Light-driven anaerobic microbial oxidation of manganese.

Oxygenic photosynthesis supplies organic carbon to the modern biosphere, but it is uncertain when this metabolism originated. It has previously been proposed1,2 that photosynthetic reaction centres capable of splitting water arose by about 3 billion years ago on the basis of the inferred presence of manganese oxides in Archaean sedimentary rocks. However, this assumes that manganese oxides can be produced only in the presence of molecular oxygen3, reactive oxygen species4,5 or by high-potential photosynthetic reaction centres6,7. Here we show that communities of anoxygenic photosynthetic microorganisms biomineralize manganese oxides in the absence of molecular oxygen and high-potential photosynthetic reaction centres. Microbial oxidation of Mn(II) under strictly anaerobic conditions during the Archaean eon would have produced geochemical signals identical to those used to date the evolution of oxygenic photosynthesis before the Great Oxidation Event1,2. This light-dependent process may also produce manganese oxides in the photic zones of modern anoxic water bodies and sediments.

Microbial functional diversity across biogeochemical provinces in the central Pacific Ocean.

Enzymes catalyze key reactions within Earth's life-sustaining biogeochemical cycles. Here, we use metaproteomics to examine the enzymatic capabilities of the microbial community (0.2 to 3 µm) along a 5,000-km-long, 1-km-deep transect in the central Pacific Ocean. Eighty-five percent of total protein abundance was of bacterial origin, with Archaea contributing 1.6%. Over 2,000 functional KEGG Ontology (KO) groups were identified, yet only 25 KO groups contributed over half of the protein abundance, simultaneously indicating abundant key functions and a long tail of diverse functions. Vertical attenuation of individual proteins displayed stratification of nutrient transport, carbon utilization, and environmental stress. The microbial community also varied along horizontal scales, shaped by environmental features specific to the oligotrophic North Pacific Subtropical Gyre, the oxygen-depleted Eastern Tropical North Pacific, and nutrient-rich equatorial upwelling. Some of the most abundant proteins were associated with nitrification and C1 metabolisms, with observed interactions between these pathways. The oxidoreductases nitrite oxidoreductase (NxrAB), nitrite reductase (NirK), ammonia monooxygenase (AmoABC), manganese oxidase (MnxG), formate dehydrogenase (FdoGH and FDH), and carbon monoxide dehydrogenase (CoxLM) displayed distributions indicative of biogeochemical status such as oxidative or nutritional stress, with the potential to be more sensitive than chemical sensors. Enzymes that mediate transformations of atmospheric gases like CO, CO2, NO, methanethiol, and methylamines were most abundant in the upwelling region. We identified hot spots of biochemical transformation in the central Pacific Ocean, highlighted previously understudied metabolic pathways in the environment, and provided rich empirical data for biogeochemical models critical for forecasting ecosystem response to climate change.

Formation of Zerovalent Iron in Iron-Reducing Cultures of Methanosarcina barkeri.

Methanogenic archaea have been shown to reduce iron from ferric [Fe(III)] to ferrous [Fe(II)] state, but minerals that form during iron reduction by different methanogens remain to be characterized. Here, we show that zerovalent iron (ZVI) minerals, ferrite [α-Fe(0)] and austenite [γ-Fe(0)], appear in the X-ray diffraction spectra minutes after the addition of ferrihydrite to the cultures of a methanogenic archaeon, Methanosarcina barkeri (M. barkeri). M. barkeri cells and redox-active, nonenzymatic soluble organic compounds in organic-rich spent culture supernatants can promote the formation of ZVI; the latter compounds also likely stabilize ZVI. Methanogenic microbes that inhabit organic- and Fe(III)-rich anaerobic environments may similarly reduce Fe(III) to Fe(II) and ZVI, with implications for the preservation of paleomagnetic signals during sediment diagenesis and potential applications in the protection of iron metals against corrosion and in the green synthesis of ZVI.

Novel archaeal tetraether lipids with a cyclohexyl ring identified in Fayetteville Green Lake, NY, and other sulfidic lacustrine settings.

