Metagenomics of the gill chamber epibiosis of deep-sea shrimp Rimicaris exoculata and discovery of zetaproteobacterial epibionts

The shrimp Rimicaris exoculata flourishes on deep-sea hydrothermal chimneys along the Mid-Atlantic Ridge (MAR). This species harbors dense community of chemoautotrophic epibiotic bacteria associated with mineral oxide deposits in its enlarged gill chamber. We used metagenomics on specimens from the Rainbow hydrothermal vent site, to investigate the metabolism of the two main sulfur-oxidizing epibionts affiliated to the Epsilonproteobacteria and Gammaproteobacteria. Both epibionts had genes of the Sox pathway for sulfur oxidation and hydrogenases. In the epsilonproteobacterial epibiont, two distinct denitrification systems (Nas/Nir and Nap/Nrf) as well as a complete rTCA cycle for carbon dioxide fixation were found, while the gammaproteobacterial epibiont was found to fix carbon dioxide via the CBB cycle with RuBisCo form II. The shrimp gill chamber metagenome provided information on host-epibiont interactions, like on virulence gene homologues and genes for surface attachment. Likewise, genes were found that might play a role in host nutritional and detoxification processes, and thus are of major importance for the survival of the shrimp and its adaptation to the hydrothermal vent environment. Interestingly, analysis of the metagenome revealed sequences affiliated to the iron-oxidizing class Zetaproteobacteria, which would explain gill chamber iron oxyhydroxide deposits. Presence of Zetaproteobacteria was confirmed by fluorescence in situ hybridizations and thereby provided first evidence for a Zetaproteobacteria-invertebrate association.