Abstract
Chemosynthetic symbioses underpin animal life at deep-sea hydrothermal vents, encompassing substantial variabilities in symbiont identity, metabolic capacity, and host dependence. Here, we characterise symbioses in two peltospirid snails from Mid-Atlantic Ridge vents,
Peltospira gargantua
and
P. smaragdina
, using 3D anatomical reconstruction, stable isotope analyses, fluorescence
in situ
hybridization, transmission electron microscopy, and metagenomics. Both species hosted abundant intracellular
Campylobacterota
within bacteriocytes of a hypertrophied oesophageal gland. Their dominant symbionts belonged to genus
Sulfurimonas
, but the two hosts were associated with distinct symbiont lineages. Symbiont genomes encoded carbon fixation through the rTCA cycle, sulfide oxidation, and Group I Ni-Fe hydrogenases, indicating combined thiotrophic and hydrogenotrophic capacities. Hydrogenase copy number varied across vent fields from one to three copies. The
P. gargantua
symbiont from the hydrogen-enriched Hydra vent field carried two divergent copies, including one with a truncated catalytic region, potentially reflecting local adaptation to vent geochemistry. Anatomical and isotopic comparisons further revealed contrasting host dependence, with
P. gargantua
having a proportionally larger oesophageal gland and ventricle coupled with a reduced radula, as well as a greater nitrogen-isotope enrichment between symbiotic and non-symbiotic tissues. The smaller oesophageal gland and larger feeding apparatus of
P. smaragdina
point to it being mixotrophic. Previously, all known peltospirid symbioses have partnered with
Gammaproteobacteria
, and we expand the known diversity of peltospirid symbioses. Our findings underscore how closely related hosts can exhibit different degrees of dependence on symbiosis, and that mixotrophic symbiosis may be prevalent in small vent species previously thought to be non-symbiotic.