Investigations of the biogeochemical roles of benthic Archaea in marine sediments are hampered by the scarcity of cultured representatives. In order to determine their metabolic capacity, we ...reconstructed the genomic content of four widespread uncultured benthic Archaea recovered from estuary sediments at 48% to 95% completeness. Four genomic bins were found to belong to different subgroups of the former Miscellaneous Crenarcheota Group (MCG) now called Bathyarchaeota: MCG‐6, MCG‐1, MCG‐7/17 and MCG‐15. Metabolic predictions based on gene content of the different genome bins indicate that subgroup 6 has the ability to hydrolyse extracellular plant‐derived carbohydrates, and that all four subgroups can degrade detrital proteins. Genes encoding enzymes involved in acetate production as well as in the reductive acetyl–CoA pathway were detected in all four genomes inferring that these Archaea are organo‐heterotrophic and autotrophic acetogens. Genes involved in nitrite reduction were detected in all Bathyarchaeota subgroups and indicate a potential for dissimilatory nitrite reduction to ammonium. Comparing the genome content of the different Bathyarchaeota subgroups indicated preferences for distinct types of carbohydrate substrates and implicitly, for different niches within the sedimentary environment.
Microbial life in marine sediment contributes substantially to global biomass and is a crucial component of the Earth system. Subseafloor sediment includes both aerobic and anaerobic microbial ...ecosystems, which persist on very low fluxes of bioavailable energy over geologic time. However, the taxonomic diversity of the marine sedimentary microbial biome and the spatial distribution of that diversity have been poorly constrained on a global scale. We investigated 299 globally distributed sediment core samples from 40 different sites at depths of 0.1 to 678 m below the seafloor. We obtained ~47 million 16S ribosomal RNA (rRNA) gene sequences using consistent clean subsampling and experimental procedures, which enabled accurate and unbiased comparison of all samples. Statistical analysis reveals significant correlations between taxonomic composition, sedimentary organic carbon concentration, and presence or absence of dissolved oxygen. Extrapolation with two fitted species–area relationship models indicates taxonomic richness in marine sediment to be 7.85 × 10³ to 6.10 × 10⁵ and 3.28 × 10⁴ to 2.46 × 10⁶ amplicon sequence variants for Archaea and Bacteria, respectively. This richness is comparable to the richness in topsoil and the richness in seawater, indicating that Bacteria are more diverse than Archaea in Earth’s global biosphere.
Members of the archaeal phylum Bathyarchaeota are among the most abundant microorganisms on Earth. Although versatile metabolic capabilities such as acetogenesis, methanogenesis, and fermentation ...have been suggested for bathyarchaeotal members, no direct confirmation of these metabolic functions has been achieved through growth of Bathyarchaeota in the laboratory. Here we demonstrate, on the basis of gene-copy numbers and probing of archaeal lipids, the growth of Bathyarchaeota subgroup Bathy-8 in enrichments of estuarine sediments with the biopolymer lignin. Other organic substrates (casein, oleic acid, cellulose, and phenol) did not significantly stimulate growth of Bathyarchaeota. Meanwhile, putative bathyarchaeotal tetraether lipids incorporated 13C from 13C-bicarbonate only when added in concert with lignin. Our results are consistent with organoautotrophic growth of a bathyarchaeotal group with lignin as an energy source and bicarbonate as a carbon source and shed light into the cycling of one of Earth’s most abundant biopolymers in anoxic marine sediment.
Marine microalgae sequester as much CO₂ into carbohydrates as terrestrial plants. Polymeric carbohydrates (i.e., glycans) provide carbon for heterotrophic organisms and constitute a carbon sink in ...the global oceans. The quantitative contributions of different algal glycans to cycling and sequestration of carbon remain unknown, partly because of the analytical challenge to quantify glycans in complex biological matrices. Here, we quantified a glycan structural type using a recently developed biocatalytic strategy, which involves laminarinase enzymes that specifically cleave the algal glycan laminarin into readily analyzable fragments. We measured laminarin along transects in the Arctic, Atlantic, and Pacific oceans and during three time series in the North Sea. These data revealed a median of 26 ± 17% laminarin within the particulate organic carbon pool. The observed correlation between chlorophyll and laminarin suggests an annual production of algal laminarin of 12 ± 8 gigatons: that is, approximately three times the annual atmospheric carbon dioxide increase by fossil fuel burning. Moreover, our data revealed that laminarin accounted for up to 50% of organic carbon in sinking diatom-containing particles, thus substantially contributing to carbon export from surface waters. Spatially and temporally variable laminarin concentrations in the sunlit ocean are driven by light availability. Collectively, these observations highlight the prominent ecological role and biogeochemical function of laminarin in oceanic carbon export and energy flow to higher trophic levels.
