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Applied and Environmental Microbiology, April 2005, p. 1694-1700, Vol. 71, No. 4
0099-2240/05/$08.00+0     doi:10.1128/AEM.71.4.1694-1700.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Dual Symbiosis in a Bathymodiolus sp. Mussel from a Methane Seep on the Gabon Continental Margin (Southeast Atlantic): 16S rRNA Phylogeny and Distribution of the Symbionts in Gills

Sébastien Duperron,^1,2 Thierry Nadalig,^1, Jean-Claude Caprais,¹ Myriam Sibuet,¹ Aline Fiala-Médioni,³ Rudolf Amann,² and Nicole Dubilier^2*

IFREMER Département Environnement Profond, Centre de Brest, Plouzané,¹ Université Pierre et Marie Curie (Paris 6), Observatoire Océanologique, Banyuls-sur-Mer, France,³ Max Planck Institute for Marine Microbiology, Bremen, Germany²

Received 28 June 2004/ Accepted 25 October 2004

Deep-sea mussels of the genus Bathymodiolus (Bivalvia: Mytilidae) harbor symbiotic bacteria in their gills and are among the dominant invertebrate species at cold seeps and hydrothermal vents. An undescribed Bathymodiolus species was collected at a depth of 3,150 m in a newly discovered cold seep area on the southeast Atlantic margin, close to the Zaire channel. Transmission electron microscopy, comparative 16S rRNA analysis, and fluorescence in situ hybridization indicated that this Bathymodiolus sp. lives in a dual symbiosis with sulfide- and methane-oxidizing bacteria. A distinct distribution pattern of the symbiotic bacteria in the gill epithelium was observed, with the thiotrophic symbiont dominating the apical region and the methanotrophic symbiont more abundant in the basal region of the bacteriocytes. No variations in this distribution pattern or in the relative abundances of the two symbionts were observed in mussels collected from three different mussel beds with methane concentrations ranging from 0.7 to 33.7 µM. The 16S rRNA sequence of the methanotrophic symbiont is most closely related to those of known methanotrophic symbionts from other bathymodiolid mussels. Surprisingly, the thiotrophic Bathymodiolus sp. 16S rRNA sequence does not fall into the monophyletic group of sequences from thiotrophic symbionts of all other Bathymodiolus hosts. While these mussel species all come from vents, this study describes the first thiotrophic sequence from a seep mussel and shows that it is most closely related (99% sequence identity) to an environmental clone sequence obtained from a hydrothermal plume near Japan.

Present address: Université Louis Pasteur (Strasbourg), Laboratoire de Dynamique, Evolution et Expression de Génomes de Microorganismes, CNRS FRE 2326, Institut de Botanique, Strasbourg, France.