Life and death in facultative chemosymbioses: control of bacterial population dynamics in the Thyasiridae

Stable associations between marine invertebrates and their chemosynthetic bacterial symbionts are predicated on both the adequate transfer of resources and the restriction of bacterial cells to a finite population within host tissues. In symbioses between thyasirid bivalves and thiotrophic bacteria, symbionts are extracellular, acquired from a free-living pool, and periodically endocytosed and digested by host bacteriocytes. Thyasirid symbionts require reduced sulphur to fuel their autotrophic metabolism; the host makes this energy source accessible to symbionts through its burrowing and irrigation behaviours. Here, we demonstrate that unlike the bacterial symbionts of many chemosymbiotic bivalves, those of Thyasira flexuosa and T. cf. gouldi divide while associated with host gill epithelial cells, possibly constituting a second method of symbiont replacement in thyasirid bivalves alongside environmental acquisition. Furthermore, exposure of T. flexuosa and T. cf. gouldi to elevated concentrations of thiosulphate, a reduced sulphur species used by many sulphur-oxidizing bacterial symbionts, results in the rapid onset of bacterial division and expansion of symbiont populations within host gills and can result in host mortality. These results highlight the flexible nature of symbioses in thyasirid bivalves and the possibility for symbiosis breakdown in some thyasirid lineages. Furthermore, results suggest a role for behaviours such as sulphide mining and irrigation in maintaining and controlling a stable population of bacterial symbionts in this family.