Pathways of carbon and energy metabolism of the epibiotic community associated with the deep-sea hydrothermal vent shrimp Rimicaris exoculata

© The Authors, 2011. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PLoS One 6 (2011): e16018, doi:10.1371/journal.pone.0016018.The shrimp Rimicaris exoculata dominates the faunal biomass at many deep-sea hydrothermal vent sites at the Mid-Atlantic Ridge. In its enlarged gill chamber it harbors a specialized epibiotic bacterial community for which a nutritional role has been proposed. We analyzed specimens from the Snake Pit hydrothermal vent field on the Mid-Atlantic Ridge by complementing a 16S rRNA gene survey with the analysis of genes involved in carbon, sulfur and hydrogen metabolism. In addition to Epsilon- and Gammaproteobacteria, the epibiotic community unexpectedly also consists of Deltaproteobacteria of a single phylotype, closely related to the genus Desulfocapsa. The association of these phylogenetic groups with the shrimp was confirmed by fluorescence in situ hybridization. Based on functional gene analyses, we hypothesize that the Gamma- and Epsilonproteobacteria are capable of autotrophic growth by oxidizing reduced sulfur compounds, and that the Deltaproteobacteria are also involved in sulfur metabolism. In addition, the detection of proteobacterial hydrogenases indicates the potential for hydrogen oxidation in these communities. Interestingly, the frequency of these phylotypes in 16S rRNA gene clone libraries from the mouthparts differ from that of the inner lining of the gill chamber, indicating potential functional compartmentalization. Our data show the specific association of autotrophic bacteria with Rimicaris exoculata from the Snake Pit hydrothermal vent field, and suggest that autotrophic carbon fixation is contributing to the productivity of the epibiotic community with the reductive tricarboxylic acid cycle as one important carbon fixation pathway. This has not been considered in previous studies of carbon fixation and stable carbon isotope composition of the shrimp and its epibionts. Furthermore, the co-occurrence of sulfur-oxidizing and sulfur-reducing epibionts raises the possibility that both may be involved in the syntrophic exchange of sulfur compounds, which could increase the overall efficiency of this epibiotic community.Funding was provided through NSF grant OCE-0452333 and the Alfried Krupp Wissenschaftskolleg Greifswald, Germany (SMS), the Max Planck Society, the German Research Foundation (DFG) Cluster of Excellence at Marum, and MOMARnet (ND, JMP), and IFM-GEOMAR (MH, JFI)

Proposal of Giesbergeria voronezhensis gen. nov., sp nov and G. kuznetsovii sp nov and reclassification of [Aquaspirillum] anulus, [A.] sinuosum and [A.] giesbergeri as Giesbergeria anulus comb. nov., G. sinuosa comb. nov and G-giesbergeri comb. nov., and [Aquaspirillum] metamorphum and [A-psychrophilum as Simplicispira metamorpha gen. nov., comb. nov and S. psychrophila comb. nov.

Five Gram-negative, motile, spiral-shaped strains were isolated from a sulfide spring (D-412T), active sludge of wastewater (D-419T, D-420, D-424) and industrial wastewater (D-416). Comparative 16S rRNA gene sequence analysis showed that the isolates belong to the family Comamonadaceae, within the class Betaproteobacteria, but fall into a distinct cluster. On the basis of phenotypic, chemotaxonomic and phylogenetic data, a new genus, Giesbergeria gen. nov., is proposed, including five species. The type species of the genus is Giesbergeria voronezhensis sp. nov. (type strain D-419T = DSM 12825T = CIP 107340T = VKM B-2350T) and other novel members of the genus are Giesbergeria kuznetsovii sp. nov. (type strain D-412T = DSM 12827T = VKM B-2352T), Giesbergeria giesbergeri comb. nov. (basonym Aquaspirillum giesbergeri), Giesbergeria sinuosa comb. nov. (basonym Aquaspirillum sinuosum) and Giesbergeria anulus comb. nov. (basonym Aquaspirillum anulus). Using the same criteria, isolate D-416 (= DSM 12826) was identified as a strain of [Aquaspirillum] metamorphum. Strain D-416, the type strain of [A.] metamorphum and the type strain of [Aquaspirillum] psychrophilum form a distinct cluster within the family Comamonadaceae (97-97.2% 16S rRNA gene sequence similarity) and share phenotypic and chemotaxonomic properties. Therefore, it is proposed that these strains are reclassified as members of a new genus, Simplicispira gen. nov., as Simplicispira metamorpha comb. nov. (the type species) and Simplicispira psychrophila comb. nov., respectively