Deep drilling into the marine sea floor has uncovered a vast sedimentary ecosystem of microbial cells. Extrapolation of direct counts of stained microbial cells to the total volume of habitable ...marine subsurface sediments suggests that between 56 Pg (ref. 1) and 303 Pg (ref. 3) of cellular carbon could be stored in this largely unexplored habitat. From recent studies using various culture-independent techniques, no clear picture has yet emerged as to whether Archaea or Bacteria are more abundant in this extensive ecosystem. Here we show that in subsurface sediments buried deeper than 1 m in a wide range of oceanographic settings at least 87% of intact polar membrane lipids, biomarkers for the presence of live cells, are attributable to archaeal membranes, suggesting that Archaea constitute a major fraction of the biomass. Results obtained from modified quantitative polymerase chain reaction and slot-blot hybridization protocols support the lipid-based evidence and indicate that these techniques have previously underestimated archaeal biomass. The lipid concentrations are proportional to those of total organic carbon. On the basis of this relationship, we derived an independent estimate of amounts of cellular carbon in the global marine subsurface biosphere. Our estimate of 90 Pg of cellular carbon is consistent, within an order of magnitude, with previous estimates, and underscores the importance of marine subsurface habitats for global biomass budgets.
Sedimentary dissolved organic matter (DOM) is an important pool of intermediates produced and consumed during early diagenesis of organic matter in the anoxic subseafloor. Rapid degradation of ...organic matter in the coastal sediment results in stratification of redox zones. However, to date little is known about the selectivity with respect to organic matter of the initial microbially mediated anaerobic degradation processes under contrasting redox conditions and how these affect the composition of DOM. In order to study the effect of sulfate reducing vs. methanogenic conditions on DOM quality and degradation, sediments (0–18 cm) from the Rhône River Delta were incubated, with redox conditions being controlled by sulfate amendment. The progress of incubation was monitored by H2, CH4, sulfate, DIC, DOC and acetate production. DOM composition was determined by 3D Fluorescence Spectroscopy, i.e., Excitation Emission Matrix Spectroscopy (EEMs), and ultra-high-resolution Fourier Transform Ion Cyclotron Resonance Mass Spectrometry (FT-ICR-MS). Parallel factor analysis (PARAFAC) of EEMs was used to distinguish different groups of DOM (humic-like and protein-like compounds) to evaluate composition, conjugation and size of DOM. Prior to incubation, humic-like sedimentary DOM predominated; nearly half of the molecular formulae (>5000) identified by FT-ICR-MS were CHO and one third were CHNO compounds. During incubation, protein-like DOM and CHNO formulae with 3 and 4 N atoms formulae were rare under both sulfate reducing and methanogenic conditions. Incubation under sulfate reducing conditions resulted in rapid release and net accumulation of dissolved organic carbon (DOC). Protein-like DOM was rapidly cycled and humic-like DOM accumulated. Consistently, CHNO formulae with 3 and 4 N atoms decreased faster, whereas formulae with one N and oxygen-rich unsaturated compounds became more concentrated. In contrast, during incubation under methanogenic conditions, there was no net accumulation of DOC; blue-shift of humic-like peaks suggest the transformation possibly associated with loss of oxygen-bearing functional groups in conjugated structures of humic substances. This interpretation is consistent with the relative decrease of oxygenation and carbon number in the pool of aromatic and highly unsaturated compounds observed by FT-ICR-MS analysis. Approximately 90% of molecular formulae that were lost under methanogenic conditions were accumulated under sulfate reducing conditions. Our results suggest that under sulfate reducing conditions degradation of organic matter results in the accumulation of highly oxidized DOM, while protein-like compounds are selectively consumed. When the redox regime changes to methanogenic conditions, microbes apparently utilize the humic-like and oxygen-rich compounds of the oxidized DOM pool that accumulated under sulfate reducing conditions. Consequently, redox regimes and the associated biogeochemical processes influence rate and fractions of DOM released by and consumed in the deep biosphere, which could ultimately shape the composition of the preserved sedimentary organic matter and the DOM released to the ocean.
