Abundance and distribution of Archaea in the subseafloor sedimentary biosphere.
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ABSTRACT:
SUBMITTER: Hoshino T
PROVIDER: S-EPMC6298964 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Submarine mud volcanoes (SMVs) are formed by muddy sediments and breccias extruded to the seafloor from a source in the deep subseafloor and are characterized by the discharge of methane and other hydrocarbon gasses and deep-sourced fluids into the overlying seawater. Although SMVs act as a natural pipeline connecting the Earth's surface and subsurface biospheres, the dispersal of deep-biosphere microorganisms and their ecological roles remain largely unknown. In this study, we investigated the microbial communities in sediment and overlying seawater at two SMVs located on the Ryukyu Trench off Tanegashima Island, southern Japan. The microbial communities in mud volcano sediments were generally distinct from those in the overlying seawaters and in the well-stratified Pacific margin sediments collected at the Peru Margin, the Juan de Fuca Ridge flank off Oregon, and offshore of Shimokita Peninsula, northeastern Japan. Nevertheless, in-depth analysis of different taxonomic groups at the sub-species level revealed that the taxon affiliated with Atribacteria, heterotrophic anaerobic bacteria that typically occur in organic-rich anoxic subseafloor sediments, were commonly found not only in SMV sediments but also in the overlying seawater. We designed a new oligonucleotide probe for detecting Atribacteria using the catalyzed reporter deposition-fluorescence in situ hybridization (CARD-FISH). CARD-FISH, digital PCR and sequencing analysis of 16S rRNA genes consistently showed that Atribacteria are abundant in the methane plumes of the two SMVs (0.58 and 1.5 × 104 cells/mL, respectively) but not in surrounding waters, suggesting that microbial cells in subseafloor sediments are dispersed as "deep-biosphere seeds" into the ocean. These findings may have important implications for the microbial transmigration between the deep subseafloor biosphere and the hydrosphere.
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Project description:The global geographic distribution of subseafloor sedimentary microbes and the cause(s) of that distribution are largely unexplored. Here, we show that total microbial cell abundance in subseafloor sediment varies between sites by ca. five orders of magnitude. This variation is strongly correlated with mean sedimentation rate and distance from land. Based on these correlations, we estimate global subseafloor sedimentary microbial abundance to be 2.9?10(29) cells [corresponding to 4.1 petagram (Pg) C and ?0.6% of Earth's total living biomass]. This estimate of subseafloor sedimentary microbial abundance is roughly equal to previous estimates of total microbial abundance in seawater and total microbial abundance in soil. It is much lower than previous estimates of subseafloor sedimentary microbial abundance. In consequence, we estimate Earth's total number of microbes and total living biomass to be, respectively, 50-78% and 10-45% lower than previous estimates.
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Project description:The exploration of Earth's terrestrial subsurface biosphere has led to the discovery of several new archaeal lineages of evolutionary significance. Similarly, the deep subseafloor crustal biosphere also harbors many unique, uncultured archaeal taxa, including those belonging to Candidatus Hydrothermarchaeota, formerly known as Marine Benthic Group-E. Recently, Hydrothermarchaeota was identified as an abundant lineage of Juan de Fuca Ridge flank crustal fluids, suggesting its adaptation to this extreme environment. Through the investigation of single-cell and metagenome-assembled genomes, we provide insight into the lineage's evolutionary history and metabolic potential. Phylogenomic analysis reveals the Hydrothermarchaeota to be an early-branching archaeal phylum, branching between the superphylum DPANN, Euryarchaeota, and Asgard lineages. Hydrothermarchaeota genomes suggest a potential for dissimilative and assimilative carbon monoxide oxidation (carboxydotrophy), as well as sulfate and nitrate reduction. There is also a prevalence of chemotaxis and motility genes, indicating adaptive strategies for this nutrient-limited fluid-rock environment. These findings provide the first genomic interpretations of the Hydrothermarchaeota phylum and highlight the anoxic, hot, deep marine crustal biosphere as an important habitat for understanding the evolution of early life.
