Dataset Information

Niche partitioning of diverse sulfur-oxidizing bacteria at hydrothermal vents.

ABSTRACT: At deep-sea hydrothermal vents, primary production is carried out by chemolithoautotrophic microorganisms, with the oxidation of reduced sulfur compounds being a major driver for microbial carbon fixation. Dense and highly diverse assemblies of sulfur-oxidizing bacteria (SOB) are observed, yet the principles of niche differentiation between the different SOB across geochemical gradients remain poorly understood. In this study niche differentiation of the key SOB was addressed by extensive sampling of active sulfidic vents at six different hydrothermal venting sites in the Manus Basin, off Papua New Guinea. We subjected 33 diffuse fluid and water column samples and 23 samples from surfaces of chimneys, rocks and fauna to a combined analysis of 16S rRNA gene sequences, metagenomes and real-time in situ measured geochemical parameters. We found Sulfurovum Epsilonproteobacteria mainly attached to surfaces exposed to diffuse venting, while the SUP05-clade dominated the bacterioplankton in highly diluted mixtures of vent fluids and seawater. We propose that the high diversity within Sulfurimonas- and Sulfurovum-related Epsilonproteobacteria observed in this study derives from the high variation of environmental parameters such as oxygen and sulfide concentrations across small spatial and temporal scales.

SUBMITTER: Meier DV

PROVIDER: S-EPMC5520155 | biostudies-literature | 2017 Jul

REPOSITORIES: biostudies-literature

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Niche partitioning of diverse sulfur-oxidizing bacteria at hydrothermal vents.

Meier Dimitri V DV Pjevac Petra P Bach Wolfgang W Hourdez Stephane S Girguis Peter R PR Vidoudez Charles C Amann Rudolf R Meyerdierks Anke A

The ISME journal 20170404 7

At deep-sea hydrothermal vents, primary production is carried out by chemolithoautotrophic microorganisms, with the oxidation of reduced sulfur compounds being a major driver for microbial carbon fixation. Dense and highly diverse assemblies of sulfur-oxidizing bacteria (SOB) are observed, yet the principles of niche differentiation between the different SOB across geochemical gradients remain poorly understood. In this study niche differentiation of the key SOB was addressed by extensive sampli ...[more]

PMID: 28375213

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Project description:Conspicuous egg-shaped, white, and smooth structures were observed at a hydrothermal vent site in the Guaymas Basin, Gulf of California. The gelatinous structures decomposed within hours after sampling. Scanning electron microscopy (SEM) and light microscopy showed that the structure consisted of filaments of less than 0.1 μm thickness, similar to those observed for "Candidatus Arcobacter sulfidicus." SEM-energy-dispersive X-ray spectroscopy (EDS) showed that the filaments were sulfur rich. According to 16S rRNA gene amplicon and fluorescence in situ hybridization (FISH) analyses, Arcobacter, a sulfide oxidizer that is known to produce filamentous elemental sulfur, was among the dominant species in the structure and was likely responsible for its formation. Arcobacter normally produces woolly snowflake like structures in opposed gradients of sulfide and oxygen. In the laboratory, we observed sulfide consumption in the anoxic zone of the structure, suggesting an anaerobic conversion. The sulfide oxidation and decomposition of the structure in the laboratory may be explained by dissolution of the sulfur filaments by reaction with sulfide under formation of polysulfides. IMPORTANCE At the deep-sea Guaymas Basin hydrothermal vent system, sulfide-rich hydrothermal fluids mix with oxygenated seawater, thereby providing a habitat for microbial sulfur oxidation. Microbial sulfur oxidation in the deep sea involves a variety of organisms and processes and can result in the excretion of elemental sulfur. Here, we report on conspicuous white and smooth gelatinous structures found on hot vents. These strange egg-shaped structures were often observed on previous occasions in the Guaymas Basin, but their composition and formation process were unknown. Our data suggest that the notable and highly ephemeral structure was likely formed by the well-known sulfide-oxidizing Arcobacter. While normally Arcobacter produces loose flocs or woolly layers, here smooth gel-like structures were found.

Project description:BACKGROUND:Chemolithoautotrophic primary production sustains dense invertebrate communities at deep-sea hydrothermal vents and hydrocarbon seeps. Symbiotic bacteria that oxidize dissolved sulfur, methane, and hydrogen gases nourish bathymodiolin mussels that thrive in these environments worldwide. The mussel symbionts are newly acquired in each generation via infection by free-living forms. This study examined geographical subdivision of the thiotrophic endosymbionts hosted by Bathymodiolus mussels living along the eastern Pacific hydrothermal vents. High-throughput sequencing data of 16S ribosomal RNA encoding gene and fragments of six protein-coding genes of symbionts were examined in the samples collected from nine vent localities at the East Pacific Rise, Galápagos Rift, and Pacific-Antarctic Ridge. RESULTS:Both of the parapatric sister-species, B. thermophilus and B. antarcticus, hosted the same numerically dominant phylotype of thiotrophic Gammaproteobacteria. However, sequences from six protein-coding genes revealed highly divergent symbiont lineages living north and south of the Easter Microplate and hosted by these two Bathymodiolus mussel species. High heterogeneity of symbiont haplotypes among host individuals sampled from the same location suggested that stochasticity associated with initial infections was amplified as symbionts proliferated within the host individuals. The mussel species presently contact one another and hybridize along the Easter Microplate, but the northern and southern symbionts appear to be completely isolated. Vicariance associated with orogeny of the Easter Microplate region, 2.5-5.3 million years ago, may have initiated isolation of the symbiont and host populations. Estimates of synonymous substitution rates for the protein-coding bacterial genes examined in this study were 0.77-1.62%/nucleotide/million years. CONCLUSIONS:Our present study reports the most comprehensive population genetic analyses of the chemosynthetic endosymbiotic bacteria based on high-throughput genetic data and extensive geographical sampling to date, and demonstrates the role of the geographical features, the Easter Microplate and geographical distance, in the intraspecific divergence of this bacterial species along the mid-ocean ridge axes in the eastern Pacific. Altogether, our results provide insights into extrinsic and intrinsic factors affecting the dispersal and evolution of chemosynthetic symbiotic partners in the hydrothermal vents along the eastern Pacific Ocean.

Dataset Information

Niche partitioning of diverse sulfur-oxidizing bacteria at hydrothermal vents.

Publications

Niche partitioning of diverse sulfur-oxidizing bacteria at hydrothermal vents.

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