Physiology, Not Nutrient Availability, May Have Limited Primary Productivity After the Emergence of Oxygenic Photosynthesis.

The evolution of oxygenic photosynthesis in Cyanobacteria was a transformative event in Earth's history. However, the scientific community disagrees over the duration of the delay between the origin of oxygenic photosynthesis and oxygenation of Earth's atmosphere, with estimates ranging from less than a hundred thousand to more than a billion years, depending on assumptions about rates of oxygen production and fluxes of reductants. Here, we propose a novel ecological hypothesis that a geologically significant delay could have been caused by biomolecular inefficiencies within proto-Cyanobacteria-ancestors of modern Cyanobacteria-that limited their maximum rates of oxygen production. Consideration of evolutionary processes and genomic data suggest to us that proto-cyanobacterial primary productivity was initially limited by photosystem instability, oxidative damage, and photoinhibition rather than nutrients or ecological competition. We propose that during the Archean era, cyanobacterial photosystems experienced protracted evolution, with biomolecular inefficiencies initially limiting primary productivity and oxygen production. Natural selection led to increases in efficiency and thus primary productivity through time. Eventually, evolutionary advances produced sufficient biomolecular efficiency that environmental factors, such as nutrient availability, limited primary productivity and shifted controls on oxygen production from physiological to environmental limitations. If correct, our novel hypothesis predicts a geologically significant interval of time between the first local oxygen production and sufficient production for oxygenation of environments. It also predicts that evolutionary rates were likely highly variable due to strong environmental selection pressures and potentially high mutation rates but low competitive interactions.

Oxygenation of Earth's atmosphere induced metabolic and ecologic transformations recorded in the Lomagundi-Jatuli carbon isotopic excursion.

The oxygenation of Earth's atmosphere represents the quintessential transformation of a planetary surface by microbial processes. In turn, atmospheric oxygenation transformed metabolic evolution; molecular clock models indicate the diversification and ecological expansion of respiratory metabolisms in the several hundred million years following atmospheric oxygenation. Across this same interval, the geological record preserves 13C enrichment in some carbonate rocks, called the Lomagundi-Jatuli excursion (LJE). By combining data from geologic and genomic records, a self-consistent metabolic evolution model emerges for the LJE. First, fermentation and methanogenesis were major processes remineralizing organic carbon before atmospheric oxygenation. Once an ozone layer formed, shallow water and exposed environments were shielded from UVB/C radiation, allowing the expansion of cyanobacterial primary productivity. High primary productivity and methanogenesis led to preferential removal of 12C into organic carbon and CH4. Extreme and variable 13C enrichments in carbonates were caused by 13C-depleted CH4 loss to the atmosphere. Through time, aerobic respiration diversified and became ecologically widespread, as did other new metabolisms. Respiration displaced fermentation and methanogenesis as the dominant organic matter remineralization processes. As CH4 loss slowed, dissolved inorganic carbon in shallow environments was no longer highly 13C enriched. Thus, the loss of extreme 13C enrichments in carbonates marks the establishment of a new microbial mat ecosystem structure, one dominated by respiratory processes distributed along steep redox gradients. These gradients allowed the exchange of metabolic by-products among metabolically diverse organisms, providing novel metabolic opportunities. Thus, the microbially induced oxygenation of Earth's atmosphere led to the transformation of microbial ecosystems, an archetypal example of planetary microbiology.IMPORTANCEThe oxygenation of Earth's atmosphere represents the most extensive known chemical transformation of a planetary surface by microbial processes. In turn, atmospheric oxygenation transformed metabolic evolution by providing oxidants independent of the sites of photosynthesis. Thus, the evolutionary changes during this interval and their effects on planetary-scale biogeochemical cycles are fundamental to our understanding of the interdependencies among genomes, organisms, ecosystems, elemental cycles, and Earth's surface chemistry through time.

Metagenome-assembled bacterial genomes from benthic microbial mats in ice-covered Lake Vanda, Antarctica.

We recovered 57 bacterial metagenome-assembled genomes (MAGs) from benthic microbial mat pinnacles from Lake Vanda, Antarctica. These MAGs provide access to genomes from polar environments and can assist in culturing and utilizing these Antarctic bacteria.

