A large fraction of globally produced methane is converted to CO2 by anaerobic oxidation in marine sediments. Strong geochemical evidence for net methane consumption in anoxic sediments is based on methane profiles, radiotracer experiments and stable carbon isotope data. But the elusive microorganisms mediating this reaction have not yet been isolated, and the pathway of anaerobic oxidation of methane is insufficiently understood. Recent data suggest that certain archaea reverse the process of methanogenesis by interaction with sulphate-reducing bacteria. Here we provide microscopic evidence for a structured consortium of archaea and sulphate-reducing bacteria, which we identified by fluorescence in situ hybridization using specific 16S rRNA-targeted oligonucleotide probes. In this example of a structured archaeal-bacterial symbiosis, the archaea grow in dense aggregates of about 100 cells and are surrounded by sulphate-reducing bacteria. These aggregates were abundant in gas-hydrate-rich sediments with extremely high rates of methane-based sulphate reduction, and apparently mediate anaerobic oxidation of methane.
Gas hydrates occur at the sediment surface on the southern summit of Hydrate Ridge, Cascadia convergent margin. The hydrates are found in mounds several meters in diameter and up to 2 m high, and are covered by sediment and mats of the filamentous sulfur-oxidizing bacteria Beggiatoa. The mounds are surrounded by vesicomyid clams (Calyptogena pacifica, C. kilmeri), which in turn are encircled by solemyid bivalves (Acharax sp.). The zonation pattern of 3 species (Calyptogena spp. and Acharax sp., which harbor chemoautotrophic bacteria in their gills, and the chemoautotrophic Beggiatoa), is also reflected in a change in the entire community structure. Beggiatoa, Calyptogena spp. and Acharax sp. are shown to be characteristic species for the different communities. The Beggiatoa community directly overlaying the gas hydrates consists of seep endemic species in high densities: gastropods (Provanna laevis, P. lomana, Pyropelta corymba, Hyalogyrina sp. nov.), bivalves (Nuculana sp. nov.) and polychaetes (Ampharetidae, Polynoidae, Dorvilleidae). Based on pooled samples, the rarefaction curves show a decrease in species diversity in the Beggiatoa and Calyptogena communities. The hydrogen sulfide gradients in the porewater of sediments below the different communities dominated by either Beggiatoa, Calyptogena spp. or Acharax sp. vary by 3 orders of magnitude. The diffusive sulfide flux based on the measured sulfide concentration gradients is highest in Beggiatoa sp. communities (23 ± 13 mol m -2 yr -1 ), slightly less in Calyptogena communities (6.6 ± 2.4 mol m -2 yr -1 ), and low in Acharax communities (0.05 ± 0.05 mol m -2 yr -1). The difference in the sulfide environment is a factor influencing the distribution patterns of the chemoautotrophy-dependant and heterotrophic species at the deep-sea sediments containing gas hydrate.KEY WORDS: Gas hydrate · Community structure · Biomass · Diversity · Sulfide · Chemoautotrophy · Cold seep
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