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Abstract

Genetic diversity of closely related free-living microorganisms is
widespread and underpins ecosystem functioning, but most evolutionary
theories predict that it destabilizes intimate mutualisms. Accordingly,
strain diversity is assumed to be highly restricted in intracellular
bacteria associated with animals. Here, we sequenced 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 functions, such as the use of energy and nutrient
sources, electron acceptors and viral defence mechanisms. Most
strain-specific genes were expressed, highlighting their potential to
affect fitness. We show that fine-scale diversity is pervasive in
Bathymodiolus sulfur-oxidizing symbionts, and hypothesize that it may be
widespread in low-cost symbioses where the environment, rather than the
host, feeds the symbionts.