Marine ammonia-oxidizing archaea of the phylum Thaumarchaeota are a cosmopolitan group of microorganisms representing a major fraction of the picoplankton in the ocean. The cytoplasmic membranes of ...Thaumarchaeota consist predominantly of intact polar isoprenoid glycerol dibiphytanyl glycerol tetraether (GDGT) lipids, which may be used as biomarkers for living Thaumarchaeota. Fossil thaumarchaeal GDGT core lipids accumulate in marine sediments and serve as the basis for geochemical proxies such as the TEX86 paleothermometer. Here, we demonstrate that the responses of membrane lipid compositions and resulting TEX86 values to growth temperature strongly diverge in three closely related thaumarchaeal pure cultures, i.e., Nitrosopumilus maritimus and two novel strains isolated from South Atlantic surface water, although the inventories of intact polar lipids and core lipids were overall similar in the three strains. N. maritimus and its closely related strain NAOA6 showed linear relationships of TEX86 and growth temperature but no correlation of TEX86 and temperature was observed in the more distantly related strain NAOA2. In contrast, the weighted average number of cycloalkyl moieties (ring index) was linearly correlated with growth temperature in all strains. This disparate relationship of TEX86 to growth temperature among closely related Thaumarchaeota suggests that the ring index but not the TEX86 ratio represents a universal response to growth temperature in marine planktonic Thaumarchaeota. Furthermore, the distinct TEX86-temperature relationships in the cultivated strains indicate that environmental GDGT signals may include an ecological component, which has important implications for ocean temperature reconstructions using the TEX86 proxy. In contrast, different growth medium salinities in the range 27–51‰ tested for N. maritimus showed no systematic effect on intact polar GDGT composition and TEX86. Similarly, N. maritimus showed only small changes in intact polar GDGT composition and TEX86 when grown at different medium pH in the range 7.3–7.9. Overall, our pure culture studies suggest that the TEX86 paleotemperature proxy is not solely dependent on growth temperature, but may amalgamate physiological, environmental, and ecological factors.
Elevated dissolved iron concentrations in the methanic zone are typical geochemical signatures of rapidly accumulating marine sediments. These sediments are often characterized by co-burial of iron ...oxides with recalcitrant aromatic organic matter of terrigenous origin. Thus far, iron oxides are predicted to either impede organic matter degradation, aiding its preservation, or identified to enhance organic carbon oxidation via direct electron transfer. Here, we investigated the effect of various iron oxide phases with differing crystallinity (magnetite, hematite, and lepidocrocite) during microbial degradation of the aromatic model compound benzoate in methanic sediments. In slurry incubations with magnetite or hematite, concurrent iron reduction, and methanogenesis were stimulated during accelerated benzoate degradation with methanogenesis as the dominant electron sink. In contrast, with lepidocrocite, benzoate degradation, and methanogenesis were inhibited. These observations were reproducible in sediment-free enrichments, even after five successive transfers. Genes involved in the complete degradation of benzoate were identified in multiple metagenome assembled genomes. Four previously unknown benzoate degraders of the genera Thermincola (Peptococcaceae, Firmicutes), Dethiobacter (Syntrophomonadaceae, Firmicutes), Deltaproteobacteria bacteria SG8_13 (Desulfosarcinaceae, Deltaproteobacteria), and Melioribacter (Melioribacteraceae, Chlorobi) were identified from the marine sediment-derived enrichments. Scanning electron microscopy (SEM) and catalyzed reporter deposition fluorescence in situ hybridization (CARD-FISH) images showed the ability of microorganisms to colonize and concurrently reduce magnetite likely stimulated by the observed methanogenic benzoate degradation. These findings explain the possible contribution of organoclastic reduction of iron oxides to the elevated dissolved Fe
pool typically observed in methanic zones of rapidly accumulating coastal and continental margin sediments.
Volatile fatty acids (VFAs) and alcohols are key intermediates of anaerobic carbon metabolism, yet their biogeochemical cycling remains poorly constrained in hydrothermal systems. We investigated the ...abundance, stable carbon isotopic composition, and metabolic cycling of VFAs and alcohols to elucidate their generation and utilization pathways in hydrothermally influenced sediments (4 °C to 90 °C) from the Guaymas Basin. Acetate (up to 229 μM) and methanol (up to 37 μM) were abundant in porewaters. The δ13C values of acetate varied between −35.6‰ and −18.1‰. Carbon isotopic signatures, thermodynamic predictions, and experimental incubations suggested biological sources such as fermentation and acetogenesis for acetate. Acetate and methanol were predominantly consumed by nonmethanogenic processes (e.g., sulfate reduction), as reflected in high oxidation rates versus low methanogenesis rates, and further evidenced through inhibition experiments with molybdate. These results reveal an important role for VFAs and alcohols as energy sources for diverse chemoheterotrophs in organic‐rich hydrothermally influenced sediments.
Plain Language Summary
Hydrothermal systems are unique seafloor habitats that host abundant and diverse microbial communities, but questions remain regarding their energy strategy and metabolic activity. We found that low molecular weight organic compounds such as acetate and methanol were abundant in the hydrothermal sediments of Guaymas Basin. Multiple lines of evidence suggested that these substrates were produced largely via biological pathways. We further investigated the microbial metabolism of acetate and methanol and found that both compounds could be used as an energy source to support various microbial processes in the hydrothermal systems.
Key Points
Volatile fatty acids (VFAs) and alcohols were abundant in the hydrothermal sediment of the Guaymas Basin
Isotopic signatures, thermodynamics, and sediment incubations suggest that the source of VFAs is biological fermentation and acetogenesis
High oxidation rates of acetate and methanol document utilization predominantly by nonmethanogenic chemoheterotrophs as an energy source
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