The gill chamber epibiosis of deep-sea shrimp Rimicaris exoculata: an in-depth metagenomic investigation and discovery of Zetaproteobacteria

Type Article
Date 2014-09
Language English
Author(s) Jan Cyrielle1, Petersen Jillian M.2, Werner Johannes2, 3, Teeling Hanno2, Huang Sixing2, Gloeckner Frank Oliver2, 3, Golyshina Olga V.4, Dubilier Nicole2, Golyshin Peter N.4, Jebbar Mohamed1, 5, Cambon-Bonavita Marie-AnneORCID6
Affiliation(s) 1 : Univ Bretagne Occidentale, LM2E, IUEM, UMR 6197, Plouzane, France.
2 : Max Planck Inst Marine Microbiol, Bremen, Germany.
3 : Jacobs Univ Bremen gGmbH, Bremen, Germany.
4 : Bangor Univ, Sch Biol Sci, Bangor, Gwynedd, Wales.
5 : IUEM, CNRS, UMR6197, LM2E, F-29280 Plouzane, France.
6 : IFREMER, Ctr Brest, REM EEP LM2E, ZI Pointe Diable, F-29280 Plouzane, France.
Source Environmental Microbiology (1462-2912) (Wiley-blackwell), 2014-09 , Vol. 16 , N. 9 , P. 2723-2738
DOI 10.1111/1462-2920.12406
WOS© Times Cited 35
Abstract The gill chamber of deep-sea hydrothermal vent shrimp Rimicaris exoculata hosts a dense community of epibiotic bacteria dominated by filamentous Epsilonproteobacteria and Gammaproteobacteria. Using metagenomics on shrimp from the Rainbow hydrothermal vent field, we showed that both epibiont groups have the potential to grow autotrophically and oxidize reduced sulfur compounds or hydrogen with oxygen or nitrate. For carbon fixation, the Epsilonproteobacteria use the reductive tricarboxylic acid cycle, whereas the Gammaproteobacteria use the Calvin–Benson–Bassham cycle. Only the epsilonproteobacterial epibionts had the genes necessary for producing ammonium. This ability likely minimizes direct competition between epibionts and also broadens the spectrum of environmental conditions that the shrimp may successfully inhabit. We identified genes likely to be involved in shrimp–epibiont interactions, as well as genes for nutritional and detoxification processes that might benefit the host. Shrimp epibionts at Rainbow are often coated with iron oxyhydroxides, whose origin is intensely debated. We identified 16S rRNA sequences and functional genes affiliated with iron-oxidizing Zetaproteobacteria, which indicates that biological iron oxidation might play a role in forming these deposits. Fluorescence in situ hybridizations confirmed the presence of active Zetaproteobacteria in the R. exoculata gill chamber, thus providing the first evidence for a Zetaproteobacteria–invertebrate association.
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Jan Cyrielle, Petersen Jillian M., Werner Johannes, Teeling Hanno, Huang Sixing, Gloeckner Frank Oliver, Golyshina Olga V., Dubilier Nicole, Golyshin Peter N., Jebbar Mohamed, Cambon-Bonavita Marie-Anne (2014). The gill chamber epibiosis of deep-sea shrimp Rimicaris exoculata: an in-depth metagenomic investigation and discovery of Zetaproteobacteria. Environmental Microbiology, 16(9), 2723-2738. Publisher's official version : https://doi.org/10.1111/1462-2920.12406 , Open Access version : https://archimer.ifremer.fr/doc/00177/28874/