Dual energy metabolism of the Campylobacterota endosymbiont in the chemosynthetic snail Alviniconcha marisindica.

Some deep-sea chemosynthetic invertebrates and their symbiotic bacteria can use molecular hydrogen (H2) as their energy source. However, how much the chemosynthetic holobiont (endosymbiont-host association) physiologically depends on H2 oxidation has not yet been determined. Here, we demonstrate that the Campylobacterota endosymbionts of the gastropod Alviniconcha marisindica in the Kairei and Edmond fields (kAlv and eAlv populations, respectively) of the Indian Ocean, utilize H2 in response to their physical and environmental H2 conditions, although the 16S rRNA gene sequence of both the endosymbionts shared 99.6% identity. A thermodynamic calculation using in situ H2 and hydrogen sulfide (H2S) concentrations indicated that chemosynthetic symbiosis could be supported by metabolic energy via H2 oxidation, particularly for the kAlv holobiont. Metabolic activity measurements showed that both the living individuals and the gill tissues consumed H2 and H2S at similar levels. Moreover, a combination of fluorescence in situ hybridization, quantitative transcript analyses, and enzymatic activity measurements showed that the kAlv endosymbiont expressed the genes and enzymes for both H2- and sulfur-oxidations. These results suggest that both H2 and H2S could serve as the primary energy sources for the kAlv holobiont. The eAlv holobiont had the ability to utilize H2, but the gene expression and enzyme activity for hydrogenases were much lower than for sulfur-oxidation enzymes. These results suggest that the energy acquisitions of A. marisindica holobionts are dependent on H2- and sulfur-oxidation in the H2-enriched Kairei field and that the mechanism of dual metabolism is controlled by the in situ H2 concentration.