The serpentinite-hosted Lost City hydrothermal field is a remarkable submarine ecosystem in which geological, chemical, and biological processes are intimately interlinked. Reactions between seawater and upper mantle peridotite produce methane- and hydrogen-rich fluids, with temperatures ranging from <40 degrees to 90 degrees C at pH 9 to 11, and carbonate chimneys 30 to 60 meters tall. A low diversity of microorganisms related to methane-cycling Archaea thrive in the warm porous interiors of the edifices. Macrofaunal communities show a degree of species diversity at least as high as that of black smoker vent sites along the Mid-Atlantic Ridge, but they lack the high biomasses of chemosynthetic organisms that are typical of volcanically driven systems.
The sulfur biogeochemical cycle integrates the metabolic activity of multiple microbial pathways (e.g., sulfate reduction, disproportionation, and sulfide oxidation) along with abiotic reactions and geological processes that cycle sulfur through various reservoirs. The sulfur cycle impacts the global carbon cycle and climate primarily through the remineralization of organic carbon. Over geological timescales, cycling of sulfur is closely tied to the redox state of Earth's exosphere through the burial of oxidized (sulfate) and reduced (sulfide) sulfur species in marine sediments. Biological sulfur cycling is associated with isotopic fractionations that can be used to trace the fluxes through various metabolic pathways. The resulting isotopic data provide insights into sulfur cycling in both modern and ancient environments via isotopic signatures in sedimentary sulfate and sulfide phases. Here, we review the deep-time δ 34 S record of marine sulfates and sulfides in light of recent advances in understanding how isotopic signatures are generated by microbial activity, how these signatures are encoded in marine sediments, and how they may be altered following deposition. The resulting picture shows a sulfur cycle intimately coupled to ambient carbon cycling, where sulfur isotopic records preserved in sedimentary rocks are critically dependent on sedimentological and geochemical conditions (e.g., iron availability) during deposition. 593 Annu. Rev. Earth Planet. Sci. 2015.43:593-622. Downloaded from www.annualreviews.org Access provided by 99.5.235.72 on 08/04/16. For personal use only.
Phanerozoic levels of atmospheric oxygen relate to the burial histories of organic carbon and pyrite sulfur. The sulfur cycle remains poorly constrained, however, leading to concomitant uncertainties in O 2 budgets. Here we present experiments linking the magnitude of fractionations of the multiple sulfur isotopes to the rate of microbial sulfate reduction. The data demonstrate that such fractionations are controlled by the availability of electron donor (organic matter), rather than by the concentration of electron acceptor (sulfate), an environmental constraint that varies among sedimentary burial environments. By coupling these results with a sediment biogeochemical model of pyrite burial, we find a strong relationship between observed sulfur isotope fractionations over the last 200 Ma and the areal extent of shallow seafloor environments. We interpret this as a global dependency of the rate of microbial sulfate reduction on the availability of organic-rich sea-floor settings. However, fractionation during the early/mid-Paleozoic fails to correlate with shelf area. We suggest that this decoupling reflects a shallower paleoredox boundary, primarily confined to the water column in the early Phanerozoic. The transition between these two states begins during the Carboniferous and concludes approximately around the Triassic-Jurassic boundary, indicating a prolonged response to a Carboniferous rise in O 2 . Together, these results lay the foundation for decoupling changes in sulfate reduction rates from the global average record of pyrite burial, highlighting how the local nature of sedimentary processes affects global records. This distinction greatly refines our understanding of the S cycle and its relationship to the history of atmospheric oxygen.Phanerozoic oxygen | sulfate-reducing bacteria T he marine sedimentary sulfur isotope record encodes information on the chemical and biological composition of Earth's ancient oceans and atmosphere (1, 2). However, our interpretation of the isotopic composition of S-bearing minerals is only as robust as our understanding of the mechanisms that impart a fractionation. Fortunately, decades of research identify microbial sulfate reduction (MSR) as the key catalyst of the marine S cycle, both setting the S cycle in motion and dominating the massdependent fractionation preserved within the geological record (1, 3, 4). Despite the large range of S-isotope variability observed in biological studies (4-6), attempts to calibrate the fractionations associated with MSR are less mechanistically definitive (7, 8) than analogous processes influencing the carbon cycle (9, 10). What is required is a means to predict S isotope signatures as a function of the physiological response to environmental conditions (e.g., reduction-oxidation potential).Microbial sulfate reduction couples the oxidation of organic matter or molecular hydrogen to the production of sulfide, setting in motion a cascade of reactions that come to define the biogeochemical S cycle. In modern marine sediments, sulfide i...
