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Applied and Environmental Microbiology, November 2003, p. 6785-6792, Vol. 69, No. 11
0099-2240/03/$08.00+0     DOI: 10.1128/AEM.69.11.6785-6792.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Environmental Acquisition of Thiotrophic Endosymbionts by Deep-Sea Mussels of the Genus Bathymodiolus

Yong-Jin Won,1,2,{dagger} Steven J. Hallam,1 Gregory D. O'Mullan,3 Irvin L. Pan,4 Kurt R. Buck,1 and Robert C. Vrijenhoek1*

Monterey Bay Aquarium Research Institute, Moss Landing, California 95039-0628,1 Graduate Program in Ecology and Evolution, Rutgers University, New Brunswick, New Jersey 08901,2 Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 08544,3 Molecular, Cellular, and Developmental Biology Program, Yale University, New Haven, Connecticut 065204

Received 4 April 2003/ Accepted 14 August 2003

Deep-sea Bathymodiolus mussels, depending on species and location, have the capacity to host sulfur-oxidizing (thiotrophic) and methanotrophic eubacteria in gill bacteriocytes, although little is known about the mussels' mode of symbiont acquisition. Previous studies of Bathymodiolus host and symbiont relationships have been based on collections of nonoverlapping species across wide-ranging geographic settings, creating an apparent model for vertical transmission. We present genetic and cytological evidence for the environmental acquisition of thiotrophic endosymbionts by vent mussels from the Mid-Atlantic Ridge. Open pit structures in cell membranes of the gill surface revealed likely sites for endocytosis of free-living bacteria. A population genetic analysis of the thiotrophic symbionts exploited a hybrid zone where two Bathymodiolus species intergrade. Northern Bathymodiolus azoricus and southern Bathymodiolus puteoserpentis possess species-specific DNA sequences that identify both their symbiont strains (internal transcribed spacer regions) and their mitochondria (ND4). However, the northern and southern symbiont-mitochondrial pairs were decoupled in the hybrid zone. Such decoupling of symbiont-mitochondrial pairs would not occur if the two elements were transmitted strictly vertically through the germ line. Taken together, these findings are consistent with an environmental source of thiotrophic symbionts in Bathymodiolus mussels, although an environmentally "leaky" system of vertical transmission could not be excluded.

* Corresponding author. Mailing address: Monterey Bay Aquarium Research Institute, 7700 Sandholdt Rd., Moss Landing, CA 95039-0628. Phone: (831) 775-1799. Fax: (831) 775-1620. E-mail: vrijen{at}mbari.org.

{dagger} Present address: Department of Genetics, Rutgers University, Piscataway, NJ 08854.

Applied and Environmental Microbiology, November 2003, p. 6785-6792, Vol. 69, No. 11
0099-2240/03/$08.00+0     DOI: 10.1128/AEM.69.11.6785-6792.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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