RATIONALE: The meromictic Fayetteville Green Lake (FGL) is of significant geobiological interest because of microbial cycling of sulfur within and below the permanent chemocline and in the euxinic deep waters. Studies of glycerol dibiphytanyl glycerol tetraethers (GDGTs) may help shed light on understanding the activity of archaeal communities in these habitats. METHODS: Normal-phase and reversed-phase liquid chromatography/mass spectrometry (LC/MS) analysis on total lipid extracts of environmental samples revealed series of GDGTs with different biphytane structures. Comparison of the mass spectrum of biphytane obtained from separated novel GDGTs with that of a synthetic C40 biphytane confirms our structural assignments. RESULTS: A unique cyclohexyl ring configured in the middle of a C40 biphytane chain was identified in these novel GDGTs. We suggest the trivial name S-GDGTs for these compounds, where 'S' stands for 'sulfidic' and 'six-membered ring'. S-GDGT derivatives composed of biphytanes modified with double bonds and cyclopentane rings were also detected in the samples we analyzed. Intact polar lipid precursors of S-GDGT include compounds with mono- and diglycosyl head groups. CONCLUSIONS: The carbon isotopic composition of S-GDGTs and their occurrence in FGL, Messel Shale as well as Salt Pond and salt marshes on Cape Cod suggest that S-GDGTs may be produced by chemoautotrophic archaea that prefer sulfidic conditions. Copyright © 2016 John Wiley & Sons, Ltd.

Predicted metabolic roles and stress responses provide insights into candidate phyla Hydrogenedentota and Sumerlaeota as members of the rare biosphere in biofilms from various environments.

Pustular mats from Shark Bay, Western Australia, host complex microbial communities bound within an organic matrix. These mats harbour many poorly characterized organisms with low relative abundances (<1%), such as candidate phyla Hydrogenedentota and Sumerlaeota. Here, we aim to constrain the metabolism and physiology of these candidate phyla by analyzing two representative metagenome-assembled genomes (MAGs) from a pustular mat. Metabolic reconstructions of these MAGs suggest facultatively anaerobic, chemoorganotrophic lifestyles of both organisms and predict that both MAGs can metabolize a diversity of carbohydrate substrates. Ca. Sumerlaeota possesses genes involved in degrading chitin, cellulose and other polysaccharides, while Ca. Hydrogenedentota can metabolize cellulose derivatives in addition to glycerol, fatty acids and phosphonates. Both Ca. phyla can respond to nitrosative stress and participate in nitrogen metabolism. Metabolic comparisons of MAGs from Shark Bay and those from various polyextreme environments (i.e., hot springs, hydrothermal vents, subsurface waters, anaerobic digesters, etc.) reveal similar metabolic capabilities and adaptations to hypersalinity, oxidative stress, antibiotics, UV radiation, nitrosative stress, heavy metal toxicity and life in surface-attached communities. These adaptations and capabilities may account for the widespread nature of these organisms and their contributions to biofilm communities in a range of extreme surface and subsurface environments.

Present-day thermal and water activity environment of the Mars Sample Return collection.

The Mars Sample Return mission intends to retrieve a sealed collection of rocks, regolith, and atmosphere sampled from Jezero Crater, Mars, by the NASA Perseverance rover mission. For all life-related research, it is necessary to evaluate water availability in the samples and on Mars. Within the first Martian year, Perseverance has acquired an estimated total mass of 355 g of rocks and regolith, and 38 µmoles of Martian atmospheric gas. Using in-situ observations acquired by the Perseverance rover, we show that the present-day environmental conditions at Jezero allow for the hydration of sulfates, chlorides, and perchlorates and the occasional formation of frost as well as a diurnal atmospheric-surface water exchange of 0.5-10 g water per m2 (assuming a well-mixed atmosphere). At night, when the temperature drops below 190 K, the surface water activity can exceed 0.5, the lowest limit for cell reproduction. During the day, when the temperature is above the cell replication limit of 245 K, water activity is less than 0.02. The environmental conditions at the surface of Jezero Crater, where these samples were acquired, are incompatible with the cell replication limits currently known on Earth.

