The biogeochemistry of microbial mats, stromatolites and the ancient biosphere

Stromatolites offer an unparalleled geologic record of early life, because they constitute the oldest and most abundant recognizable remains of microbial ecosystems. Microbial mats are living homologs of stromatolites; thus, the physiology of the microbiota as well as the processes which create those features of mats (e.g., biomarker organic compounds, elemental and stable isotopic compositions) which are preserved in the ancient record. Observations of the carbon isotopic composition (delta C-13) of stromatolites and microbial mats were made and are consistent with the hypothesis that atmospheric CO2 concentrations have declined by at least one to two orders of magnitude during the past 2.5 Ga. Whereas delta C-13 values of carbonate carbon average about 0 permil during both the early and mid-Proterozoic, the delta C-13 values of stromatolitic organic matter increase from an average of -35 between 2.0 and 2.6 Ga ago to an average of about -28 about 1.0 Ga ago. Modern microbial mats in hypersaline environments have delta C-13 values typically in the range of -5 to -9, relative to an inorganic bicarbonate source at 0 permil. Both microbial mats and pur cultures of cyanobacteria grown in waters in near equilibrium with current atmospheric CO2 levels exhibit minimal discrimination against C-13. In contrast, hot spring cyanobacterial mats or cyanobacterial cultures grown under higher CO2 levels exhibit substantially greater discrimination. If care is taken to compare modern mats with stromatolites from comparable environments, it might be possible to estimate ancient levels of atmospheric CO2. In modern microbial mats, a tight coupling exists between photosynthetic organic carbon production and subsequent carbon oxidation, mostly by sulfate reduction. The rate of one process fuels a high rate of the other, with much of the sulfate reduction occurring within the same depth interval as oxygenic photosynthesis. Other aspects of this study are presented

Microbial mats of the Tswaing impact crater: results of a South African exobiology expedition and implications for the search for biological molecules on Mars

We describe microbial mats from the Tswaing impact crater in South Africa. The mats provide insights into the unique biological characteristics of impact craters and can help strategies for the search for biomolecules on Mars

Structure and function of natural sulphide-oxidizing microbial mats under dynamic input of light and chemical energy

We studied the interaction between phototrophic and chemolithoautotrophic sulphide-oxidizing microorganisms in natural microbial mats forming in sulphidic streams. The structure of these mats varied between two end-members: one characterized by a layer dominated by large sulphur-oxidizing bacteria (SOB; mostly Beggiatoa-like) on top of a cyanobacterial layer (B/C mats) and the other with an inverted structure (C/B mats). C/B mats formed where the availability of oxygen from the water column was limited (<5 mu M). Aerobic chemolithotrophic activity of the SOB depended entirely on oxygen produced locally by cyanobacteria during high light conditions. In contrast, B/C mats formed at locations where oxygen in the water column was comparatively abundant (445 mu M) and continuously present. Here SOB were independent of the photosynthetic activity of cyanobacteria and outcompeted the cyanobacteria in the uppermost layer of the mat where energy sources for both functional groups were concentrated. Outcompetition of photosynthetic microbes in the presence of light was facilitated by the decoupling of aerobic chemolithotrophy and oxygenic phototrophy. Remarkably, the B/C mats conserved much less energy than the C/B mats, although similar amounts of light and chemical energy were available. Thus ecosystems do not necessarily develop towards optimal energy usage. Our data suggest that, when two independent sources of energy are available, the structure and activity of microbial communities is primarily determined by the continuous rather than the intermittent energy source, even if the time-integrated energy flux of the intermittent energy source is greater

Microbial mats and the search for minimal ecosystems

This article reviews some ecological concepts common to all kinds of ecosystems, describes the characteristics of microbial mats, and focuses on the description of the Ebro Delta microbial mats, to assess whether they fit the concept of a minimal ecosystem. First, microorganisms as components of ecosystems are considered, and some features of microbial life, including ubiquity, size and metabolism, genetic versatility, and strategies to overcome unfavorable conditions, are discussed. Models for ecosystems, regardless of their size, have the same basic components; tropical forests, multilayered planktonic microbial communities, and benthic microbial mats are analogous ecosystems at different scales. The structure –in terms of populations and communities– and ecophysiology of microbial mats are also discussed. The linear distribution of microbial populations along steep gradients of light and hydrogen sulfide allows for the simultaneous presence of different microbial populations. Defining the minimal ecosystem requirements necessary for the survival and proliferation of organisms is crucial in the search for extraterrestrial life and for establishing ecosystems beyond the Earth

Searching for Evidence of Life in Deep Time and Space

Cyanobacterial mats provide insights into ancient benthic microbial communities and their biosignatures. Thick mats occupy hypersaline saltern ponds at Guerrero Negro, Baja California, Mexico. Mat biota maintains rapid rates of biogeochemical processes under steep and rapidly changing environmental gradients. Cycling of C, O, and S all increased identically with temperature, indicating the tight coupling of these cycles. An enormous microbial diversity exhibits a highly structured spatial distribution of populations. Combined universal clone libraries from all mat layers indicated Bacteria/Archaea/Eukarya ratios of 57:7:1. More than 10,000 unique bacterial sequences were present. The relative abundance of Archaea increased with depth - below 10 cm, solvent-extractable archaeal lipids were twice as abundant as bacterial lipids. Only 15 species of Eukarya were found among 890 clones analyzed. Degradation of the mats insoluble macromolecular organic fraction (IMOM) by hydropyrolysis released a complex variety of linear, branched and polycyclic alkane structures, e.g., hopanes, methylhopanes and steranes. Covalent binding of these biosignatures into IMOM aids their long-term geological preservation. Mars rover missions revealed evidence of long-lived fluvial lacustrine systems and organics in associated mudstones. NASAs Mars 2020 rover mission will examine sediments in Jezero crater, including a delta and shoreline carbonate deposits, environments that on Earth have sustained microbial mats