Biogeographic distribution of five Antarctic cyanobacteria using large-scale k-mer searching with sourmash branchwater.

Cyanobacteria form diverse communities and are important primary producers in Antarctic freshwater environments, but their geographic distribution patterns in Antarctica and globally are still unresolved. There are however few genomes of cultured cyanobacteria from Antarctica available and therefore metagenome-assembled genomes (MAGs) from Antarctic cyanobacteria microbial mats provide an opportunity to explore distribution of uncultured taxa. These MAGs also allow comparison with metagenomes of cyanobacteria enriched communities from a range of habitats, geographic locations, and climates. However, most MAGs do not contain 16S rRNA gene sequences, making a 16S rRNA gene-based biogeography comparison difficult. An alternative technique is to use large-scale k-mer searching to find genomes of interest in public metagenomes. This paper presents the results of k-mer based searches for 5 Antarctic cyanobacteria MAGs from Lake Fryxell and Lake Vanda, assigned the names Phormidium pseudopriestleyi FRX01, Microcoleus sp. MP8IB2.171, Leptolyngbya sp. BulkMat.35, Pseudanabaenaceae cyanobacterium MP8IB2.15, and Leptolyngbyaceae cyanobacterium MP9P1.79 in 498,942 unassembled metagenomes from the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA). The Microcoleus sp. MP8IB2.171 MAG was found in a wide variety of environments, the P. pseudopriestleyi MAG was found in environments with challenging conditions, the Leptolyngbyaceae cyanobacterium MP9P1.79 MAG was only found in Antarctica, and the Leptolyngbya sp. BulkMat.35 and Pseudanabaenaceae cyanobacterium MP8IB2.15 MAGs were found in Antarctic and other cold environments. The findings based on metagenome matches and global comparisons suggest that these Antarctic cyanobacteria have distinct distribution patterns ranging from locally restricted to global distribution across the cold biosphere and other climatic zones.

Genomic profiles of four novel cyanobacteria MAGs from Lake Vanda, Antarctica: insights into photosynthesis, cold tolerance, and the circadian clock.

Cyanobacteria in polar environments face environmental challenges, including cold temperatures and extreme light seasonality with small diurnal variation, which has implications for polar circadian clocks. However, polar cyanobacteria remain underrepresented in available genomic data, and there are limited opportunities to study their genetic adaptations to these challenges. This paper presents four new Antarctic cyanobacteria metagenome-assembled genomes (MAGs) from microbial mats in Lake Vanda in the McMurdo Dry Valleys in Antarctica. The four MAGs were classified as Leptolyngbya sp. BulkMat.35, Pseudanabaenaceae cyanobacterium MP8IB2.15, Microcoleus sp. MP8IB2.171, and Leptolyngbyaceae cyanobacterium MP9P1.79. The MAGs contain 2.76 Mbp - 6.07 Mbp, and the bin completion ranges from 74.2-92.57%. Furthermore, the four cyanobacteria MAGs have average nucleotide identities (ANIs) under 90% with each other and under 77% with six existing polar cyanobacteria MAGs and genomes. This suggests that they are novel cyanobacteria and demonstrates that polar cyanobacteria genomes are underrepresented in reference databases and there is continued need for genome sequencing of polar cyanobacteria. Analyses of the four novel and six existing polar cyanobacteria MAGs and genomes demonstrate they have genes coding for various cold tolerance mechanisms and most standard circadian rhythm genes with the Leptolyngbya sp. BulkMat.35 and Leptolyngbyaceae cyanobacterium MP9P1.79 contained kaiB3, a divergent homolog of kaiB.

Phylogeny and Evolutionary History of Respiratory Complex I Proteins in Melainabacteria.

