Epsilonproteobacteria as gill epibionts of the hydrothermal vent gastropod Cyathermia naticoides (North East-Pacific Rise)

Mollusks, and particularly gastropods, are one of the major taxonomic groups at vents. In these ecosystems, devoid of light, chemoautotrophic bacteria are at the base of the food web and symbiotic association between metazoa and these bacteria is numerous. Nevertheless, apart few “large-size” well-known species, the “small-size” gastropods (shell <5 mm), although very abundant, remain poorly studied regarding symbioses. We investigated here Cyathermia naticoides (Waren and Bouchet in Zool Scr 18(1), 1989), a small coiled gastropod found in abundance on the East Pacific Rise among Riftia pachyptila tubes, and usually inferred to graze on tubeworm bacterial cover, and/or filter feeding. Among mollusks, symbioses are well known in large species and almost exclusively rely on sulfide or methane-oxidizing proteobacterial endosymbionts, occurring within the host tissues in gill epithelial bacteriocytes. Combining several approaches (molecular biology, microscopy, stable isotopes analyses), we described here an unusual symbiosis, where autotrophic filamentous Epsilonproteobacteria are located extracellularly, at the base of host gill filaments. Numerous endocytotic lysosome-like structures were observed in the gill epithelium of the animal suggesting bacteria may contribute to its nutrition through intracellular digestion by gill cells. Additional food source by non-symbiotic proteobacteria grazed on R. pachyptila tubes could complete the diet. The possible role of temperature in the selection of Epsilon- vs Gammaproteobacterial partners is discussed.