An inorganic geochemical argument for coupled anaerobic oxidation of methane and iron reduction in marine sediments

Here, we present results from sediments collected in the Argentine Basin, a non‐steady state depositional marine system characterized by abundant oxidized iron within methane‐rich layers due to sediment reworking followed by rapid deposition. Our comprehensive inorganic data set shows that iron reduction in these sulfate and sulfide‐depleted sediments is best explained by a microbially mediated process—implicating anaerobic oxidation of methane coupled to iron reduction (Fe‐AOM) as the most likely major mechanism. Although important in many modern marine environments, iron‐driven AOM may not consume similar amounts of methane compared with sulfate‐dependent AOM. Nevertheless, it may have broad impact on the deep biosphere and dominate both iron and methane cycling in sulfate‐lean marine settings. Fe‐AOM might have been particularly relevant in the Archean ocean, >2.5 billion years ago, known for its production and accumulation of iron oxides (in iron formations) in a biosphere likely replete with methane but low in sulfate. Methane at that time was a critical greenhouse gas capable of sustaining a habitable climate under relatively low solar luminosity, and relationships to iron cycling may have impacted if not dominated methane loss from the biosphere.     

Non‐enzymatic glycolysis and pentose phosphate pathway‐like reactions in a plausible Archean ocean

The reaction sequences of central metabolism, glycolysis and the pentose phosphate pathway provide essential precursors for nucleic acids, amino acids and lipids. However, their evolutionary origins are not yet understood. Here, we provide evidence that their structure could have been fundamentally shaped by the general chemical environments in earth's earliest oceans. We reconstructed potential scenarios for oceans of the prebiotic Archean based on the composition of early sediments. We report that the resultant reaction milieu catalyses the interconversion of metabolites that in modern organisms constitute glycolysis and the pentose phosphate pathway. The 29 observed reactions include the formation and/or interconversion of glucose, pyruvate, the nucleic acid precursor ribose‐5‐phosphate and the amino acid precursor erythrose‐4‐phosphate, antedating reactions sequences similar to that used by the metabolic pathways. Moreover, the Archean ocean mimetic increased the stability of the phosphorylated intermediates and accelerated the rate of intermediate reactions and pyruvate production. The catalytic capacity of the reconstructed ocean milieu was attributable to its metal content. The reactions were particularly sensitive to ferrous iron Fe(II), which is understood to have had high concentrations in the Archean oceans. These observations reveal that reaction sequences that constitute central carbon metabolism could have been constrained by the iron‐rich oceanic environment of the early Archean. The origin of metabolism could thus date back to the prebiotic world.     

Proterozoic photosynthesis – a critical review

Chlorophyll‐based photosynthesis has fuelled the biosphere since at least the early Archean, but it was the ecological takeover of oxygenic cyanobacteria in the early Palaeoproterozoic, and of photosynthetic eukaryotes in the late Neoproterozoic, that gave rise to a recognizably modern ocean–atmosphere system. The fossil record offers a unique view of photosynthesis in deep time, but is deeply compromised by differential preservation and non‐diagnostic morphologies. The pervasively polyphyletic expression of modern cyanobacterial phenotypes means that few Proterozoic fossils are likely to be members of extant clades; rather than billion‐year stasis, their similarity to modern counterparts is better interpreted as a combination of serial convergence and extinction, facilitated by high levels of horizontal gene transfer. There are few grounds for identifying cyanobacterial akinetes or crown‐group Nostocales in the Proterozoic record. Such recognition undermines the results of various ancestral state reconstruction analyses, as well as molecular clock estimates calibrated against demonstrably problematic Proterozoic fossils. Eukaryotic organisms are likely to have acquired their (stem‐group nostocalean) photoendosymbionts/plastids by at least the Palaeoproterozoic, but remained ecologically marginalized by incumbent cyanobacteria until the late Neoproterozoic appearance of suspension‐feeding animals.     