There is a close connection between modern-day biosynthesis of particular triterpenoid biomarkers and presence of molecular oxygen in the environment. Thus, the detection of steroid and triterpenoid hydrocarbons far back in Earth history has been used to infer the antiquity of oxygenic photosynthesis. This prompts the question: were these compounds produced similarly in the past? In this paper, we address this question with a review of the current state of knowledge surrounding the oxygen requirement for steroid biosynthesis and phylogenetic patterns in the distribution of steroid and triterpenoid biosynthetic pathways.The hopanoid and steroid biosynthetic pathways are very highly conserved within the bacterial and eukaryotic domains, respectively. Bacteriohopanepolyols are produced by a wide range of bacteria, and are methylated in significant abundance at the C2 position by oxygen-producing cyanobacteria. On the other hand, sterol biosynthesis is sparsely distributed in distantly related bacterial taxa and the pathways do not produce the wide range of products that characterize eukaryotes. In particular, evidence for sterol biosynthesis by cyanobacteria appears flawed. Our experiments show that cyanobacterial cultures are easily contaminated by sterol-producing rust fungi, which can be eliminated by treatment with cycloheximide affording sterol-free samples.Sterols are ubiquitous features of eukaryotic membranes, and it appears likely that the initial steps in sterol biosynthesis were present in their modern form in the last common ancestor of eukaryotes. Eleven molecules of O 2 are required by four enzymes to produce one molecule of cholesterol. Thermodynamic arguments, optimization of function and parsimony all indicate that an ancestral anaerobic pathway is highly unlikely.The known geological record of molecular fossils, especially steranes and triterpanes, is notable for the limited number of structural motifs that have been observed. With a few exceptions, the carbon skeletons are the same as those found in the lipids of extant organisms and no demonstrably extinct structures have been reported. Furthermore, their patterns of occurrence over billion year time-scales correlate strongly with environments of deposition. Accordingly, biomarkers are excellent indicators of environmental conditions even though the taxonomic affinities of all biomarkers cannot be precisely specified. Biomarkers are ultimately tied to biochemicals with very specific functional properties, and interpretations of the biomarker record will benefit from increased understanding of the biological roles of geologically durable molecules.
Proteorhodopsins (PRs) are retinal-containing proteins that catalyze light-activated proton efflux across the cell membrane. These photoproteins are known to be globally distributed in the ocean's photic zone, and they are found in a diverse array of Bacteria and Archaea. Recently, light-enhanced growth rates and yields have been reported in at least one PR-containing marine bacterium, but the physiological basis of light-activated growth stimulation has not yet been determined. To describe more fully PR photosystem genetics and biochemistry, we functionally surveyed a marine picoplankton large-insert genomic library for recombinant clones expressing PR photosystems in vivo. Our screening approach exploited transient increases in vector copy number that significantly enhanced the sensitivity of phenotypic detection. Two genetically distinct recombinants, initially identified by their orange pigmentation, expressed a small cluster of genes encoding a complete PR-based photosystem. Genetic and biochemical analyses of transposon mutants verified the function of gene products in the photopigment and opsin biosynthetic pathways. Heterologous expression of six genes, five encoding photopigment biosynthetic proteins and one encoding a PR, generated a fully functional PR photosystem that enabled photophosphorylation in recombinant Escherichia coli cells exposed to light. Our results demonstrate that a single genetic event can result in the acquisition of phototrophic capabilities in an otherwise chemoorganotrophic microorganism, and they explain in part the ubiquity of PR photosystems among diverse microbial taxa.photoheterotrophy ͉ rhodopsin ͉ lateral gene transfer ͉ marine ͉ metagenomics
The functionality of cellular membranes relies on the molecular order imparted by lipids. In eukaryotes, sterols such as cholesterol modulate membrane order, yet they are not typically found in prokaryotes. The structurally similar bacterial hopanoids exhibit similar ordering properties as sterols in vitro, but their exact physiological role in living bacteria is relatively uncharted. We present evidence that hopanoids interact with glycolipids in bacterial outer membranes to form a highly ordered bilayer in a manner analogous to the interaction of sterols with sphingolipids in eukaryotic plasma membranes. Furthermore, multidrug transport is impaired in a hopanoid-deficient mutant of the gram-negative Methylobacterium extorquens, which introduces a link between membrane order and an energy-dependent, membrane-associated function in prokaryotes. Thus, we reveal a convergence in the architecture of bacterial and eukaryotic membranes and implicate the biosynthetic pathways of hopanoids and other order-modulating lipids as potential targets to fight pathogenic multidrug resistance.
These data reveal complexity in the sulfate concentration-fractionation relationship. 42Sulfur isotope fractionation during sulfate reduction relates to environmental sulfate 43 concentrations but also to strain-specific physiological parameters such as the affinity of sulfate-44 reducing microorganisms for sulfate and electron donors. Previous studies have suggested that 45 the relationship between sulfate concentration and isotope fractionation is best fit with a MM fit. 46suggested We present a simple model, grounded in the physiology of sulfate reduction, in which 47 the ratio of MM relationships for sulfate and electron donor uptake produces the relationships 48 seen in experimental studies: a MM relationship with sulfate concentration, and a hyperbolic 49 relationship with growth rate. 50Since both environmental and biological factors influence the fractionation recorded in 51 geological samples, understanding their relationship is critical to interpreting the sulfur isotope 52 record. As the acquisition machinery for sulfate and electron acquisition has been subject to 53 selective pressure over Earth history, its evolution may complicate efforts to uniquely reconstruct 54 ambient sulfate concentrations from a single sulfur isotopic composition. 55Patterns of SRB S-isotope fractionation 2 56
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