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 (Warén 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.
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We thank the chief scientists, N. Le Bris and F. Lallier, as well as the captain and crew of the RV Atalante and the ‘Nautile’ team for their help during the Mescal 2010 cruise. We thank E. Thiébaut and Marjolaine Matabos for their help in sorting an identifying the various gastropods sampled. TEM was performed at the ‘Plateforme de Microscopie Electronique’ (MNHN) with the help of C. Djediat. Work was funded through UPMC and CNRS.
Conflict of interest
The authors declare that they have no conflict of interest.
The authors declare that the experiments comply with the current laws of the country they were performed (France).
Communicated by M.Kühl.
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Phylogenetic reconstruction based on a 100-aa-long fragment of the aclB gene. A maximum-likelihood approach using the JTT matrix-based model and a discrete Gamma distribution of evolutionary rates with a proportion of invariant sites was used. All bacteria from the ingroup are Epsilonproteobacteria, and the tree is rooted on two Aquificales. Boostrap percentage values based on 500 replicates are displayed. Scale bar corresponds to 10 % estimated sequence divergence (PDF 103 kb)
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Zbinden, M., Marqué, L., Gaudron, S.M. et al. Epsilonproteobacteria as gill epibionts of the hydrothermal vent gastropod Cyathermia naticoides (North East-Pacific Rise). Mar Biol 162, 435–448 (2015). https://doi.org/10.1007/s00227-014-2591-7
- Hydrothermal Vent
- Gill Filament
- Filamentous Bacterium
- Gill Epithelium