Host Shaping Associated Microbiota in Hydrothermal Vent Snails from the Indian Ocean Ridge

Snails at hydrothermal vents rely on symbiotic bacteria for nutrition; however, the specifics of these associations in adapting to such extreme environments remain underexplored. This study investigated the community structure and metabolic potential of bacteria associated with two Indian Ocean vent snails, Chrysomallon squamiferum and Gigantopelta aegis. Using microscopic, phylogenetic, and metagenomic analyses, this study examines bacterial communities inhabiting the foot and gland tissues of these snails. G. aegis exhibited exceptionally low bacterial diversity (Shannon index 0.14-0.18), primarily Gammaproteobacteria (99.9%), including chemosynthetic sulfur-oxidizing Chromatiales using Calvin-Benson-Bassham cycle and methane-oxidizing Methylococcales in the glands. C. squamiferum hosted significantly more diverse symbionts (Shannon indices 1.32-4.60). Its black variety scales were dominated by Campylobacterota (67.01-80.98%), such as Sulfurovum, which perform sulfur/hydrogen oxidation via the reductive tricarboxylic acid cycle, with both Campylobacterota and Gammaproteobacteria prevalent in the glands. The white-scaled variety of C. squamiferum had less Campylobacterota but a higher diversity of heterotrophic bacteria, including Delta-/Alpha-Proteobacteria, Bacteroidetes, and Firmicutes (classified as Desulfobacterota, Pseudomomonadota, Bacteroidota, and Bacillota in GTDB taxonomy). In C. squamiferum, Gammaproteobacteria, including Chromatiales, Thiotrichales, and a novel order "Endothiobacterales," were chemosynthetic, capable of oxidizing sulfur, hydrogen, or iron, and utilizing the Calvin-Benson-Bassham cycle for carbon fixation. Heterotrophic Delta- and Alpha-Proteobacteria, Bacteroidetes, and Firmicutes potentially utilize organic matter from protein, starch, collagen, amino acids, thereby contributing to the holobiont community and host nutrition accessibility. The results indicate that host species and intra-species variation, rather than the immediate habitat, might shape the symbiotic microbial communities, crucial for the snails' adaptation to vent ecosystems.