Coming together – symbiont acquisition and early development ofBathymodiolusmussels

Abstract

Symbiotic associations between animals and microorganisms are widespread and have a profound impact on the ecology, behaviour, physiology, and evolution of the host. Research on deep-sea mussels of the genus Bathymodiolus has revealed how chemosynthetic symbionts sustain their host with energy, allowing them to survive in the nutrient-poor environment of the deep ocean. However, to date, we know little about the initial symbiont colonization and how this is integrated into the early development of these mussels. Here we analysed the early developmental life stages of B. azoricus, “B”. childressi and B. puteoserpentis and the changes that occur once the mussels are colonized by symbionts. We combined synchrotron-radiation based μCT, correlative light and electron microscopy and fluorescence in situ hybridization to show that the symbiont colonization started when the animal settled on the sea floor and began its metamorphosis into an adult animal. Furthermore, we observed aposymbiotic life stages with a fully developed digestive system which was streamlined after symbiont acquisition. This suggests that bathymodiolin mussels change their nutritional strategy from initial filter-feeding to relying on the energy provided by their symbionts. After ~35 years of research on bathymodiolin mussels, we are beginning to answer fundamental ecological questions concerning their life cycle and the establishment of symbiosis.

“There and back again” - Ultrastructural changes in the gills of Bathymodiolus vent-mussels during symbiont loss: Back to a regular filter-feeding epidermis

“…However, the apical spongy appearance could also be a sign that endocytosis continues, but that there are no new bacteria to phagocyte, so the newly created vacuoles remain empty. Endocytosis in Bathymodiolus has indeed been shown possible during the entire life of the deep-sea mussel (Wentrup et al, 2013) and is first seen at the very initiation of the symbiosis in the larval stage, just after metamorphosis (Laming et al, 2018;Franke et al, 2020).…”

“…Additional symbiont types have been identified, but usually in low abundances (Zielinski et al, 2009;Raggi et al, 2013;Assiéet al, 2016). Bathymodiolus acquire their symbionts just after their larval metamorphosis, at the plantigrade settlement stage, and this triggers the differentiation of their gill epithelium into a symbiont containing organ (Laming et al, 2018;Franke et al, 2020). Symbionts can either be acquired from the surrounding environment (i.e.…”

“…horizontal transfer) and/or be escaped symbionts from nearby Bathymodiolus (i.e. lateral transfer), (Won et al, 2003;Wentrup et al, 2013;Franke et al, 2020). During mussel growth, the gills continuously grow in length at their posterior end.…”