A case study for late Archean and Proterozoic biogeochemical iron‐ and sulphur cycling in a modern habitat—the Arvadi Spring

As a consequence of Earth's surface oxygenation, ocean geochemistry changed from ferruginous (iron(II)‐rich) into more complex ferro‐euxinic (iron(II)‐sulphide‐rich) conditions during the Paleoproterozoic. This transition must have had profound implications for the Proterozoic microbial community that existed within the ocean water and bottom sediment; in particular, iron‐oxidizing bacteria likely had to compete with emerging sulphur‐metabolizers. However, the nature of their coexistence and interaction remains speculative. Here, we present geochemical and microbiological data from the Arvadi Spring in the eastern Swiss Alps, a modern model habitat for ferro‐euxinic transition zones in late Archean and Proterozoic oceans during high‐oxygen intervals, which enables us to reconstruct the microbial community structure in respective settings for this geological era. The spring water is oxygen‐saturated but still contains relatively elevated concentrations of dissolved iron(II) (17.2 ± 2.8 μM) and sulphide (2.5 ± 0.2 μM) with simultaneously high concentrations of sulphate (8.3 ± 0.04 mM). Solids consisting of quartz, calcite, dolomite and iron(III) oxyhydroxide minerals as well as sulphur‐containing particles, presumably elemental S⁰, cover the spring sediment. Cultivation‐based most probable number counts revealed microaerophilic iron(II)‐oxidizers and sulphide‐oxidizers to represent the largest fraction of iron‐ and sulphur‐metabolizers in the spring, coexisting with less abundant iron(III)‐reducers, sulphate‐reducers and phototrophic and nitrate‐reducing iron(II)‐oxidizers. 16S rRNA gene 454 pyrosequencing showed sulphide‐oxidizing Thiothrix species to be the dominating genus, supporting the results from our cultivation‐based assessment. Collectively, our results suggest that anaerobic and microaerophilic iron‐ and sulphur‐metabolizers could have coexisted in oxygenated ferro‐sulphidic transition zones of late Archean and Proterozoic oceans, where they would have sustained continuous cycling of iron and sulphur compounds.     

Formation of micro‐spherulitic barite in association with organic matter within sulfidized stromatolites of the 3.48 billion‐year‐old Dresser Formation,Pilbara Craton

The shallow marine and subaerial sedimentary and hydrothermal rocks of the ~3.48 billion‐year‐old Dresser Formation are host to some of Earth's oldest stromatolites and microbial remains. This study reports on texturally distinctive, spherulitic barite micro‐mineralization that occur in association with primary, autochthonous organic matter within exceptionally preserved, strongly sulfidized stromatolite samples obtained from drill cores. Spherulitic barite micro‐mineralization within the sulfidized stromatolites generally forms submicron‐scale aggregates that show gradations from hollow to densely crystallized, irregular to partially radiating crystalline interiors. Several barite micro‐spherulites show thin outer shells. Within stromatolites, barite micro‐spherulites are intimately associated with petrographically earliest dolomite and nano‐porous pyrite enriched in organic matter, the latter of which is a possible biosignature assemblage that hosts microbial remains. Barite spherulites are also observed within layered barite in proximity to stromatolite layers, where they are overgrown by compositionally distinct (Sr‐rich), coarsely crystalline barite that may have been sourced from hydrothermal veins at depth. Micro‐spherulitic barite, such as reported here, is not known from hydrothermal systems that exceed the upper temperature limit for life. Rather, barite with near‐identical morphology and micro‐texture is known from zones of high bio‐productivity under low‐temperature conditions in the modern oceans, where microbial activity and/or organic matter of degrading biomass controls the formation of spherulitic aggregates. Hence, the presence of micro‐spherulitic barite in the organic matter‐bearing Dresser Formation sulfidized stromatolites lend further support for a biogenic origin of these unusual, exceptionally well‐preserved, and very ancient microbialites.     