Biophysical basis for the geometry of conical stromatolites.

Stromatolites may be Earth's oldest macroscopic fossils; however, it remains controversial what, if any, biological processes are recorded in their morphology. Although the biological interpretation of many stromatolite morphologies is confounded by the influence of sedimentation, conical stromatolites form in the absence of sedimentation and are, therefore, considered to be the most robust records of biophysical processes. A qualitative similarity between conical stromatolites and some modern microbial mats suggests a photosynthetic origin for ancient stromatolites. To better understand and interpret ancient fossils, we seek a quantitative relationship between the geometry of conical stromatolites and the biophysical processes that control their growth. We note that all modern conical stromatolites and many that formed in the last 2.8 billion years display a characteristic centimeter-scale spacing between neighboring structures. To understand this prominent-but hitherto uninterpreted-organization, we consider the role of diffusion in mediating competition between stromatolites. Having confirmed this model through laboratory experiments and field observation, we find that organization of a field of stromatolites is set by a diffusive time scale over which individual structures compete for nutrients, thus linking form to physiology. The centimeter-scale spacing between modern and ancient stromatolites corresponds to a rhythmically fluctuating metabolism with a period of approximately 20 hr. The correspondence between the observed spacing and the day length provides quantitative support for the photosynthetic origin of conical stromatolites throughout geologic time.

Assessing the Influence of HGT on the Evolution of Stress Responses in Microbial Communities from Shark Bay, Western Australia.

Pustular microbial mats in Shark Bay, Western Australia, are modern analogs of microbial systems that colonized peritidal environments before the evolution of complex life. To understand how these microbial communities evolved to grow and metabolize in the presence of various environmental stresses, the horizontal gene transfer (HGT) detection tool, MetaCHIP, was used to identify the horizontal transfer of genes related to stress response in 83 metagenome-assembled genomes from a Shark Bay pustular mat. Subsequently, maximum-likelihood phylogenies were constructed using these genes and their most closely related homologs from other environments in order to determine the likelihood of these HGT events occurring within the pustular mat. Phylogenies of several stress-related genes-including those involved in response to osmotic stress, oxidative stress and arsenic toxicity-indicate a potentially long history of HGT events and are consistent with these transfers occurring outside of modern pustular mats. The phylogeny of a particular osmoprotectant transport gene reveals relatively recent adaptations and suggests interactions between Planctomycetota and Myxococcota within these pustular mats. Overall, HGT phylogenies support a potentially broad distribution in the relative timing of the HGT events of stress-related genes and demonstrate ongoing microbial adaptations and evolution in these pustular mat communities.

A review of microbial-environmental interactions recorded in Proterozoic carbonate-hosted chert.

The record of life during the Proterozoic is preserved by several different lithologies, but two in particular are linked both spatially and temporally: chert and carbonate. These lithologies capture a snapshot of dominantly peritidal environments during the Proterozoic. Early diagenetic chert preserves some of the most exceptional Proterozoic biosignatures in the form of microbial body fossils and mat textures. This fossiliferous and kerogenous chert formed in shallow marine environments, where chert nodules, layers, and lenses are often surrounded by and encased within carbonate deposits that themselves often contain kerogen and evidence of former microbial mats. Here, we review the record of biosignatures preserved in peritidal Proterozoic chert and chert-hosting carbonate and discuss this record in the context of experimental and environmental studies that have begun to shed light on the roles that microbes and organic compounds may have played in the formation of these deposits. Insights gained from these studies suggest temporal trends in microbial-environmental interactions and place new constraints on past environmental conditions, such as the concentration of silica in Proterozoic seawater, interactions among organic compounds and cations in seawater, and the influence of microbial physiology and biochemistry on selective preservation by silicification.

Organic-rich bimineralic ooids record biological processes in Shark Bay, Western Australia.

