Organosulfur cycling in the multi-partner symbiosis between lucinid bivalves, sulphur-oxidizing symbionts, and Endozoicomonas

Abstract

Organosulfur compounds play an important role in chemotaxis, stress protection, and nutrition in many marine symbioses. Lucinidae, an ancient and species-rich family of marine bivalves, host chemosynthetic sulphur-oxidising bacteria within gill epithelial cells, and is well-known for its contribution to inorganic sulphur cycling in marine sediments worldwide. Little is known about organosulfur transformations by lucinid-associated microbiota or the hosts potential contribution. Here, we integrated field measurements, genomics, transcriptomics, and experimental assays to investigate organosulfur cycling in three lucinid species from temperate and tropical environments. Concentrations of the osmolyte dimethylsulphoniopropionate (DMSP) in lucinids were typically much higher than in their surrounding environment, and varied with host species and season, but not with symbiont abundance. Indeed, candidate DMSP synthesis DSYB genes were expressed by the animal hosts implying that the host may be the source of DMSP. Furthermore, a newly identified and isolated Candidatus Endozoicomonas endolucinida symbiont was capable of DMSP catabolism to dimethylsulphide (DMS), which could be further syntrophically oxidised by the sulphur-oxidising symbionts that encode methanethiol oxidase genes in their genomes. Finally, incubation experiments supported a combined role of the host and its associated microbiome in organosulfur cycling during stress, with the highest DMSP concentrations measured when holobionts were incubated with antibiotics under anoxic conditions. This study identified a previously unrecognised microbial partner in lucinid symbioses and revealed its potential organosulphur-based metabolic interactions with both the host and the sulphur-oxidising symbionts, highlighting the capacity of these widespread associations to influence global organosulfur cycling.