Microbial communities associated with phosphogenic sediments and phosphoclast‐associated DNA of the Benguela upwelling system

The processes that lead to the precipitation of authigenic calcium phosphate minerals in certain marine pore waters remain poorly understood. Phosphogenesis occurs in sediments beneath some oceanic upwelling zones that harbor polyphosphate‐accumulating bacteria. These bacteria are believed to concentrate phosphate in sediment pore waters, creating supersaturated conditions with respect to apatite precursors. However, the relationship between microbes and phosphorite formation is not fully resolved. To further study this association, we examined microbial community data generated from two sources: sediment cores recovered from the shelf of the Benguela upwelling region where phosphorites are currently forming, and DNA preserved within phosphoclasts recovered from a phosphorite deposit along the Benguela shelf. iTag and clone library sequencing of the 16S rRNA gene showed that many of our sediment‐hosted communities shared large numbers of phylotypes with one another, and that the same metabolic guilds were represented at localities across the shelf. Sulfate‐reducing bacteria and sulfur‐oxidizing bacteria were particularly abundant in our datasets, as were phylotypes that are known to carry out nitrification and the anaerobic oxidation of ammonium. The DNA extracted from phosphoclasts contained the signature of a distinct microbial community from those observed in the modern sediments. While some aspects of the modern and phosphoclast communities were similar, we observed both an enrichment of certain common microbial classes found in the modern phosphogenic sediments and a relative depletion of others. The phosphoclast‐associated DNA could represent a relict signature of one or more microbial assemblages that were present when the apatite or its precursors precipitated. While these taxa may or may not have contributed to the precipitation of the apatite that now hosts their genetic remains, several groups represented in the phosphoclast extract dataset have the genetic potential to metabolize polyphosphate, and perhaps modulate phosphate concentrations in pore waters where carbonate fluorapatite (or its precursors) are known to be precipitating.     

Modeling the carbon cycle in Lake Matano

Lake Matano, Indonesia, is a stratified anoxic lake with iron‐rich waters that has been used as an analogue for the Archean and early Proterozoic oceans. Past studies of Lake Matano report large amounts of methane production, with as much as 80% of primary production degraded via methanogenesis. Low δ¹³C values of DIC in the lake are difficult to reconcile with this notion, as fractionation during methanogenesis produces isotopically heavy CO₂. To help reconcile these observations, we develop a box model of the carbon cycle in ferruginous Lake Matano, Indonesia, that satisfies the constraints of CH₄ and DIC isotopic profiles, sediment composition, and alkalinity. We estimate methane fluxes smaller than originally proposed, with about 9% of organic carbon export to the deep waters degraded via methanogenesis. In addition, despite the abundance of Fe within the waters, anoxic ferric iron respiration of organic matter degrades <3% of organic carbon export, leaving methanogenesis as the largest contributor to anaerobic organic matter remineralization, while indicating a relatively minor role for iron as an electron acceptor. As the majority of carbon exported is buried in the sediments, we suggest that the role of methane in the Archean and early Proterozoic oceans is less significant than presumed in other studies.     

Evolutionary timing of the origins of mesophilic sulphate reduction and oxygenic photosynthesis: a phylogenomic dating approach