The evolution of oxygenic photosynthesis was one of the most transformative evolutionary events in Earth's history, leading eventually to the oxygenation of Earth's atmosphere and, consequently, the evolution of aerobic respiration. Previous work has shown that the terminal electron acceptors (complex IV) of aerobic respiration likely evolved after the evolution of oxygenic photosynthesis. However, complex I of the respiratory complex chain can be involved in anaerobic processes and, therefore, may have pre-dated the evolution of oxygenic photosynthesis. If so, aerobic respiration may have built upon respiratory chains that pre-date the rise of oxygen in Earth's atmosphere. The Melainabacteria provide a unique opportunity to examine this hypothesis because they contain genes for aerobic respiration but likely diverged from the Cyanobacteria before the evolution of oxygenic photosynthesis. Here, we examine the phylogenies of translated complex I sequences from 44 recently published Melainabacteria metagenome assembled genomes and genomes from other Melainabacteria, Cyanobacteria, and other bacterial groups to examine the evolutionary history of complex I. We find that complex I appears to have been present in the common ancestor of Melainabacteria and Cyanobacteria, supporting the idea that aerobic respiration built upon respiratory chains that pre-date the evolution of oxygenic photosynthesis and the rise of oxygen.

Metabolic Capacity of the Antarctic Cyanobacterium Phormidium pseudopriestleyi That Sustains Oxygenic Photosynthesis in the Presence of Hydrogen Sulfide.

Sulfide inhibits oxygenic photosynthesis by blocking electron transfer between H2O and the oxygen-evolving complex in the D1 protein of Photosystem II. The ability of cyanobacteria to counter this effect has implications for understanding the productivity of benthic microbial mats in sulfidic environments throughout Earth history. In Lake Fryxell, Antarctica, the benthic, filamentous cyanobacterium Phormidium pseudopriestleyi creates a 1-2 mm thick layer of 50 µmol L-1 O2 in otherwise sulfidic water, demonstrating that it sustains oxygenic photosynthesis in the presence of sulfide. A metagenome-assembled genome of P. pseudopriestleyi indicates a genetic capacity for oxygenic photosynthesis, including multiple copies of psbA (encoding the D1 protein of Photosystem II), and anoxygenic photosynthesis with a copy of sqr (encoding the sulfide quinone reductase protein that oxidizes sulfide). The genomic content of P. pseudopriestleyi is consistent with sulfide tolerance mechanisms including increasing psbA expression or directly oxidizing sulfide with sulfide quinone reductase. However, the ability of the organism to reduce Photosystem I via sulfide quinone reductase while Photosystem II is sulfide-inhibited, thereby performing anoxygenic photosynthesis in the presence of sulfide, has yet to be demonstrated.

Importance of environmental factors over habitat connectivity in shaping bacterial communities in microbial mats and bacterioplankton in an Antarctic freshwater system.

Freshwater ecosystems are considered hotspots of biodiversity in Antarctic polar deserts. Anticipated warming is expected to change the hydrology of these systems due to increased meltwater and reduction of ice cover, with implications for environmental conditions and physical connectivity between habitats. Using 16S rRNA gene sequencing, we evaluated microbial mat and planktonic communities within a connected freshwater system in the McMurdo Wright Valley, Antarctica, to determine the roles of connectivity and habitat conditions in controlling microbial assemblage composition. We examined communities from glacial Lake Brownworth, the perennially ice-covered Lake Vanda and the Onyx River, which connects the two. In Lake Vanda, we found distinct microbial assemblages occupying sub-habitats at different lake depths, while the communities from Lake Brownworth and Onyx River were structurally similar. Despite the higher physical connectivity and dispersal opportunities between bacterial communities in the shallow parts of the system, environmental abiotic conditions dominated over dispersal in driving community structure. Functional metabolic pathway predictions suggested differences in the functional gene potential between the microbial mat communities located in shallower and deeper water depths. The findings suggest that increasing temperatures and meltwater due to future climate change will affect bacterial diversity and functioning in Antarctic freshwater ecosystems.

Structure and distribution of chalky deposits in the Pacific oyster using x-ray computed tomography (CT).

Oysters are unusual among bivalves in that they possess chambers, often filled with soft, chalky calcite, that are irregularly scattered throughout the shell. Because the function of these so-called chalky deposits is still unclear, evaluating the growth and distribution of chalk is important for elucidating the ecological function of this unique shell trait. Specimens of the Pacific oyster Magallana gigas, an oyster well known for chalk expression, were grown in Bodega Harbor, Bodega Bay, CA. At the end of an 11 month growing period, specimens were culled and selected animals were submitted for x-ray computed-tomography imaging. Three-dimensional reconstructions of oyster shells were used to assess the overall distribution of chalk, and also to better understand the relationship between chalk and other structures within the shell. Results indicate that chalky deposits underly sculptural features on the shell exterior, such as external ridges and changes in growth direction, and also that there is a relationship between chalk formation and oyster processes of cementation. Overall, chalk is useful for a cementing lifestyle because it enables morphological plasticity needed to conform to irregular substrates, but also acts as a cheap building material to facilitate rapid growth.

