Dataset Information

Abundances of hyperthermophilic autotrophic Fe(III) oxide reducers and heterotrophs in hydrothermal sulfide chimneys of the northeastern Pacific Ocean.

ABSTRACT: The abundances of hyperthermophilic heterotrophs, methanogens, and autotrophic reducers of amorphous Fe(III) oxide in 18 samples of deep-sea hydrothermal vent sulfide chimneys of the Endeavour Segment were measured. The results indicate that conditions favor the growth of iron reducers toward the interiors of these deposits and that of heterotrophs toward the outer surfaces near high-temperature polychaete worms (Paralvinella sulfincola).

SUBMITTER: Ver Eecke HC

PROVIDER: S-EPMC2612199 | biostudies-literature | 2009 Jan

REPOSITORIES: biostudies-literature

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Abundances of hyperthermophilic autotrophic Fe(III) oxide reducers and heterotrophs in hydrothermal sulfide chimneys of the northeastern Pacific Ocean.

Ver Eecke Helene C HC Kelley Deborah S DS Holden James F JF

Applied and environmental microbiology 20081031 1

The abundances of hyperthermophilic heterotrophs, methanogens, and autotrophic reducers of amorphous Fe(III) oxide in 18 samples of deep-sea hydrothermal vent sulfide chimneys of the Endeavour Segment were measured. The results indicate that conditions favor the growth of iron reducers toward the interiors of these deposits and that of heterotrophs toward the outer surfaces near high-temperature polychaete worms (Paralvinella sulfincola). ...[more]

PMID: 18978076

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Project description:BackgroundDeep-sea hydrothermal vents are highly productive biodiversity hotspots in the deep ocean supported by chemosynthetic microorganisms. Prominent features of these systems are sulfide chimneys emanating high-temperature hydrothermal fluids. While several studies have investigated the microbial diversity in both active and inactive sulfide chimneys that have been extinct for up to thousands of years, little is known about chimneys that have ceased activity more recently, as well as the microbial succession occurring during the transition from active to inactive chimneys.ResultsGenome-resolved metagenomics was applied to an active and a recently extinct (~?7?years) sulfide chimney from the 9-10° N hydrothermal vent field on the East Pacific Rise. Full-length 16S rRNA gene and a total of 173 high-quality metagenome assembled genomes (MAGs) were retrieved for comparative analysis. In the active chimney (L-vent), sulfide- and/or hydrogen-oxidizing Campylobacteria and Aquificae with the potential for denitrification were identified as the dominant community members and primary producers, fixing carbon through the reductive tricarboxylic acid (rTCA) cycle. In contrast, the microbiome of the recently extinct chimney (M-vent) was largely composed of heterotrophs from various bacterial phyla, including Delta-/Beta-/Alphaproteobacteria and Bacteroidetes. Gammaproteobacteria were identified as the main primary producers, using the oxidation of metal sulfides and/or iron oxidation coupled to nitrate reduction to fix carbon through the Calvin-Benson-Bassham (CBB) cycle. Further analysis revealed a phylogenetically distinct Nitrospirae cluster that has the potential to oxidize sulfide minerals coupled to oxygen and/or nitrite reduction, as well as for sulfate reduction, and that might serve as an indicator for the early stages of chimneys after venting has ceased.ConclusionsThis study sheds light on the composition, metabolic functions, and succession of microbial communities inhabiting deep-sea hydrothermal vent sulfide chimneys. Collectively, microbial succession during the life span of a chimney could be described to proceed from a "fluid-shaped" microbial community in newly formed and actively venting chimneys supported by the oxidation of reductants in the hydrothermal fluid to a "mineral-shaped" community supported by the oxidation of minerals after hydrothermal activity has ceased. Remarkably, the transition appears to occur within the first few years, after which the communities stay stable for thousands of years. Video Abstract.

