments of the mid-Proterozoic.PostprintPeer reviewe

Mission to planet Earth : the first two billion years

Solar radiation and geological processes over the first few million years of Earth’s history, followed soon thereafter by the origin of life, steered our planet towards an evolutionary trajectory of long-lived habitability that ultimately enabled the emergence of complex life. We review the most important conditions and feedbacks over the first 2 billion years of this trajectory, which perhaps represent the best analogue for other habitable worlds in the galaxy. Crucial aspects included: (1) the redox state and volatile content of Earth’s building blocks, which determined the longevity of the magma ocean and its ability to degas H2O and other greenhouse gases, in particular CO2, allowing the condensation of a water ocean; (2) the chemical properties of the resulting degassed mantle, including oxygen fugacity, which would have not only affected its physical properties and thus its ability to recycle volatiles and nutrients via plate tectonics, but also contributed to the timescale of atmospheric oxygenation; (3) the emergence of life, in particular the origin of autotrophy, biological N2 fixation, and oxygenic photosynthesis, which accelerated sluggish abiotic processes of transferring some volatiles back into the lithosphere; (4) strong stellar UV radiation on the early Earth, which may have eroded significant amounts of atmospheric volatiles, depending on atmospheric CO2/N2 ratios and thus impacted the redox state of the mantle as well as the timing of life’s origin; and (5) evidence of strong photochemical effects on Earth’s sulfur cycle, preserved in the form of mass-independent sulfur isotope fractionation, and potentially linked to fractionation in organic carbon isotopes. The early Earth presents itself as an exoplanet analogue that can be explored through the existing rock record, allowing us to identify atmospheric signatures diagnostic of biological metabolisms that may be detectable on other inhabited planets with next-generation telescopes. We conclude that investigating the development of habitable conditions on terrestrial planets, an inherently complex problem, requires multi-disciplinary collaboration and creative solutions.Publisher PDFPeer reviewe

Volcanic controls on the microbial habitability of Mars‐analogue hydrothermal environments

Due to their potential to support chemolithotrophic life, relic hydrothermal systems on Mars are a key target for astrobiological exploration. We analysed water and sediments at six geothermal pools from the rhyolitic Kerlingarfjöll and basaltic Kverkfjöll volcanoes in Iceland, to investigate the localised controls on the habitability of these systems in terms of microbial community function. Our results show that host lithology plays a minor role in pool geochemistry and authigenic mineralogy, with the system geochemistry primarily controlled by deep volcanic processes. We find that by dictating pool water pH and redox conditions, deep volcanic processes are the primary control on microbial community structure and function, with water input from the proximal glacier acting as a secondary control by regulating pool temperatures. Kerlingarfjöll pools have reduced, circum-neutral CO2-rich waters with authigenic calcite-, pyrite- and kaolinite-bearing sediments. The dominant metabolisms inferred from community profiles obtained by 16S rRNA gene sequencing are methanogenesis, respiration of sulphate and sulphur (S0) oxidation. In contrast, Kverkfjöll pools have oxidised, acidic (pH 42- and high argillic alteration, resulting in Al-phyllosilicate-rich sediments. The prevailing metabolisms here are iron oxidation, sulphur oxidation and nitrification. Where analogous ice-fed hydrothermal systems existed on early Mars, similar volcanic processes would likely have controlled localised metabolic potential and thus habitability. Moreover, such systems offer several habitability advantages, including a localised source of metabolic redox pairs for chemolithotrophic microorganisms and accessible trace metals. Similar pools could have provided transient environments for life on Mars; when paired with surface or near-surface ice, these habitability niches could have persisted into the Amazonian. Additionally, they offer a confined site for biosignature formation and deposition that lends itself well to in situ robotic exploration

Selenium isotopes as a biogeochemical proxy in deep time

Funding during the compilation of this manuscript was provided by the NASA postdoctoral program.PostprintPeer reviewe