A phylogenetically novel cyanobacterium most closely related to Gloeobacter.

Clues to the evolutionary steps producing innovations in oxygenic photosynthesis may be preserved in the genomes of organisms phylogenetically placed between non-photosynthetic Vampirovibrionia (formerly Melainabacteria) and the thylakoid-containing Cyanobacteria. However, only two species with published genomes are known to occupy this phylogenetic space, both within the genus Gloeobacter. Here, we describe nearly complete, metagenome-assembled genomes (MAGs) of an uncultured organism phylogenetically placed near Gloeobacter, for which we propose the name Candidatus Aurora vandensis {Au'ro.ra. L. fem. n. aurora, the goddess of the dawn in Roman mythology; van.de'nsis. N.L. fem. adj. vandensis of Lake Vanda, Antarctica}. The MAG of A. vandensis contains homologs of most genes necessary for oxygenic photosynthesis including key reaction center proteins. Many accessory subunits associated with the photosystems in other species either are missing from the MAG or are poorly conserved. The MAG also lacks homologs of genes associated with the pigments phycocyanoerethrin, phycoeretherin and several structural parts of the phycobilisome. Additional characterization of this organism is expected to inform models of the evolution of oxygenic photosynthesis.

Environmental control on the distribution of metabolic strategies of benthic microbial mats in Lake Fryxell, Antarctica.

Ecological theories posit that heterogeneity in environmental conditions greatly affects community structure and function. However, the degree to which ecological theory developed using plant- and animal-dominated systems applies to microbiomes is unclear. Investigating the metabolic strategies found in microbiomes are particularly informative for testing the universality of ecological theories because microorganisms have far wider metabolic capacity than plants and animals. We used metagenomic analyses to explore the relationships between the energy and physicochemical gradients in Lake Fryxell and the metabolic capacity of its benthic microbiome. Statistical analysis of the relative abundance of metabolic marker genes and gene family diversity shows that oxygenic photosynthesis, carbon fixation, and flavin-based electron bifurcation differentiate mats growing in different environmental conditions. The pattern of gene family diversity points to the likely importance of temporal environmental heterogeneity in addition to resource gradients. Overall, we found that the environmental heterogeneity of photosynthetically active radiation (PAR) and oxygen concentration ([O2]) in Lake Fryxell provide the framework by which metabolic diversity and composition of the community is structured, in accordance with its phylogenetic structure. The organization of the resulting microbial ecosystems are consistent with the maximum power principle and the species sorting model.

Energetic and Environmental Constraints on the Community Structure of Benthic Microbial Mats in Lake Fryxell, Antarctica.

Ecological communities are regulated by the flow of energy through environments. Energy flow is typically limited by access to photosynthetically active radiation (PAR) and oxygen concentration (O2). The microbial mats growing on the bottom of Lake Fryxell, Antarctica, have well-defined environmental gradients in PAR and (O2). We analyzed the metagenomes of layers from these microbial mats to test the extent to which access to oxygen and light controls community structure. We found variation in the diversity and relative abundances of Archaea, Bacteria and Eukaryotes across three (O2) and PAR conditions: high (O2) and maximum PAR, variable (O2) with lower maximum PAR, and low (O2) and maximum PAR. We found distinct communities structured by the optimization of energy use on a millimeter-scale across these conditions. In mat layers where (O2) was saturated, PAR structured the community. In contrast, (O2) positively correlated with diversity and affected the distribution of dominant populations across the three habitats, suggesting that meter-scale diversity is structured by energy availability. Microbial communities changed across covarying gradients of PAR and (O2). The comprehensive metagenomic analysis suggests that the benthic microbial communities in Lake Fryxell are structured by energy flow across both meter- and millimeter-scales.

