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.
ABSTRACT
Chloroflexi are widespread in subsurface environments, and recent studies indicate that they represent a major fraction of the communities in subseafloor sediment. Here, we compare the ...abundance, diversity, metabolic potential and gene expression of Chloroflexi from three abyssal sediment cores from the western North Atlantic Gyre (water depth >5400 m) covering up to 15 million years of sediment deposition, where Chloroflexi were found to represent major components of the community at all sites. Chloroflexi communities die off in oxic red clay over 10–15 million years, and gene expression was below detection. In contrast, Chloroflexi abundance and gene expression at the anoxic abyssal clay site increase below the seafloor and peak in 2–3 million-year-old sediment, indicating a comparably higher activity. Metatranscriptomes from the anoxic site reveal increased expression of Chloroflexi genes involved in cell wall biogenesis, protein turnover, inorganic ion transport, defense mechanisms and prophages. Phylogenetic analysis shows that these Chloroflexi are closely related to homoacetogenic subseafloor clades and actively transcribe genes involved in sugar fermentations, gluconeogenesis and Wood–Ljungdahl pathway in the subseafloor. Concomitant expression of cell division genes indicates that these putative homoacetogenic Chloroflexi are actively growing in these million-year-old anoxic abyssal sediments.
Anaerobic Chloroflexi are transcriptionally active, grow and divide in anoxic abyssal clay that are millions of years old, whereas aerobic Chloroflexi die off in oxic abyssal red clay.
One of the greatest mass extinctions in Earth's history occurred at the end of the Cretaceous era, sixty-five million years (Myr) ago. Considerable evidence indicates that the impact of a large ...asteroid or comet was the ultimate cause of this extraordinary event. At the time of mass extinction, the organic flux to the deep sea collapsed, and production of calcium carbonate by marine plankton radically declined. These biogeochemical processes did not fully recover for a few million years. The drastic decline and long lag in final recovery of these processes are most simply explained as consequences of open-ocean ecosystem alteration by the mass extinction. If this explanation is correct, the extent and timing of marine biogeochemical recovery from the end-Cretaceous event was ultimately contingent on the extent and timing of open-ocean ecosystem recovery. The biogeochemical recovery may in turn have created new evolutionary opportunities for a diverse array of marine organisms.
Oceanic subtropical gyres are considered biological deserts because of the extremely low availability of nutrients and thus minimum productivities. The major source of nutrient nitrogen in these ...ecosystems is N(2)-fixation. The South Pacific Gyre (SPG) is the largest ocean gyre in the world, but measurements of N(2)-fixation therein, or identification of microorganisms involved, are scarce. In the 2006/2007 austral summer, we investigated nitrogen and carbon assimilation at 11 stations throughout the SPG. In the ultra-oligotrophic waters of the SPG, the chlorophyll maxima reached as deep as 200 m. Surface primary production seemed limited by nitrogen, as dissolved inorganic carbon uptake was stimulated upon additions of (15)N-labeled ammonium and leucine in our incubation experiments. N(2)-fixation was detectable throughout the upper 200 m at most stations, with rates ranging from 0.001 to 0.19 nM N h(-1). N(2)-fixation in the SPG may account for the production of 8-20% of global oceanic new nitrogen. Interestingly, comparable (15)N(2)-fixation rates were measured under light and dark conditions. Meanwhile, phylogenetic analyses for the functional gene biomarker nifH and its transcripts could not detect any common photoautotrophic diazotrophs, such as, Trichodesmium, but a prevalence of γ-proteobacteria and the unicellular photoheterotrophic Group A cyanobacteria. The dominance of these likely heterotrophic diazotrophs was further verified by quantitative PCR. Hence, our combined results show that the ultra-oligotrophic SPG harbors a hitherto unknown heterotrophic diazotrophic community, clearly distinct from other oceanic gyres previously visited.