Marine ooids have formed in microbially colonized environments for billions of years, but the microbial contributions to mineral formation in ooids continue to be debated. Here we provide evidence of these contributions in ooids from Carbla Beach, Shark Bay, Western Australia. Dark 100-240 µm diameter ooids from Carbla Beach contain two different carbonate minerals. These ooids have 50-100 µm-diameter dark nuclei that contain aragonite, amorphous iron sulfide, detrital aluminosilicate grains and organic matter, and 10-20 µm-thick layers of high-Mg calcite that separate nuclei from aragonitic outer cortices. Raman spectroscopy indicates organic enrichments in the nuclei and high-Mg calcite layers. Synchrotron-based microfocused X-ray fluorescence mapping reveals high-Mg calcite layers and the presence of iron sulfides and detrital grains in the peloidal nuclei. Iron sulfide grains within the nuclei indicate past sulfate reduction in the presence of iron. The preservation of organic signals in and around high-Mg calcite layers and the absence of iron sulfide suggest that organics stabilized high-Mg calcite under less sulfidic conditions. Aragonitic cortices that surround the nuclei and Mg-calcite layers do not preserve microporosity, iron sulfide minerals nor organic enrichments, indicating growth under more oxidizing conditions. These morphological, compositional, and mineralogical signals of microbial processes in dark ooids from Shark Bay, Western Australia, record the formation of ooid nuclei and the accretion of magnesium-rich cortical layers in benthic, reducing, microbially colonized areas.

Effects of iron and nitrogen limitation on sulfur isotope fractionation during microbial sulfate reduction.

Sulfate-reducing microbes utilize sulfate as an electron acceptor and produce sulfide that is depleted in heavy isotopes of sulfur relative to sulfate. Thus, the distribution of sulfur isotopes in sediments can trace microbial sulfate reduction (MSR), and it also has the potential to reflect the physiology of sulfate-reducing microbes. This study investigates the relationship between the availability of iron and reduced nitrogen and the magnitude of S-isotope fractionation during MSR by a marine sulfate-reducing bacterium, DMSS-1, a Desulfovibrio species, isolated from salt marsh in Cape Cod, MA. Submicromolar levels of iron increase sulfur isotope fractionation by about 50% relative to iron-replete cultures of DMSS-1. Iron-limited cultures also exhibit decreased cytochrome c-to-total protein ratios and cell-specific sulfate reduction rates (csSRR), implying changes in the electron transport chain that couples carbon and sulfur metabolisms. When DMSS-1 fixes nitrogen in ammonium-deficient medium, it also produces larger fractionation, but it occurs at faster csSRRs than in the ammonium-replete control cultures. The energy and reducing power required for nitrogen fixation may be responsible for the reverse trend between S-isotope fractionation and csSRR in this case. Iron deficiency and nitrogen fixation by sulfate-reducing microbes may lead to the large observed S-isotope effects in some euxinic basins and various anoxic sediments.

Morphological record of oxygenic photosynthesis in conical stromatolites.

Conical stromatolites are thought to be robust indicators of the presence of photosynthetic and phototactic microbes in aquatic environments as early as 3.5 billion years ago. However, phototaxis alone cannot explain the ubiquity of disrupted, curled, and contorted laminae in the crests of many Mesoproterozoic, Paleoproterozoic, and some Archean conical stromatolites. Here, we demonstrate that cyanobacterial production of oxygen in the tips of modern conical aggregates creates contorted laminae and submillimeter-to-millimeter-scale enmeshed bubbles. Similarly sized fossil bubbles and contorted laminae may be present only in the crestal zones of some conical stromatolites 2.7 billion years old or younger. This implies not only that cyanobacteria built Proterozoic conical stromatolites but also that fossil bubbles may constrain the timing of the evolution of oxygenic photosynthesis.

Metagenomic, (bio)chemical, and microscopic analyses reveal the potential for the cycling of sulfated EPS in Shark Bay pustular mats.