First Detections of Dichlorobenzene Isomers and Trichloromethylpropane from Organic Matter Indigenous to Mars Mudstone in Gale Crater, Mars: Results from the Sample Analysis at Mars Instrument Onboard the Curiosity Rover.

Chromatographic analysis of the Cumberland mudstone in Gale crater by the Sample Analysis at Mars (SAM) instrument revealed the detection of two to three isomers of dichlorobenzene. Their individual concentrations were estimated to be in the 0.5-17 ppbw range relative to the sample mass. We also report the first detection of trichloromethylpropane and the confirmation of the detection of chlorobenzene previously reported. Supporting laboratory experiments excluded the SAM internal background as the source of those compounds, thus confirming the organic carbon and chlorine of the newly detected chlorohydrocarbons are indigenous to the mudstone sample. Laboratory experiments also demonstrated that the chlorohydrocarbons were mainly produced from chemical reactions occurring in the SAM ovens between organic molecules and oxychlorines contained in the sample. The results we obtained show that meteoritic organics and tested chemical species (a polycyclic aromatic hydrocarbon, an amino acid, and a carboxylic acid) were plausible organic precursors of the chlorinated aromatic molecules detected with SAM, thus suggesting that they could be among the organic molecules present in the mudstone. Results from this study coupled with previously reported detections of chlorinated aromatics (<300 ppbw) indigenous to the same mudstone highlight that organics can be preserved from the harsh surface conditions even at shallow depth. The detection of new chlorohydrocarbons with SAM confirms that organic molecules should have been available in an environment favorable to life forms, strengthening the habitability aspect of Gale crater.

Environmental controls on bacteriohopanepolyol profiles of benthic microbial mats from Lake Fryxell, Antarctica.

Bacteriohopanepolyols (BHPs) are pentacyclic triterpenoid lipids that contribute to the structural integrity and physiology of some bacteria. Because some BHPs originate from specific classes of bacteria, BHPs have potential as taxonomically and environmentally diagnostic biomarkers. For example, a stereoisomer of bacteriohopanetetrol (informally BHT II) has been associated with anaerobic ammonium oxidation (anammox) bacteria and suboxic to anoxic marine environments where anammox is active. As a result, the detection of BHT II in the sedimentary record and fluctuations in the relative abundance of BHT II may inform reconstructions of nitrogen cycling and ocean redox changes through the geological record. However, there are uncertainties concerning the sources of BHT II and whether or not BHT II is produced in abundance in non-marine environments, both of which are pertinent to interpretations of BHT II signatures in sediments. To address these questions, we investigate the BHP composition of benthic microbial mats from Lake Fryxell, Antarctica. Lake Fryxell is a perennially ice-covered lake with a sharp oxycline in a density-stabilized water column. We describe the diversity and abundance of BHPs in benthic microbial mats across a transect from oxic to anoxic conditions. Generally, BHP abundances and diversity vary with the morphologies of microbial mats, which were previously shown to reflect local environmental conditions, such as irradiance and oxygen and sulfide concentrations. BHT II was identified in mats that exist within oxic to anoxic portions of the lake. However, anammox bacteria have yet to be identified in Lake Fryxell. We examine our results in the context of BHPs as biomarkers in modern and ancient environments.

Bacteriohopanepolyols across environmental gradients in Lake Vanda, Antarctica.

Bacteriohopanepolyols (BHPs) are bacterial membrane lipids that may be used as biological or environmental biomarkers. Previous studies have described the diversity, distribution, and abundance of BHPs in a variety of modern environments. However, the regulation of BHP production in polar settings is not well understood. Benthic microbial mats from ice-covered lakes of the McMurdo Dry Valleys, Antarctica provide an opportunity to investigate the sources, physiological roles, and preservation of BHPs in high-latitude environments. Lake Vanda is one of the most stable lakes on Earth, with microbial communities occupying specific niches along environmental gradients. We describe the influence of mat morphology and local environmental conditions on the diversity and distribution of BHPs and their biological sources in benthic microbial mats from Lake Vanda. The abundance and diversity of C-2 methylated hopanoids (2-MeBHP) are of particular interest, given that their stable degradation products, 2-methylhopanes, are among the oldest and most prevalent taxonomically informative biomarkers preserved in sedimentary rocks. Furthermore, the interpretation of sedimentary 2-methylhopanes is of great interest to the geobiology community. We identify cyanobacteria as the sole source of 2-MeBHP in benthic microbial mats from Lake Vanda and assess the hypothesis that 2-MeBHP are regulated in response to a particular environmental variable, namely solar irradiance.