Project description:Hydrothermal systems are excellent natural laboratories for the study of how chemical energy landscapes shape microbial communities. Yet, only a few attempts have been made to quantify relationships between energy availability and microbial community structure in these systems. Here, we have investigated how microbial communities and chemical energy availabilities vary along cross-sections of two hydrothermal chimneys from the Soria Moria Vent Field and the Bruse Vent Field. Both vent fields are located on the Arctic Mid-Ocean Ridge, north of the Jan Mayen Island and the investigated chimneys were venting fluids with markedly different H2S:CH4 ratios. Energy landscapes were inferred from a stepwise in silico mixing of hydrothermal fluids (HFs) with seawater, where Gibbs energies of relevant redox-reactions were calculated at each step. These calculations formed the basis for simulations of relative abundances of primary producers in microbial communities. The simulations were compared with an analysis of 24 samples from chimney wall transects by sequencing of 16S rRNA gene amplicons using 454 sequencing. Patterns in relative abundances of sulfide oxidizing Epsilonproteobacteria and methane oxidizing Methylococcales and ANME-1, were consistent with simulations. However, even though H2 was present in HFs from both chimneys, the observed abundances of putative hydrogen oxidizing anaerobic sulfate reducers (Archaeoglobales) and methanogens (Methanococcales) in the inner parts of the Soria Moria Chimney were considerably higher than predicted by simulations. This indicates biogenic production of H2 in the chimney wall by fermentation, and suggests that biological activity inside the chimneys may modulate energy landscapes significantly. Our results are consistent with the notion that energy landscapes largely shape the distribution of primary producers in hydrothermal systems. Our study demonstrates how a combination of modeling and field observations can be useful in deciphering connections between chemical energy landscapes and metabolic networks within microbial communities.

Project description:UNLABELLED:Sulfur is an important element in sustaining microbial communities present in hydrothermal vents. Sulfur oxidation has been extensively studied due to its importance in chemosynthetic pathways in hydrothermal fields; however, less is known about sulfate reduction. Here, the metagenomes of hydrothermal chimneys located on the ultraslow-spreading Southwest Indian Ridge (SWIR) were pyrosequenced to elucidate the associated microbial sulfur cycle. A taxonomic summary of known genes revealed a few dominant bacteria that participated in the microbial sulfur cycle, particularly sulfate-reducing Deltaproteobacteria. The metagenomes studied contained highly abundant genes related to sulfur oxidation and reduction. Several carbon metabolic pathways, in particular the Calvin-Benson-Bassham pathway and the reductive tricarboxylic acid cycles for CO2 fixation, were identified in sulfur-oxidizing autotrophic bacteria. In contrast, highly abundant genes related to the oxidation of short-chain alkanes were grouped with sulfate-reducing bacteria, suggesting an important role for short-chain alkanes in the sulfur cycle. Furthermore, sulfur-oxidizing bacteria were associated with enrichment for genes involved in the denitrification pathway, while sulfate-reducing bacteria displayed enrichment for genes responsible for hydrogen utilization. In conclusion, this study provides insights regarding major microbial metabolic activities that are driven by the sulfur cycle in low-temperature hydrothermal chimneys present on an ultraslow midocean ridge. IMPORTANCE:There have been limited studies on chimney sulfides located at ultraslow-spreading ridges. The analysis of metagenomes of hydrothermal chimneys on the ultraslow-spreading Southwest Indian Ridge suggests the presence of a microbial sulfur cycle. The sulfur cycle should be centralized within a microbial community that displays enrichment for sulfur metabolism-related genes. The present study elucidated a significant role of the microbial sulfur cycle in sustaining an entire microbial community in low-temperature hydrothermal chimneys on an ultraslow spreading midocean ridge, which has characteristics distinct from those of other types of hydrothermal fields.

Dataset Information

Abundances of hyperthermophilic autotrophic Fe(III) oxide reducers and heterotrophs in hydrothermal sulfide chimneys of the northeastern Pacific Ocean.

Publications

Abundances of hyperthermophilic autotrophic Fe(III) oxide reducers and heterotrophs in hydrothermal sulfide chimneys of the northeastern Pacific Ocean.

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