Until recently, the deep‐branching relationships in the bacterial domain have been unresolved. A new phylogenetic approach (termed compartmentalization) was able to resolve these deep‐branching relationships successfully by using a large number of genes from whole genome sequences and by reducing long branch attraction artefacts. This new, well‐resolved phylogenetic tree reveals the evolutionary relationships between diverse bacterial groups that leave important traces in the geological record. It shows that mesophilic sulphate reducers originated before the Cyanobacteria, followed by the origination of sulphur‐ and pyrite‐oxidizing bacteria after oxygen became available in the biosphere. This evolutionary pattern mirrors a similar pattern in the Palaeoproterozoic geological record. Sulphur isotopic fractionation records indicate that large‐scale bacterial sulphate reduction began in marine environments around 2.45 billion years ago (Ga), followed by rapid oxygenation of the atmosphere about 2.3 or 2.2 Ga. Oxygenation was then followed by increasing oceanic sulphate concentrations (probably owing to pyrite oxidation and continental weathering), which then resulted in the disappearance of banded iron formations by 1.8 Ga. The similarity between the phylogenetic and geological records suggests that the geochemical changes observed on the Palaeoproterozoic Earth were caused by major origination events in the mesophilic bacteria, and that these geochemical changes then caused additional origination events, such as aerobic respiration. If so, then constraints on divergence dates can be established for many microbial groups, including the Cyanobacteria, mesophilic bacteria, mesophilic sulphate reducers, methanotrophs, several anoxygenic phototrophs, as well as for mitochondrial endosymbiosis. These dates may also help to explain a large number of other changes in the geological record of the Neoarchean and Palaeoproterozoic Earth. This hypothesis, however, does not agree with the finding of cyanobacterial and eukaryote lipids at 2.7 Ga, and suggests that further work needs to be done to elucidate the discrepancies in both these areas.     

Microbial diversity and iron oxidation at Okuoku‐hachikurou Onsen,a Japanese hot spring analog of Precambrian iron formations

Banded iron formations (BIFs) are rock deposits common in the Archean and Paleoproterozoic (and regionally Neoproterozoic) sedimentary successions. Multiple hypotheses for their deposition exist, principally invoking the precipitation of iron via the metabolic activities of oxygenic, photoferrotrophic, and/or aerobic iron‐oxidizing bacteria. Some isolated environments support chemistry and mineralogy analogous to processes involved in BIF deposition, and their study can aid in untangling the factors that lead to iron precipitation. One such process analog system occurs at Okuoku‐hachikurou (OHK) Onsen in Akita Prefecture, Japan. OHK is an iron‐ and CO₂‐rich, circumneutral hot spring that produces a range of precipitated mineral textures containing fine laminae of aragonite and iron oxides that resemble BIF fabrics. Here, we have performed 16S rRNA gene amplicon sequencing of microbial communities across the range of microenvironments in OHK to describe the microbial diversity present and to gain insight into the cycling of iron, oxygen, and carbon in this ecosystem. These analyses suggest that productivity at OHK is based on aerobic iron‐oxidizing Gallionellaceae. In contrast to other BIF analog sites, Cyanobacteria, anoxygenic phototrophs, and iron‐reducing micro‐organisms are present at only low abundances. These observations support a hypothesis where low growth yields and the high stoichiometry of iron oxidized per carbon fixed by aerobic iron‐oxidizing chemoautotrophs like Gallionellaceae result in accumulation of iron oxide phases without stoichiometric buildup of organic matter. This system supports little dissimilatory iron reduction, further setting OHK apart from other process analog sites where iron oxidation is primarily driven by phototrophic organisms. This positions OHK as a study area where the controls on primary productivity in iron‐rich environments can be further elucidated. When compared with geological data, the metabolisms and mineralogy at OHK are most similar to specific BIF occurrences deposited after the Great Oxygenation Event, and generally discordant with those that accumulated before it.     