Organic matter preserved in 3-billion-year-old mudstones at Gale crater, Mars.

Establishing the presence and state of organic matter, including its possible biosignatures, in martian materials has been an elusive quest, despite limited reports of the existence of organic matter on Mars. We report the in situ detection of organic matter preserved in lacustrine mudstones at the base of the ~3.5-billion-year-old Murray formation at Pahrump Hills, Gale crater, by the Sample Analysis at Mars instrument suite onboard the Curiosity rover. Diverse pyrolysis products, including thiophenic, aromatic, and aliphatic compounds released at high temperatures (500° to 820°C), were directly detected by evolved gas analysis. Thiophenes were also observed by gas chromatography-mass spectrometry. Their presence suggests that sulfurization aided organic matter preservation. At least 50 nanomoles of organic carbon persists, probably as macromolecules containing 5% carbon as organic sulfur molecules.

The Mars Science Laboratory (MSL) Mast cameras and Descent imager: Investigation and instrument descriptions.

The Mars Science Laboratory Mast camera and Descent Imager investigations were designed, built, and operated by Malin Space Science Systems of San Diego, CA. They share common electronics and focal plane designs but have different optics. There are two Mastcams of dissimilar focal length. The Mastcam-34 has an f/8, 34 mm focal length lens, and the M-100 an f/10, 100 mm focal length lens. The M-34 field of view is about 20° × 15° with an instantaneous field of view (IFOV) of 218 µrad; the M-100 field of view (FOV) is 6.8° × 5.1° with an IFOV of 74 µrad. The M-34 can focus from 0.5 m to infinity, and the M-100 from ~1.6 m to infinity. All three cameras can acquire color images through a Bayer color filter array, and the Mastcams can also acquire images through seven science filters. Images are ≤1600 pixels wide by 1200 pixels tall. The Mastcams, mounted on the ~2 m tall Remote Sensing Mast, have a 360° azimuth and ~180° elevation field of regard. Mars Descent Imager is fixed-mounted to the bottom left front side of the rover at ~66 cm above the surface. Its fixed focus lens is in focus from ~2 m to infinity, but out of focus at 66 cm. The f/3 lens has a FOV of ~70° by 52° across and along the direction of motion, with an IFOV of 0.76 mrad. All cameras can acquire video at 4 frames/second for full frames or 720p HD at 6 fps. Images can be processed using lossy Joint Photographic Experts Group and predictive lossless compression.

Mineralogy, provenance, and diagenesis of a potassic basaltic sandstone on Mars: CheMin X-ray diffraction of the Windjana sample (Kimberley area, Gale Crater).

The Windjana drill sample, a sandstone of the Dillinger member (Kimberley formation, Gale Crater, Mars), was analyzed by CheMin X-ray diffraction (XRD) in the MSL Curiosity rover. From Rietveld refinements of its XRD pattern, Windjana contains the following: sanidine (21% weight, ~Or95); augite (20%); magnetite (12%); pigeonite; olivine; plagioclase; amorphous and smectitic material (~25%); and percent levels of others including ilmenite, fluorapatite, and bassanite. From mass balance on the Alpha Proton X-ray Spectrometer (APXS) chemical analysis, the amorphous material is Fe rich with nearly no other cations-like ferrihydrite. The Windjana sample shows little alteration and was likely cemented by its magnetite and ferrihydrite. From ChemCam Laser-Induced Breakdown Spectrometer (LIBS) chemical analyses, Windjana is representative of the Dillinger and Mount Remarkable members of the Kimberley formation. LIBS data suggest that the Kimberley sediments include at least three chemical components. The most K-rich targets have 5.6% K2O, ~1.8 times that of Windjana, implying a sediment component with >40% sanidine, e.g., a trachyte. A second component is rich in mafic minerals, with little feldspar (like a shergottite). A third component is richer in plagioclase and in Na2O, and is likely to be basaltic. The K-rich sediment component is consistent with APXS and ChemCam observations of K-rich rocks elsewhere in Gale Crater. The source of this sediment component was likely volcanic. The presence of sediment from many igneous sources, in concert with Curiosity's identifications of other igneous materials (e.g., mugearite), implies that the northern rim of Gale Crater exposes a diverse igneous complex, at least as diverse as that found in similar-age terranes on Earth.

