Diverse styles of submarine venting on the ultraslow spreading Mid-Cayman Rise

German, Christopher R.; Bowen, A.; Coleman, Max; Honig, D. L.; Huber, Julie A.; Jakuba, M.; Kinsey, James C.; Kurz, Mark D.; Leroy, Sylvie; McDermott, J. M.; Lépinay, Bernard Mercier de; Nakamura, Kozo; Seewald, Jeffrey S.; Smith, Julie L.; Sylva, Sean P.; Dover, C. L. Van; Whitcomb, Louis L.; Yoerger, D.

doi:10.1073/pnas.1009205107

Cited by 150 publications

(158 citation statements)

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“…SUP05 is abundant in oxic/anoxic interfacial environments such as deep-sea hydrothermal plumes (Sunamura et al, 2004;Dick and Tebo, 2010;German et al, 2010), oxygen minimum zones (Stevens and Ulloa, 2008;Lavik et al, 2009;Walsh et al, 2009;Canfield et al, 2010) and symbioses with deep-sea bivalves (Newton et al, 2007). Our data set supports previous genomic studies that showed that members of this group are chemolithoautotrophic, obtaining energy by coupling sulfur oxidation to reduction of nitrate and/or oxygen (Newton et al, 2007;Walsh et al, 2009).…”

Section: Discussionsupporting

confidence: 80%

“…Thus, little is known about the nature of plume microbial communities or their relationship to those of the seafloor or surrounding deep seawater. Several studies have reported the SUP05 group of sulfur-oxidizing Gammaproteobacteria in deep-sea hydrothermal plumes in widespread geographical locations (Sunamura et al, 2004;Dick and Tebo, 2010;German et al, 2010). Other prevalent microbial groups identified in plumes include Epsilonproteobacteria (Sunamura et al, 2004;Nakagawa et al, 2005;German et al, 2010), ammonia-oxidizing Betaproteobacteria (Lam et al, 2008), methanotrophs (Naganuma et al, 2004;Lam et al, 2008) and Marine Group I (MGI) archaea (Takai et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

“…Several studies have reported the SUP05 group of sulfur-oxidizing Gammaproteobacteria in deep-sea hydrothermal plumes in widespread geographical locations (Sunamura et al, 2004;Dick and Tebo, 2010;German et al, 2010). Other prevalent microbial groups identified in plumes include Epsilonproteobacteria (Sunamura et al, 2004;Nakagawa et al, 2005;German et al, 2010), ammonia-oxidizing Betaproteobacteria (Lam et al, 2008), methanotrophs (Naganuma et al, 2004;Lam et al, 2008) and Marine Group I (MGI) archaea (Takai et al, 2004). Although these studies have expanded our knowledge of the major microbial groups present in plumes, it remains unclear which microbes are metabolically active in the plume environment, how they are linked to biogeochemical processes of interest and whether they are derived from seafloor environments (for example, chimneys and sediments) or ambient deep seawater.…”

Section: Introductionmentioning

confidence: 99%

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The metatranscriptome of a deep-sea hydrothermal plume is dominated by water column methanotrophs and lithotrophs

et al. 2012

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Microorganisms mediate geochemical processes in deep-sea hydrothermal vent plumes, which are a conduit for transfer of elements and energy from the subsurface to the oceans. Despite this important microbial influence on marine geochemistry, the ecology and activity of microbial communities in hydrothermal plumes is largely unexplored. Here, we use a coordinated metagenomic and metatranscriptomic approach to compare microbial communities in Guaymas Basin hydrothermal plumes to background waters above the plume and in the adjacent Carmen Basin. Despite marked increases in plume total RNA concentrations (3-4 times) and microbially mediated manganese oxidation rates (15-125 times), plume and background metatranscriptomes were dominated by the same groups of methanotrophs and chemolithoautotrophs. Abundant community members of Guaymas Basin seafloor environments (hydrothermal sediments and chimneys) were not prevalent in the plume metatranscriptome. De novo metagenomic assembly was used to reconstruct genomes of abundant populations, including Marine Group I archaea, Methylococcaceae, SAR324 Deltaproteobacteria and SUP05 Gammaproteobacteria. Mapping transcripts to these genomes revealed abundant expression of genes involved in the chemolithotrophic oxidation of ammonia (amo), methane (pmo) and sulfur (sox). Whereas amo and pmo gene transcripts were abundant in both plume and background, transcripts of sox genes for sulfur oxidation from SUP05 groups displayed a 10-20-fold increase in plumes. We conclude that the biogeochemistry of Guaymas Basin hydrothermal plumes is mediated by microorganisms that are derived from seawater rather than from seafloor hydrothermal environments such as chimneys or sediments, and that hydrothermal inputs serve as important electron donors for primary production in the deep Gulf of California.