A coupled atmosphere–ecosystem model of the early Archean Earth

A coupled photochemical‐ecosystem model has been developed to simulate the early Archean biosphere. The model incorporates kinetic and nutrient limitations on biological productivity, along with constraints imposed by metabolic thermodynamics. We have used this model to predict the biogenic CH₄ flux and net primary productivity (NPP) of the marine biosphere prior to the advent of oxygenic photosynthesis. Organisms considered include chemotrophic and organotrophic methanogens, H₂‐, H₂S‐, and Fe‐using anoxygenic phototrophs, S‐reducing bacteria, CO‐using acetogens, and fermentative bacteria. CH₄ production and NPP in our model are limited by the downward flux of H₂, CO, S₈, and H₂S through the atmosphere–ocean interface and by the upwelling rate of Fe²⁺ from the deep oceans. For reasonable estimates of the supply rates of these compounds, we find that the biogenic CH₄ flux should have ranged from approximately ¹/₃ to 2.5 times the modern CH₄ flux. In the anoxic Archean atmosphere, this would have produced CH₄ concentrations of 100 ppmv to as much as 35 000 ppmv (3.5%), depending on the rate at which hydrogen escaped to space. Recent calculations indicating that hydrogen escape was slow favour the higher CH₄ concentrations. Calculated NPP is lower than in the modern oceans by a factor of at least 40. In our model, H₂‐based metabolism is moderately more productive than Fe²⁺‐based metabolism, with S‐based metabolism being considerably less productive. Internal recycling of sulphur within the surface ocean could conceivably raise rates of sulphur metabolism by a factor of 10 higher than the values predicted by our model. Although explicit climate calculations have not been performed here, our results are consistent with the idea that the Archean climate was warm, and possibly very hot. Some or most of our ecosystem scenarios are consistent with the carbon isotope record, depending on how that record is interpreted. If the conventional view is correct and organic carbon burial accounted for approximately 20% of total carbon burial during the Archean, then only two of our phototroph‐based model ecosystems are plausible. However, if a recent alternative analysis is correct and only approximately 0–10% of total buried carbon was organic, then essentially all of our anaerobic ecosystems are plausible. A better understanding of both the geochemical and the biological records is needed to better constrain our models.     

Different physiological responses of cyanobacteria to ultraviolet‐B radiation under iron‐replete and iron‐deficient conditions: Implications for underestimating the negative effects of UV‐B radiation

Iron deficiency has been considered one of the main limiting factors of phytoplankton productivity in some aquatic systems including oceans and lakes. Concomitantly, solar ultraviolet‐B radiation has been shown to have both deleterious and positive impacts on phytoplankton productivity. However, how iron‐deficient cyanobacteria respond to UV‐B radiation has been largely overlooked in aquatic systems. In this study, physiological responses of four cyanobacterial strains (Microcystis and Synechococcus), which are widely distributed in freshwater or marine systems, were investigated under different UV‐B irradiances and iron conditions. The growth, photosynthetic pigment composition, photosynthetic activity, and nonphotochemical quenching of the different cyanobacterial strains were drastically altered by enhanced UV‐B radiation under iron‐deficient conditions, but were less affected under iron‐replete conditions. Intracellular reactive oxygen species (ROS) and iron content increased and decreased, respectively, with increased UV‐B radiation under iron‐deficient conditions for both Microcystis aeruginosa FACHB 912 and Synechococcus sp. WH8102. On the contrary, intracellular ROS and iron content of these two strains remained constant and increased, respectively, with increased UV‐B radiation under iron‐replete conditions. These results indicate that iron‐deficient cyanobacteria are more susceptible to enhanced UV‐B radiation. Therefore, UV‐B radiation probably plays an important role in influencing primary productivity in iron‐deficient aquatic systems, suggesting that its effects on the phytoplankton productivity may be underestimated in iron‐deficient regions around the world.     

Planktonic marine iron oxidizers drive iron mineralization under low‐oxygen conditions