Microscale spatial distributions of microbes in marine intertidal sediments and photosynthetic microbial mats

Marine sedimentary habitats generally have their highest microbial activity in the top few centimeters. Where light reaches the surface sediments, benthic oxygenic photoautotrophs composed of cyanobacteria and eukaryotic microalgae (such as diatoms) dominate. In situations with a low grazing pressure like intertidal flats, this leads to permanently vertically laminated microbial communities (photosynthetic microbial mats). Although the importance of collecting samples at the scale relevant for microbial activity in sedimentary habitats has been acknowledged, this aspect is still virtually unstudied. The main focus in this thesis concerns, therefore, microscale (μm to mm) spatial distributions of key players in photosynthetic microbial mats, i.e. viruses, prokaryotes and oxygenic photoautotrophs. Initially, two methods were developed; to extract and count viruses from microbial mats, and to discriminate in a non-intrusive manner the different photoautotrophic groups. Application showed strong vertical and horizontal microscale heterogeneity in the distributions of these microbes, both in intertidal sediment (Scotland) and photosynthetic microbial mats (Netherlands). Moreover, I studied the effect mortality agents, such as viruses and fungi, may have on microscale spatial and temporal distributions of key members of the microbial mats and sediment. High viral abundances in the microbial mats indicated that viruses could be a significant structuring factor. Fungi clearly affected the spatial distribution of oxygenic photoautotrophs by degrading benthic cyanobacteria and diatoms in ring-like shapes during summer and autumn. Based on these findings I recommend more research on microscale distributions and underlying mortality processes to improve our understanding of species diversity, succession and biogeochemical cycling in microbial mats

Taphonomy of Biosignatures in Microbial Mats on Little Ambergris Cay, Turks and Caicos Islands

Microbial mats are taxonomically and metabolically diverse microbial ecosystems, with a characteristic layering that reflects vertical gradients in light and oxygen availability. Silicified microbial mats in Proterozoic carbonate successions are generally interpreted in terms of the surficial, mat building community. However, information about biodiversity in the once-surface-layer can be lost through decay as the mats accrete. To better understand how information about surface microbial communities is impacted by processes of decay within the mat, we studied microbial mats from Little Ambergris Cay, Turks and Caicos Islands. We used molecular techniques, microscopy and geochemistry to investigate microbial mat taphonomy – how processes of degradation affect biological signatures in sedimentary rocks, including fossils, molecular fossils and isotopic records. The top < 1 cm of these mats host cyanobacteria-rich communities overlying and admixed with diverse bacterial and eukaryotic taxa. Lower layers contain abundant, often empty, sheaths of large filamentous cyanobacteria, preserving their record as key mat-builders. Morphological remains and free lipid biomarkers of several bacterial groups, as well as diatoms, arthropods, and other eukaryotes also persist in lower mat layers, although at lower abundances than in surface layers. Carbon isotope signatures of organic matter were consistent with the majority of the biomass being sourced from CO2-limited cyanobacteria. Porewater sulfide sulfur isotope values were lower than seawater sulfate sulfur isotope values by ∼45–50‰, consistent with microbial sulfate reduction under sulfate-replete conditions. Our findings provide insight into how processes of degradation and decay bias biosignatures in the geological record of microbial mats, especially mats that formed widely during the Proterozoic (2,500–541 million years ago) Eon. Cyanobacteria were the key mat-builders, their robust and cohesive fabric retained at depth. Additionally, eukaryotic remains and eukaryotic biosignatures were preserved at depth, which suggests that microbial mats are not inherently biased against eukaryote preservation, either today or in the past

Fine‐scale measurement of diffusivity in a microbial mat with nuclear magnetic resonance imaging

Noninvasive 1H‐nuclear magnetic resonance (NMR) imaging was used to investigate the diffusive properties of microbial mats in two dimensions. Pulsed field gradient NMR was used to acquire images of the H2O diffusion coefficient, Ds, and multiecho imaging NMR was used to obtain images of the water density in two structurally different microbial mats sampled from Solar Lake (Egypt). We found a pronounced lateral and vertical variability of both water density and water diffusion coefficient, correlated with the laminated and heterogeneous distribution of microbial cells and exopolymers within the mats. The average water density varied from 0.5 to 0.9, whereas the average water diffusion coefficient ranged from 0.4 to 0.9 relative to the values obtained in the stagnant water above the mat samples. The apparent water diffusivities estimated from NMR imaging compared well to apparent O2 diffusivities measured with a diffusivity microsensor. Analysis of measured O2 concentration profiles with a diffusion‐reaction model showed that both the magnitude of calculated rates and the depth distribution of calculated O2 consumption/production zones changed when the observed variations of diffusivity were taken into account. With NMR imaging, diffusivity can be determined at high spatial resolution, which can resolve inherent lateral and vertical heterogeneities found in most natural benthic systems

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