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Project description:We explore archaeal distributions in sedimentary subseafloor habitats of Guaymas Basin and the adjacent Sonora Margin, located in the Gulf of California, México. Sampling locations include (1) control sediments without hydrothermal or seep influence, (2) Sonora Margin sediments underlying oxygen minimum zone water, (3) compacted, highly reduced sediments from a pressure ridge with numerous seeps at the base of the Sonora Margin, and (4) sediments impacted by hydrothermal circulation at the off-axis Ringvent site. Generally, archaeal communities largely comprise Bathyarchaeal lineages, members of the Hadesarchaea, MBG-D, TMEG, and ANME-1 groups. Variations in archaeal community composition reflect locally specific environmental challenges. Background sediments are divided into surface and subsurface niches. Overall, the environmental setting and history of a particular site, not isolated biogeochemical properties out of context, control the subseafloor archaeal communities in Guaymas Basin and Sonora Margin sediments.
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Project description:Costa Rica Margin Subseafloor Microbial Community Analysis
| PRJEB11766 | ENA
Project description:Oceanic ridge flank systems represent one of the largest and least-explored microbial habitats on Earth. Fundamental ecological questions regarding community activity, recruitment, and succession in this environment remain unanswered. Here, we investigated ammonia-oxidizing archaea (AOA) in the sediment-buried basalts on the oxic and young ridge flank at North Pond, a sediment-filled pond on the western flank of the Mid-Atlantic Ridge, and compared them with those in the overlying sediments and bottom seawater. Nitrification in the North Pond basement is thermodynamically favorable and is supported by a reaction-transport model simulating the dynamics of nitrate in the crustal fluids. Nitrification rate is estimated to account for 6% to 7% of oxygen consumption, which is similar to the ratios found in marine oxic sediments, suggesting that aerobic mineralization of organic matter is the major ammonium source for crustal nitrifiers. Using the archaeal 16S rRNA and amoA genes as phylogenetic markers, we show that AOA, composed solely of Nitrosopumilaceae, are the major archaeal dwellers at North Pond. Phylogenetic analysis reveals that the crustal AOA communities are distinct from those in the bottom seawater and the upper oxic sediments but are similar to those in the basal part of the overlying sediment column, suggesting either similar environmental selection or the dispersal of microbes across the sediment-basement interface. Additionally, quantitative abundance data suggest enrichment of the dominant Nitrosopumilaceae clade (Eta clade) in the basement compared to the seawater. This study explored AOA and their activity in the upper oceanic crust, and our results have ecological implications for the biogeochemical cycling of nitrogen in the crustal subsurface.IMPORTANCE Ridge flanks represent the major avenue of chemical and heat exchange between the Earth's oceans and the lithosphere and are thought to harbor an enormous and understudied biosphere. However, little is known about the diversity and functionality of the crustal biosphere. Here, we report an indigenous community of archaea specialized in ammonia oxidation (i.e., AOA) in the oxic oceanic crust at North Pond. These AOA are the dominant archaea and are likely responsible for most of the cycling taking place in the first step of nitrification, a feasible nitrogen cycling step in the oxic basement. The crustal AOA community structure significantly differs from that in deep ocean water but is similar to that of the community in the overlying sediments in close proximity. This report links the occurrence of AOA to their metabolic activity in the oxic subseafloor crust and suggests that ecological selection and in situ proliferation may shape the microbial community structure in the rocky subsurface.
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Project description:Studies of deeply buried, sedimentary microbial communities and associated biogeochemical processes during Ocean Drilling Program Leg 201 showed elevated prokaryotic cell numbers in sediment layers where methane is consumed anaerobically at the expense of sulfate. Here, we show that extractable archaeal rRNA, selecting only for active community members in these ecosystems, is dominated by sequences of uncultivated Archaea affiliated with the Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group, whereas known methanotrophic Archaea are not detectable. Carbon flow reconstructions based on stable isotopic compositions of whole archaeal cells, intact archaeal membrane lipids, and other sedimentary carbon pools indicate that these Archaea assimilate sedimentary organic compounds other than methane even though methanotrophy accounts for a major fraction of carbon cycled in these ecosystems. Oxidation of methane by members of Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group without assimilation of methane-carbon provides a plausible explanation. Maintenance energies of these subsurface communities appear to be orders of magnitude lower than minimum values known from laboratory observations, and ecosystem-level carbon budgets suggest that community turnover times are on the order of 100-2,000 years. Our study provides clues about the metabolic functionality of two cosmopolitan groups of uncultured Archaea.