Observations of modern microbes have led to several hypotheses on how microbes precipitated the extensive iron formations in the geologic record, but we have yet to resolve the exact microbial contributions. An initial hypothesis was that cyanobacteria produced oxygen which oxidized iron abiotically; however, in modern environments such as microbial mats, where Fe(II) and O₂ coexist, we commonly find microaerophilic chemolithotrophic iron‐oxidizing bacteria producing Fe(III) oxyhydroxides. This suggests that such iron oxidizers could have inhabited niches in ancient coastal oceans where Fe(II) and O₂ coexisted, and therefore contributed to banded iron formations (BIFs) and other ferruginous deposits. However, there is currently little evidence for planktonic marine iron oxidizers in modern analogs. Here, we demonstrate successful cultivation of planktonic microaerophilic iron‐oxidizing Zetaproteobacteria from the Chesapeake Bay during seasonal stratification. Iron oxidizers were associated with low oxygen concentrations and active iron redox cycling in the oxic–anoxic transition zone (<3 μm O₂, <0.2 μm H₂S). While cyanobacteria were also detected in this transition zone, oxygen concentrations were too low to support significant rates of abiotic iron oxidation. Cyanobacteria may be providing oxygen for microaerophilic iron oxidation through a symbiotic relationship; at high Fe(II) levels, cyanobacteria would gain protection against Fe(II) toxicity. A Zetaproteobacteria isolate from this site oxidized iron at rates sufficient to account for deposition of geologic iron formations. In sum, our results suggest that once oxygenic photosynthesis evolved, microaerophilic chemolithotrophic iron oxidizers were likely important drivers of iron mineralization in ancient oceans.     

Nanoscale petrographic and geochemical insights on the origin of the Palaeoproterozoic stromatolitic phosphorites from Aravalli Supergroup,India

Stromatolites composed of apatite occur in post‐Lomagundi–Jatuli successions (late Palaeoproterozoic) and suggest the emergence of novel types of biomineralization at that time. The microscopic and nanoscopic petrology of organic matter in stromatolitic phosphorites might provide insights into the suite of diagenetic processes that formed these types of stromatolites. Correlated geochemical micro‐analyses of the organic matter could also yield molecular, elemental and isotopic compositions and thus insights into the role of specific micro‐organisms among these communities. Here, we report on the occurrence of nanoscopic disseminated organic matter in the Palaeoproterozoic stromatolitic phosphorite from the Aravalli Supergroup of north‐west India. Organic petrography by micro‐Raman and Transmission Electron Microscopy demonstrates syngeneity of the organic matter. Total organic carbon contents of these stromatolitic phosphorite columns are between 0.05 and 3.0 wt% and have a large range of δ¹³C_org values with an average of ?18.5‰ (1σ = 4.5‰). δ¹⁵N values of decarbonated rock powders are between ?1.2 and +2.7‰. These isotopic compositions point to the important role of biological N₂‐fixation and CO₂‐fixation by the pentose phosphate pathway consistent with a population of cyanobacteria. Microscopic spheroidal grains of apatite (MSGA) occur in association with calcite microspar in microbial mats from stromatolite columns and with chert in the core of diagenetic apatite rosettes. Organic matter extracted from the stromatolitic phosphorites contains a range of molecular functional group (e.g. carboxylic acid, alcohol, and aliphatic hydrocarbons) as well as nitrile and nitro groups as determined from C‐ and N‐XANES spectra. The presence of organic nitrogen was independently confirmed by a CN^? peak detected by ToF‐SIMS. Nanoscale petrography and geochemistry allow for a refinement of the formation model for the accretion and phototrophic growth of stromatolites. The original microbial biomass is inferred to have been dominated by cyanobacteria, which might be an important contributor of organic matter in shallow‐marine phosphorites.     

THE CYANOBACTERIAL CHLOROPHYLL‐BINDING‐PROTEIN ISIA ACTS TO INCREASE THE IN VIVO EFFECTIVE ABSORPTION CROSS‐SECTION OF PSI UNDER IRON LIMITATION1

