Host species-specific gene expression by a widespread and flexible chemosynthetic symbiont

Associations with microbial symbionts shape the ecology and evolution of almost all eukaryotes. One of their defining features is their specificity, but despite this, many symbioses show a degree of flexibility, with some symbiont species capable of colonizing multiple (often closely related) host species. Although widespread, the functional and evolutionary consequences of flexibility in host-symbiont pairings is poorly understood. Bivalves from the diverse, globally distributed, and ecologically important family Lucinidae are ideal for investigating this, as multiple host species can associate with the same symbiont species, often at the same location. We used metatranscriptomics to investigate the molecular responses of one symbiont species, Candidatus Thiodiazotropha endolucinida, in association with three different host species that co-occur in seagrass meadows in the Caribbean Sea. In replicated experiments, we identified host species-specific patterns of symbiont gene expression including those for key functions such as carbon fixation, cell division, and sulfide oxidation. Our work shows that the symbiont consistently responds in different ways to association with different host species. Because all samples were collected at the same site on the same day, and were thus exposed to the same environmental conditions, these differences are likely driven by host rather than environmental factors. In addition, host species had significantly different carbon isotope signatures, which were consistent with distinct modes of host-microbe interaction indicated by transcriptomics. Our results show that not only symbiont genotype, but also symbiont phenotype may enable coexistence of closely related host species, demonstrating the power of symbiosis in promoting and maintaining biodiversity.