Colwellia and sulfur-oxidizing bacteria: An unusual dual symbiosis in a Terua mussel (Mytilidae: Bathymodiolinae) from whale falls in the Antilles arc

• Terua n. sp. is the first mussel species identified from whale fall ecosystems in the Antilles arc (Guadeloupe).
• It derives from ancestors found in the Pacific Ocean.
• Terua n. sp. harbors an unusual dual symbiosis involving extracellular sulfur-oxidizing and Colwellia-related bacteria.
• This symbiosis could be an adaptation to sunken bone habitats.

Seven individuals of a single morphotype of mussels (Bivalvia: Mytilidae) were found attached to a naturally sunken whale intervertebral disk collected in Guadeloupe (Caribbean) at 800 m depth. These specimens resemble small Idas mussels which are found worldwide at cold seeps and hydrothermal vents, and typically harbor ectosymbiotic bacteria on their gills upon which they depend for nutrition. Based on multi-locus gene sequencing, these specimens appear to belong to a new species closely related to two species now included within the genus Terua. Unexpectedly, its closest relatives are found in the Pacific, questioning how this species has reached the Antilles arc. Based on marker gene sequence analysis, electron and fluorescence microscopy, Terua n. sp. harbors two distinct and abundant extracellular bacterial symbionts located between microvilli at the apical surface of host gill epithelial cells. One is a sulfur-oxidizing bacterium similar to the symbionts previously identified in several deep-sea mussels, while the other is related to Colwellia species, a group of cold-adapted heterotrophic bacteria able to degrade organic compounds. This study provides the first evidence for the existence of a dual symbiosis in mussels from whale fall ecosystems in the Caribbean. The evolutionary history of Terua n. sp. and potential role of its Colwellia symbionts are discussed.