Microbial Mat Communities along an Oxygen Gradient in a Perennially Ice-Covered Antarctic Lake.

Lake Fryxell is a perennially ice-covered lake in the McMurdo Dry Valleys, Antarctica, with a sharp oxycline in a water column that is density stabilized by a gradient in salt concentration. Dissolved oxygen falls from 20 mg liter(-1) to undetectable over one vertical meter from 8.9- to 9.9-m depth. We provide the first description of the benthic mat community that falls within this oxygen gradient on the sloping floor of the lake, using a combination of micro- and macroscopic morphological descriptions, pigment analysis, and 16S rRNA gene bacterial community analysis. Our work focused on three macroscopic mat morphologies that were associated with different parts of the oxygen gradient: (i) "cuspate pinnacles" in the upper hyperoxic zone, which displayed complex topography and were dominated by phycoerythrin-rich cyanobacteria attributable to the genus Leptolyngbya and a diverse but sparse assemblage of pennate diatoms; (ii) a less topographically complex "ridge-pit" mat located immediately above the oxic-anoxic transition containing Leptolyngbya and an increasing abundance of diatoms; and (iii) flat prostrate mats in the upper anoxic zone, dominated by a green cyanobacterium phylogenetically identified as Phormidium pseudopriestleyi and a single diatom, Diadesmis contenta. Zonation of bacteria was by lake depth and by depth into individual mats. Deeper mats had higher abundances of bacteriochlorophylls and anoxygenic phototrophs, including Chlorobi and Chloroflexi. This suggests that microbial communities form assemblages specific to niche-like locations. Mat morphologies, underpinned by cyanobacterial and diatom composition, are the result of local habitat conditions likely defined by irradiance and oxygen and sulfide concentrations.

Preserved Filamentous Microbial Biosignatures in the Brick Flat Gossan, Iron Mountain, California.

A variety of actively precipitating mineral environments preserve morphological evidence of microbial biosignatures. One such environment with preserved microbial biosignatures is the oxidized portion of a massive sulfide deposit, or gossan, such as that at Iron Mountain, California. This gossan may serve as a mineralogical analogue to some ancient martian environments due to the presence of oxidized iron and sulfate species, and minerals that only form in acidic aqueous conditions, in both environments. Evaluating the potential biogenicity of cryptic textures in such martian gossans requires an understanding of how microbial textures form biosignatures on Earth. The iron-oxide-dominated composition and morphology of terrestrial, nonbranching filamentous microbial biosignatures may be distinctive of the underlying formation and preservation processes. The Iron Mountain gossan consists primarily of ferric oxide (hematite), hydrous ferric oxide (HFO, predominantly goethite), and jarosite group minerals, categorized into in situ gossan, and remobilized iron deposits. We interpret HFO filaments, found in both gossan types, as HFO-mineralized microbial filaments based in part on (1) the presence of preserved central filament lumina in smooth HFO mineral filaments that are likely molds of microbial filaments, (2) mineral filament formation in actively precipitating iron-oxide environments, (3) high degrees of mineral filament bending consistent with a flexible microbial filament template, and (4) the presence of bare microbial filaments on gossan rocks. Individual HFO filaments are below the resolution of the Mars Curiosity and Mars 2020 rover cameras, but sinuous filaments forming macroscopic matlike textures are resolvable. If present on Mars, available cameras may resolve these features identified as similar to terrestrial HFO filaments and allow subsequent evaluation for their biogenicity by synthesizing geochemical, mineralogical, and morphological analyses. Sinuous biogenic filaments could be preserved on Mars in an iron-rich environment analogous to Iron Mountain, with the Pahrump Hills region and Hematite Ridge in Gale Crater as tentative possibilities.