Diversity matters: Deep-sea mussels harbor multiple symbiont strains

Genetic diversity of closely-related free-living microbes is widespread and underpins ecosystem functioning, but most evolutionary theories predict that it destabilizes intimate mutualisms. Indeed, symbiont strain diversity has long assumed to be restricted in intracellular bacteria associated with animals. Here, we sequenced the metagenomes and metatranscriptomes of 18 Bathymodiolus mussel individuals from four species, covering their known distribution range at deep-sea hydrothermal vents in the Atlantic. We show that as many as 16 strains of intracellular, sulfur-oxidizing symbionts coexist in individual Bathymodiolus mussels. Co-occurring symbiont strains differed extensively in key metabolic functions, such as the use of energy and nutrient sources, electron acceptors and viral defense mechanisms. Most strain-specific genes were expressed, highlighting their adaptive potential. We show that fine-scale diversity is pervasive in Bathymodiolus symbionts, and hypothesize that it may be widespread in low-cost symbioses where the environment, not the host, feeds the symbionts.