Iron availability limits primary production in >30% of the world’s oceans; hence phytoplankton have developed acclimation strategies. In particular, cyanobacteria express IsiA (iron‐stress‐induced) under iron stress, which can become the most abundant chl‐binding protein in the cell. Within iron‐limited oceanic regions with significant cyanobacterial biomass, IsiA may represent a significant fraction of the total chl. We spectroscopically measured the effective cross‐section of the photosynthetic reaction center PSI (σ_PSI) in vivo and biochemically quantified the absolute abundance of PSI, PSII, and IsiA in the model cyanobacterium Synechocystis sp. PCC 6803. We demonstrate that accumulation of IsiA results in a ～60% increase in σ_PSI, in agreement with the theoretical increase in cross‐section based on the structure of the biochemically isolated IsiA‐PSI supercomplex from cyanobacteria. Deriving a chl budget, we suggest that IsiA plays a primary role as a light‐harvesting antenna for PSI. On progressive iron‐stress in culture, IsiA continues to accumulate without a concomitant increase in σ_PSI, suggesting that there may be a secondary role for IsiA. In natural populations, the potential physiological significance of the uncoupled pool of IsiA remains to be established. However, the functional role as a PSI antenna suggests that a large fraction of IsiA‐bound chl is directly involved in photosynthetic electron transport.     

Belowground carbon flux links biogeochemical cycles and resource‐use efficiency at the global scale

Nutrient limitation is pervasive in the terrestrial biosphere, although the relationship between global carbon (C) nitrogen (N) and phosphorus (P) cycles remains uncertain. Using meta‐analysis we show that gross primary production (GPP) partitioning belowground is inversely related to soil‐available N : P, increasing with latitude from tropical to boreal forests. N‐use efficiency is highest in boreal forests, and P‐use efficiency in tropical forests. High C partitioning belowground in boreal forests reflects a 13‐fold greater C cost of N acquisition compared to the tropics. By contrast, the C cost of P acquisition varies only 2‐fold among biomes. This analysis suggests a new hypothesis that the primary limitation on productivity in forested ecosystems transitions from belowground resources at high latitudes to aboveground resources at low latitudes as C‐intensive root‐ and mycorrhizal‐mediated nutrient capture is progressively replaced by rapidly cycling, enzyme‐derived nutrient fluxes when temperatures approach the thermal optimum for biogeochemical transformations.     

Archean Iron-Based Metabolism Analysis and the Photoferrotrophy-Driven Hypothesis of Microbial Magnetotaxis Origin

Despite its biological and geological significance, the origin of microbial magnetosome biomineralization, as well as the evolution of magnetotaxis, is still not well understood. Recently, the origin of magnetotaxis has been proposed to already exist in the Archean Eon. However, the Archean environment was fully anoxic. Therefore, what was the reason for the evolution of magnetotaxis in the anoxic Archean ocean and what mechanism could lead to the formation of single domain-sized magnetite nanoparticles that are a necessary condition of magnetotaxis functionality? Since the genetically controlled magnetosomes formation is extremely energetically demanding, in this review, we analyze Archean anoxic iron-based metabolism and we delineate the alternative possibilities of non-genetically controlled magnetosomes precursor origin as a necessary condition of magnetotaxis emergence. We show that coupling of anoxygenic photosynthesis with ferrous iron as an electron donor, with anaerobic respiration with ferric iron as an electron acceptor, provided sufficient material for non-genetically controlled magnetite formation. The co-evolution of cyanobacteria is suggested as the possible environmental pressure responsible for the emergence of Archean magnetotaxis. In accordance with the hypothesis of the reactive oxygen species-protective function of the first magnetosomes, we show that the formation of single domain-sized magnetite nanoparticles did not have to be initially connected with magnetotaxis origin, neither had to be genetically controlled nor intracellular. Instead, it could result from the long-lasting ambient pressure of metabolically produced extracellular iron oxide minerals in photoferrotrophs together with the emergence of local oxygen oases. The presence of oxygen could favor cells with the ability to navigate into oxic-anoxic transition zones since the oxygen was entirely toxic to Archean life. This evolutionary advantageous trait could finally result in a niche construction origin of genes responsible for intracellular magnetosome formation, which have remained preserved until today.     

