High rates of apoptosis visualized in the symbiont-bearing gills of deep-sea Bathymodiolus mussels

Symbiosis between Bathymodiolus and Gammaproteobacteria enables these deep-sea mussels to live in toxic environments like hydrothermal vents and cold seeps. The quantity of endosymbionts within the gill-bacteriocytes appears to vary according to the hosts environment. We investigated the hypothesis of a control of the endosymbionts density by apoptosis, a programmed cell death. We used fluorometric TUNEL-method and active Caspase-3-targeting antibodies to visualize and quantify apoptotic cells in mussel gills. To avoid artefacts due to depressurization upon specimen recovery from the deep-sea, we compared the apoptotic rates between mussels recovered unpressurised, versus mussels recovered in a pressure-maintaining device, in two species from hydrothermal vents on the Mid-Atlantic Ridge: Bathymodiolus azoricus and B. puteoserpentis. Our results show that pressurized recovery had no significant effect on the apoptotic rate in the gill filaments. Apoptotic levels were highest in the ciliated zone and in the circulating hemocytes, compared to the bacteriocyte zone. Apoptotic gill-cells in B. aff. boomerang from the pockmarks off the Gulf of Guinea, show similar distribution patterns. Deep-sea symbiotic mussels have much higher rates of apoptosis in their gills than the coastal mussel Mytilus edulis without chemolithoautotrophic symbionts. We discuss how apoptosis might be one of the mechanisms that contribute to the adaptation of deep-sea mussels to toxic environments and/or to symbiosis.