Cyanobacteria and extracellular polymeric substances (EPS) in peritidal pustular microbial mats have a two-billion-year-old fossil record. To understand the composition, production, degradation, and potential role of EPS in modern analogous communities, we sampled pustular mats from Shark Bay, Australia and analyzed their EPS matrix. Biochemical and microscopic analyses identified sulfated organic compounds as major components of mat EPS. Sulfur was more abundant in the unmineralized regions with cyanobacteria and less prevalent in areas that contained fewer cyanobacteria and more carbonate precipitates. Sequencing and assembly of the pustular mat sample resulted in 83 high-quality metagenome-assembled genomes (MAGs). Metagenomic analyses confirmed cyanobacteria as the primary sources of these sulfated polysaccharides. Genes encoding for sulfatases, glycosyl hydrolases, and other enzymes with predicted roles in the degradation of sulfated polysaccharides were detected in the MAGs of numerous clades including Bacteroidetes, Chloroflexi, Hydrogenedentes, Myxococcota, Verrucomicrobia, and Planctomycetes. Measurable sulfatase activity in pustular mats and fresh cyanobacterial EPS confirmed the role of sulfatases in the degradation of sulfated EPS. These findings suggest that the synthesis, modification, and degradation of sulfated polysaccharides influence microbial interactions, carbon cycling, and biomineralization processes within peritidal pustular microbial mats.

Aqueous alteration processes in Jezero crater, Mars-implications for organic geochemistry.

The Perseverance rover landed in Jezero crater, Mars, in February 2021. We used the Scanning Habitable Environments with Raman and Luminescence for Organics and Chemicals (SHERLOC) instrument to perform deep-ultraviolet Raman and fluorescence spectroscopy of three rocks within the crater. We identify evidence for two distinct ancient aqueous environments at different times. Reactions with liquid water formed carbonates in an olivine-rich igneous rock. A sulfate-perchlorate mixture is present in the rocks, which probably formed by later modifications of the rocks by brine. Fluorescence signatures consistent with aromatic organic compounds occur throughout these rocks and are preserved in minerals related to both aqueous environments.

Geological, multispectral, and meteorological imaging results from the Mars 2020 Perseverance rover in Jezero crater.

Perseverance's Mastcam-Z instrument provides high-resolution stereo and multispectral images with a unique combination of spatial resolution, spatial coverage, and wavelength coverage along the rover's traverse in Jezero crater, Mars. Images reveal rocks consistent with an igneous (including volcanic and/or volcaniclastic) and/or impactite origin and limited aqueous alteration, including polygonally fractured rocks with weathered coatings; massive boulder-forming bedrock consisting of mafic silicates, ferric oxides, and/or iron-bearing alteration minerals; and coarsely layered outcrops dominated by olivine. Pyroxene dominates the iron-bearing mineralogy in the fine-grained regolith, while olivine dominates the coarse-grained regolith. Solar and atmospheric imaging observations show significant intra- and intersol variations in dust optical depth and water ice clouds, as well as unique examples of boundary layer vortex action from both natural (dust devil) and Ingenuity helicopter-induced dust lifting. High-resolution stereo imaging also provides geologic context for rover operations, other instrument observations, and sample selection, characterization, and confirmation.

Compositionally and density stratified igneous terrain in Jezero crater, Mars.

Before Perseverance, Jezero crater's floor was variably hypothesized to have a lacustrine, lava, volcanic airfall, or aeolian origin. SuperCam observations in the first 286 Mars days on Mars revealed a volcanic and intrusive terrain with compositional and density stratification. The dominant lithology along the traverse is basaltic, with plagioclase enrichment in stratigraphically higher locations. Stratigraphically lower, layered rocks are richer in normative pyroxene. The lowest observed unit has the highest inferred density and is olivine-rich with coarse (1.5 millimeters) euhedral, relatively unweathered grains, suggesting a cumulate origin. This is the first martian cumulate and shows similarities to martian meteorites, which also express olivine disequilibrium. Alteration materials including carbonates, sulfates, perchlorates, hydrated silicates, and iron oxides are pervasive but low in abundance, suggesting relatively brief lacustrine conditions. Orbital observations link the Jezero floor lithology to the broader Nili-Syrtis region, suggesting that density-driven compositional stratification is a regional characteristic.