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Section: Discussionsupporting

confidence: 80%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The metatranscriptome of a deep-sea hydrothermal plume is dominated by water column methanotrophs and lithotrophs

et al. 2012

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“…Located at 2,350-m depth on the Mid-Cayman Rise (13,14), hydrothermal fluids emanate from the Von Damm vent field at temperatures as high as 226°C (Fig. S1).…”

Section: Resultsmentioning

confidence: 99%

Pathways for abiotic organic synthesis at submarine hydrothermal fields

McDermott

Seewald

German

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

286

303

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Arguments for an abiotic origin of low-molecular weight organic compounds in deep-sea hot springs are compelling owing to implications for the sustenance of deep biosphere microbial communities and their potential role in the origin of life. Theory predicts that warm H 2 -rich fluids, like those emanating from serpentinizing hydrothermal systems, create a favorable thermodynamic drive for the abiotic generation of organic compounds from inorganic precursors. Here, we constrain two distinct reaction pathways for abiotic organic synthesis in the natural environment at the Von Damm hydrothermal field and delineate spatially where inorganic carbon is converted into bioavailable reduced carbon. We reveal that carbon transformation reactions in a single system can progress over hours, days, and up to thousands of years. Previous studies have suggested that CH 4 and higher hydrocarbons in ultramafic hydrothermal systems were dependent on H 2 generation during active serpentinization. Rather, our results indicate that CH 4 found in vent fluids is formed in H 2 -rich fluid inclusions, and higher n-alkanes may likely be derived from the same source. This finding implies that, in contrast with current paradigms, these compounds may form independently of actively circulating serpentinizing fluids in ultramafic-influenced systems. Conversely, widespread production of formate by ΣCO 2 reduction at Von Damm occurs rapidly during shallow subsurface mixing of the same fluids, which may support anaerobic methanogenesis. Our finding of abiogenic formate in deep-sea hot springs has significant implications for microbial life strategies in the present-day deep biosphere as well as early life on Earth and beyond.abiotic organic synthesis | hydrothermal systems | methane | formate | fluid-vapor inclusions S eawater-derived hydrothermal fluids venting at oceanic spreading centers are a net source for dissolved carbon to the deep sea, with vent fluid carbon contents directly tied to the sustenance of the subseafloor biosphere (1). Highly reducing fluids rich in dissolved H 2 , such as those discharging from serpentinizing hydrothermal systems, are of particular interest because of the potential for abiotic reduction of dissolved inorganic carbon ðΣCO 2 = CO 2 + HCO − 3 + CO 2− 3 Þ to organic compounds (2-6) and their potential role as precursor compounds for prebiotic chemistry associated with the origin of life (7). Although there is increasing evidence that supports an abiotic origin for CH 4 and other low-molecular weight organic compounds in ultramafic-hosted hydrothermal systems (8-10), the physical conditions, reaction pathways, and timescales that control abiotic organic synthesis at oceanic spreading centers remain elusive. Working models for the formation of abiotic CH 4 and other hydrocarbons observed in vent fluids involve reduction of ΣCO 2 and/or CO through Fischer-Tropsch-type processes during active circulation of seawater-derived hydrothermal fluids that are highly enriched in dissolved H 2 because of serpentinization of...

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“…Surveys of the small subunit (SSU) ribosomal RNA (rRNA) genes using tag pyrosequencing and clone libraries have revealed the composition of plume microbial communities (Sunamura et al, 2004;Dick and Tebo, 2010;German et al, 2010;Sylvan et al, 2012). Metagenomic, metatranscriptomic and metaproteomic methods have provided insights into the roles of dominant organisms involved in oxidation of sulfur, hydrogen, methane and ammonia in hydrothermal plumes such as SUP05 Gammaproteobacteria , Methylococcaceae Gammaproteobacteria (Li et al, 2014a), Marine Group I Thaumarchaea (Baker et al, 2012) and SAR324 Deltaproteobacteria (Sheik et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center

2015

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Microbial processes within deep-sea hydrothermal plumes affect ocean biogeochemistry on global scales. In rising hydrothermal plumes, a combination of microbial metabolism and particle formation processes initiate the transformation of reduced chemicals like hydrogen sulfide, hydrogen, methane, iron, manganese and ammonia that are abundant in hydrothermal vent fluids. Despite the biogeochemical importance of this rising portion of plumes, it is understudied in comparison to neutrally buoyant plumes. Here we use metagenomics and bioenergetic modeling to describe the abundance and genetic potential of microorganisms in relation to available electron donors in five different hydrothermal plumes and three associated background deep-sea waters from the Eastern Lau Spreading Center located in the Western Pacific Ocean. Three hundred and thirty one distinct genomic 'bins' were identified, comprising an estimated 951 genomes of archaea, bacteria, eukarya and viruses. A significant proportion of these genomes is from novel microorganisms and thus reveals insights into the energy metabolism of heretofore unknown microbial groups. Community-wide analyses of genes encoding enzymes that oxidize inorganic energy sources showed that sulfur oxidation was the most abundant and diverse chemolithotrophic microbial metabolism in the community. Genes for sulfur oxidation were commonly present in genomic bins that also contained genes for oxidation of hydrogen and methane, suggesting metabolic versatility in these microbial groups. The relative diversity and abundance of genes encoding hydrogen oxidation was moderate, whereas that of genes for methane and ammonia oxidation was low in comparison to sulfur oxidation. Bioenergetic-thermodynamic modeling supports the metagenomic analyses, showing that oxidation of elemental sulfur with oxygen is the most dominant catabolic reaction in the hydrothermal plumes. We conclude that the energy metabolism of microbial communities inhabiting rising hydrothermal plumes is dictated by the underlying plume chemistry, with a dominant role for sulfur-based chemolithoautotrophy.

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Diverse styles of submarine venting on the ultraslow spreading Mid-Cayman Rise

Cited by 150 publications

References 41 publications

The metatranscriptome of a deep-sea hydrothermal plume is dominated by water column methanotrophs and lithotrophs

The metatranscriptome of a deep-sea hydrothermal plume is dominated by water column methanotrophs and lithotrophs

Pathways for abiotic organic synthesis at submarine hydrothermal fields

Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center

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