Mass-independent fractionation of sulfur isotopes in sulfides from the pre-3770 Ma Isua Supracrustal Belt, West Greenland

Redox chemistry of the coupled atmosphere–hydrosphere system has coevolved with the biosphere, from global anoxia in the Archean to an oxygenated Proterozoic surface environment. However, to trace these changes to the very beginning of the rock record presents special challenges. All known Eoarchean (c. 3850–3600 Ma) volcanosedimentary successions (i.e. supracrustal rocks) are restricted to high‐grade gneissic terranes that seldom preserve original sedimentary structures and lack primary organic biomarkers. Although complicated by metamorphic overprinting, sulfur isotopes from Archean supracrustal rocks have the potential to preserve signatures of both atmospheric chemistry and metabolic fractionation from the original sediments. We present a synthesis of multiple sulfur isotope measurements (³²S, ³³S and ³⁴S) performed on sulfides from amphibolite facies banded iron‐formations (BIFs) and ferruginous garnet‐biotite (metapelitic) schists from the pre‐3770 Ma Isua Supracrustal Belt (ISB) in West Greenland. Because these data come from some of the oldest rocks of interpretable marine sedimentary origin, they provide the opportunity to (i) explore for possible biosignatures of sulfur metabolisms in early life; (ii) assess changes in atmospheric redox chemistry from ～3.8 Ga; and (iii) lay the groundwork to elucidate sulfur biogeochemical cycles on the early Earth. We find that sulfur isotope results from Isua do not unambiguously indicate microbially induced sulfur isotopic fractionation at that time. A significantly expanded data set of Δ³³S analyses for Isua dictates that the atmosphere was devoid of free oxygen at time of deposition and also shows that the effects of post‐depositional metamorphic remobilization and/or dilution can be traced in mass‐independently fractionated sulfur isotopes.     

Radiation of nitrogen‐metabolizing enzymes across the tree of life tracks environmental transitions in Earth history

Nitrogen is an essential element to life and exerts a strong control on global biological productivity. The rise and spread of nitrogen‐utilizing microbial metabolisms profoundly shaped the biosphere on the early Earth. Here, we reconciled gene and species trees to identify birth and horizontal gene transfer events for key nitrogen‐cycling genes, dated with a time‐calibrated tree of life, in order to examine the timing of the proliferation of these metabolisms across the tree of life. Our results provide new insights into the evolution of the early nitrogen cycle that expand on geochemical reconstructions. We observed widespread horizontal gene transfer of molybdenum‐based nitrogenase back to the Archean, minor horizontal transfer of genes for nitrate reduction in the Archean, and an increase in the proliferation of genes metabolizing nitrite around the time of the Mesoproterozoic (~1.5 Ga). The latter coincides with recent geochemical evidence for a mid‐Proterozoic rise in oxygen levels. Geochemical evidence of biological nitrate utilization in the Archean and early Proterozoic may reflect at least some contribution of dissimilatory nitrate reduction to ammonium (DNRA) rather than pure denitrification to N₂. Our results thus help unravel the relative dominance of two metabolic pathways that are not distinguishable with current geochemical tools. Overall, our findings thus provide novel constraints for understanding the evolution of the nitrogen cycle over time and provide insights into the bioavailability of various nitrogen sources in the early Earth with possible implications for the emergence of eukaryotic life.     

Microbes: Mini Iron Factories

Microbes have flourished in extreme habitats since beginning of the Earth and have played an important role in geological processes like weathering, mineralization, diagenesis, mineral formation and destruction. Biotic mineralization is one of the most fascinating examples of how microbes have been influencing geological processes. Iron oxidizing and reducing bacteria are capable of precipitating wide varieties of iron oxides (magnetite), carbonates (siderite) and sulphides (greigite) via controlled or induced mineralization processes. Microbes have also been considered to play an important role in the history of evolution of sedimentary rocks on Earth from the formation of banded iron formations during the Archean to modern biotic bog iron and ochre deposits. Here, we discuss the role that microbes have been playing in precipitation of iron and the role and importance of interdisciplinary studies in the field of geology and biology in solving some of the major geological mysteries.