Reaction-diffusion model of nutrient uptake in a biofilm: theory and experiment.

Microbes in natural settings typically live attached to surfaces in complex communities called biofilms. Despite the many advantages of biofilm formation, communal living forces microbes to compete with one another for resources. Here we combine mathematical models with stable isotope techniques to test a reaction-diffusion model of competition in a photosynthetic biofilm. In this model, a nutrient is transported through the mat by diffusion and is consumed at a rate proportional to its local concentration. When the nutrient is supplied from the surface of the biofilm, the balance between diffusion and consumption gives rise to gradients of nutrient availability, resulting in gradients of nutrient uptake. To test this model, a biofilm was incubated for a fixed amount of time with an isotopically labeled nutrient that was incorporated into cellular biomass. Thus, the concentration of labeled nutrient in a cell is a measure of the mean rate of nutrient incorporation over the course of the experiment. Comparison of this measurement to the solution of the reaction-diffusion model in the biofilm confirms the presence of gradients in nutrient uptake with the predicted shape. The excellent agreement between theory and experiment lends strong support to this one-parameter model of reaction and diffusion of nutrients in a biofilm. Having validated this model empirically, we discuss how these dynamics may arise from diffusion through a reactive heterogeneous medium. More generally, this result identifies stable isotope techniques as a powerful tool to test quantitative models of chemical transport through biofilms.

Organic Electron Donors and Terminal Electron Acceptors Structure Anaerobic Microbial Communities and Interactions in a Permanently Stratified Sulfidic Lake.

The extent to which nutrients structure microbial communities in permanently stratified lakes is not well understood. This study characterized microbial communities from the anoxic layers of the meromictic and sulfidic Fayetteville Green Lake (FGL), NY, United States, and investigated the roles of organic electron donors and terminal electron acceptors in shaping microbial community structure and interactions. Bacterial communities from the permanently stratified layer below the chemocline (monimolimnion) and from enrichment cultures inoculated by lake sediments were analyzed using 16S rRNA gene sequencing. Results showed that anoxygenic phototrophs dominated microbial communities in the upper monimolimnion (21 m), which harbored little diversity, whereas the most diverse communities resided at the bottom of the lake (∼52 m). Organic electron donors explained 54% of the variation in the microbial community structure in aphotic cultures enriched on an array of organic electron donors and different inorganic electron acceptors. Electron acceptors only explained 10% of the variation, but were stronger drivers of community assembly in enrichment cultures supplemented with acetate or butyrate compared to the cultures amended by chitin, lignin or cellulose. We identified a range of habitat generalists and habitat specialists in both the water column and enrichment samples using Levin's index. Network analyses of interactions among microbial groups revealed Chlorobi and sulfate reducers as central to microbial interactions in the upper monimolimnion, while Syntrophaceae and other fermenting organisms were more important in the lower monimolimnion. The presence of photosynthetic microbes and communities that degrade chitin and cellulose far below the chemocline supported the downward transport of microbes, organic matter and oxidants from the surface and the chemocline. Collectively, our data suggest niche partitioning of bacterial communities via interactions that depend on the availability of different organic electron donors and terminal electron acceptors. Thus, light, as well as the diversity and availability of chemical resources drive community structure and function in FGL, and likely in other stratified, meromictic lakes.

A new model for silicification of cyanobacteria in Proterozoic tidal flats.

Microbial fossils preserved by early diagenetic chert provide a window into the Proterozoic biosphere, but seawater chemistry, microbial processes, and the interactions between microbes and the environment that contributed to this preservation are not well constrained. Here, we use fossilization experiments to explore the processes that preserve marine cyanobacterial biofilms by the precipitation of amorphous silica in a seawater medium that is analogous to Proterozoic seawater. These experiments demonstrate that the exceptional silicification of benthic marine cyanobacteria analogous to the oldest diagnostic cyanobacterial fossils requires interactions among extracellular polymeric substances (EPS), photosynthetically induced pH changes, magnesium cations (Mg2+ ), and >70 ppm silica.