Water radiolysis continuously produces H
and oxidized chemicals in wet sediment and rock. Radiolytic H
has been identified as the primary electron donor (food) for microorganisms in continental ...aquifers kilometers below Earth's surface. Radiolytic products may also be significant for sustaining life in subseafloor sediment and subsurface environments of other planets. However, the extent to which most subsurface ecosystems rely on radiolytic products has been poorly constrained, due to incomplete understanding of radiolytic chemical yields in natural environments. Here we show that all common marine sediment types catalyse radiolytic H
production, amplifying yields by up to 27X relative to pure water. In electron equivalents, the global rate of radiolytic H
production in marine sediment appears to be 1-2% of the global organic flux to the seafloor. However, most organic matter is consumed at or near the seafloor, whereas radiolytic H
is produced at all sediment depths. Comparison of radiolytic H
consumption rates to organic oxidation rates suggests that water radiolysis is the principal source of biologically accessible energy for microbial communities in marine sediment older than a few million years. Where water permeates similarly catalytic material on other worlds, life may also be sustained by water radiolysis.
The deep subseafloor biosphere is among the least-understood habitats on Earth, even though the huge microbial biomass therein plays an important role for potential long-term controls on global ...biogeochemical cycles. We report here the vertical and geographical distribution of microbes and their phylogenetic diversities in deeply buried marine sediments of the Pacific Ocean Margins. During the Ocean Drilling Program Legs 201 and 204, we obtained sediment cores from the Peru and Cascadia Margins that varied with respect to the presence of dissolved methane and methane hydrate. To examine differences in prokaryotic distribution patterns in sediments with or without methane hydrates, we studied >2,800 clones possessing partial sequences (400-500 bp) of the 16S rRNA gene and 348 representative clone sequences (≈1 kbp) from the two geographically separated subseafloor environments. Archaea of the uncultivated Deep-Sea Archaeal Group were consistently the dominant phylotype in sediments associated with methane hydrate. Sediment cores lacking methane hydrates displayed few or no Deep-Sea Archaeal Group phylotypes. Bacterial communities in the methane hydrate-bearing sediments were dominated by members of the JS1 group, Planctomycetes, and Chloroflexi. Results from cluster and principal component analyses, which include previously reported data from the West and East Pacific Margins, suggest that, for these locations in the Pacific Ocean, prokaryotic communities from methane hydrate-bearing sediment cores are distinct from those in hydrate-free cores. The recognition of which microbial groups prevail under distinctive subseafloor environments is a significant step toward determining the role these communities play in Earth's essential biogeochemical processes.
Global maps of sulfate and methane in marine sediments reveal two provinces of subsurface metabolic activity: a sulfate-rich open-ocean province, and an ocean-margin province where sulfate is limited ...to shallow sediments. Methane is produced in both regions but is abundant only in sulfate-depleted sediments. Metabolic activity is greatest in narrow zones of sulfate-reducing methane oxidation along ocean margins. The metabolic rates of subseafloor life are orders of magnitude lower than those of life on Earth's surface. Most microorganisms in subseafloor sediments are either inactive or adapted for extraordinarily low metabolic activity.
Subseafloor sediment hosts a large, taxonomically rich, and metabolically diverse microbial ecosystem. However, the factors that control microbial diversity in subseafloor sediment have rarely been ...explored. Here, we show that bacterial richness varies with organic degradation rate and sediment age. At three open-ocean sites (in the Bering Sea and equatorial Pacific) and one continental margin site (Indian Ocean), richness decreases exponentially with increasing sediment depth. The rate of decrease in richness with increasing depth varies from site to site. The vertical succession of predominant terminal electron acceptors correlates with abundance-weighted community composition but does not drive the vertical decrease in richness. Vertical patterns of richness at the open-ocean sites closely match organic degradation rates; both properties are highest near the seafloor and decline together as sediment depth increases. This relationship suggests that (i) total catabolic activity and/or electron donor diversity exerts a primary influence on bacterial richness in marine sediment and (ii) many bacterial taxa that are poorly adapted for subseafloor sedimentary conditions are degraded in the geologically young sediment, where respiration rates are high. Richness consistently takes a few hundred thousand years to decline from near-seafloor values to much lower values in deep anoxic subseafloor sediment, regardless of sedimentation rate, predominant terminal electron acceptor, or oceanographic context.
