Phylogenetic relationships of hydrothermal vent mussels (Bathymodiolinae) and their symbionts

Abstract

Deep-sea mussels of the subfamily Bathymodiolinae (Bivalvia, Pteriomorphia, Mytilidae) are dominant members of hydrothermal vent communities across the globe and have been found within every known hydrothermal vent biogeographic province. Thus, the apparent rarity of bathymodiolines at vents of the Juan de Fuca Ridge (JdF) is a notable exception. We examined mussels collected from the JdF over a span of 18 yr to clarify the classifications of mussel hosts and their symbiotic bacteria, and the relationships between sparsely distributed individuals. Several specimens, previously classified as Bathymodiolus and Adipicola, were reassigned as Adipicola sp. JdF based on new phylogenetic evidence and previous morphological studies. Adipicola sp. JdF are the most deeply branching members of Adipicola identified to date. Ultrastructural, molecular phylogenetic, and stable carbon isotope analyses indicated that Adipicola sp. JdF mussels harbor bacterial chemoautotrophic symbionts that appear to be extracellular and that are closely related to symbionts of other bathymodioline hosts. This study demonstrates that a sparsely distributed, yet cohesive, population of Adipicola has inhabited JdF vents for at least the past 18 yr. Moreover, the presence of extracellular symbionts in Adipicola sp. JdF at hydrothermal vents stands in contrast to the evolutionary patterns proposed for bathymodiolines in general. Adipicola sp. JdF represents an exception to the trend of bathymodiolines harboring extracellular symbionts living exclusively in shallow marine wood and bone habitats (<1000 m), indicating that bathymodiolines are more flexible with regard to habitat and symbiont characteristics than previously considered.