| S-EPMC1533785 | biostudies-literature
Project description:The subseafloor marine biosphere may be one of the largest reservoirs of microbial biomass on Earth and has recently been the subject of debate in terms of the composition of its microbial inhabitants, particularly on sediments from the Peru Margin. A metagenomic analysis was made by using whole-genome amplification and pyrosequencing of sediments from Ocean Drilling Program Site 1229 on the Peru Margin to further explore the microbial diversity and overall community composition within this environment. A total of 61.9 Mb of genetic material was sequenced from sediments at horizons 1, 16, 32, and 50 m below the seafloor. These depths include sediments from both primarily sulfate-reducing methane-generating regions of the sediment column. Many genes of the annotated genes, including those encoding ribosomal proteins, corresponded to those from the Chloroflexi and Euryarchaeota. However, analysis of the 16S small-subunit ribosomal genes suggests that Crenarchaeota are the abundant microbial member. Quantitative PCR confirms that uncultivated Crenarchaeota are indeed a major microbial group in these subsurface samples. These findings show that the marine subsurface is a distinct microbial habitat and is different from environments studied by metagenomics, especially because of the predominance of uncultivated archaeal groups.
| S-EPMC2492506 | biostudies-literature
Project description:Ammonia-oxidizing archaea (AOA) dominate microbial communities throughout oxic subseafloor sediment deposited over millions of years in the North Atlantic Ocean. Rates of nitrification correlated with the abundance of these dominant AOA populations, whose metabolism is characterized by ammonia oxidation, mixotrophic utilization of organic nitrogen, deamination, and the energetically efficient chemolithoautotrophic hydroxypropionate/hydroxybutyrate carbon fixation cycle. These AOA thus have the potential to couple mixotrophic and chemolithoautotrophic metabolism via mixotrophic deamination of organic nitrogen, followed by oxidation of the regenerated ammonia for additional energy to fuel carbon fixation. This metabolic feature likely reduces energy loss and improves AOA fitness under energy-starved, oxic conditions, thereby allowing them to outcompete other taxa for millions of years.
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Project description:Marine subsurface sediments on the Pacific margin harbor diverse microbial communities even at depths of several hundreds meters below the seafloor (mbsf) or more. Previous PCR-based molecular analysis showed the presence of diverse reductive dehalogenase gene (rdhA) homologs in marine subsurface sediment, suggesting that anaerobic respiration of organohalides is one of the possible energy-yielding pathways in the organic-rich sedimentary habitat. However, primer-independent molecular characterization of rdhA has remained to be demonstrated. Here, we studied the diversity and frequency of rdhA homologs by metagenomic analysis of five different depth horizons (0.8, 5.1, 18.6, 48.5, and 107.0 mbsf) at Site C9001 off the Shimokita Peninsula of Japan. From all metagenomic pools, remarkably diverse rdhA-homologous sequences, some of which are affiliated with novel clusters, were observed with high frequency. As a comparison, we also examined frequency of dissimilatory sulfite reductase genes (dsrAB), key functional genes for microbial sulfate reduction. The dsrAB were also widely observed in the metagenomic pools whereas the frequency of dsrAB genes was generally smaller than that of rdhA-homologous genes. The phylogenetic composition of rdhA-homologous genes was similar among the five depth horizons. Our metagenomic data revealed that subseafloor rdhA homologs are more diverse than previously identified from PCR-based molecular studies. Spatial distribution of similar rdhA homologs across wide depositional ages indicates that the heterotrophic metabolic processes mediated by the genes can be ecologically important, functioning in the organic-rich subseafloor sedimentary biosphere.
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