Subseafloor sediment provides a wonderful opportunity to investigate the drivers of microbial diversity in communities that may have been isolated for millions of years. Our paper shows the impact of in situ conditions on bacterial community structure in subseafloor sediment. Specifically, it shows that bacterial richness in subseafloor sediment declines exponentially with sediment age, and in parallel with organic-fueled oxidation rate. This result suggests that subseafloor diversity ultimately depends on electron donor diversity and/or total community respiration. This work studied how and why biological richness changes over time in the extraordinary ecosystem of subseafloor sediment.
We examine the 0–100 Ma paleoceanographic record retained in pelagic clay from the South Pacific Gyre (SPG) by analyzing 47 major, trace, and rare earth elements in bulk sediment in 206 samples from ...seven sites drilled during Integrated Ocean Drilling Program Expedition 329. We use multivariate statistical analyses (Q‐mode factor analysis and multiple linear regression) of the geochemical data to construct a model of bulk pelagic clay composition and mass accumulation rates (MAR) of six end‐members, (post‐Archean average Australian shale, rhyolite, basalt, Fe‐Mn‐oxyhydroxides, apatite, and excess Si). Integrating the results with Co‐based age models at Sites U1365, U1366, U1369, and U1370, we link changes in MAR of these components to global oceanographic, terrestrial, and climatic transformations through the Cenozoic. Our results track the spatial extent (thousands of kilometers) of dust deposition in the SPG during the aridification of Australia. Dispersed ash is a significant component of the pelagic clay, often comprising >50% by mass, and records episodes of Southern Hemisphere volcanism. Because both are transported by wind, the correlation of dust and ash MAR depends on the site's latitude and suggests meridional shifts in the position of atmospheric circulation cells. The hydrothermal MARs provide evidence for rapid deposition from the Osbourn Trough spreading ridge before it went extinct. Excess Si MARs show that the abrupt increase in siliceous productivity observed at Site U1371 also extended at least as far north as Sites U1369 and U1370, suggesting large‐scale reorganizations of oceanic Si distributions ~10–8 Ma in the southern SPG.
Key Points
Forty‐seven element concentrations in 206 bulk sediment samples from seven sites in the South Pacific
Multivariate statistical models quantify dust, ash, and other fluxes 100–0 Ma
Dust and ash records climate and meridional shifts in atmospheric circulation
Subseafloor sedimentary life in the South Pacific Gyre D'Hondt, Steven; Spivack, Arthur J; Pockalny, Robert ...
Proceedings of the National Academy of Sciences - PNAS,
07/2009, Letnik:
106, Številka:
28
Journal Article
Recenzirano
Odprti dostop
The low-productivity South Pacific Gyre (SPG) is Earth's largest oceanic province. Its sediment accumulates extraordinarily slowly (0.1-1 m per million years). This sediment contains a living ...community that is characterized by very low biomass and very low metabolic activity. At every depth in cored SPG sediment, mean cell abundances are 3 to 4 orders of magnitude lower than at the same depths in all previously explored subseafloor communities. The net rate of respiration by the subseafloor sedimentary community at each SPG site is 1 to 3 orders of magnitude lower than the rates at previously explored sites. Because of the low respiration rates and the thinness of the sediment, interstitial waters are oxic throughout the sediment column in most of this region. Consequently, the sedimentary community of the SPG is predominantly aerobic, unlike previously explored subseafloor communities. Generation of H₂ by radiolysis of water is a significant electron-donor source for this community. The per-cell respiration rates of this community are about 2 orders of magnitude higher (in oxidation/reduction equivalents) than in previously explored anaerobic subseafloor communities. Respiration rates and cell concentrations in subseafloor sediment throughout almost half of the world ocean may approach those in SPG sediment.
PDF
