Proteobacteria with chemosynthetic potential are highly enriched in the gills of Hypoplectrus reef fishes

A variety of marine invertebrates are known to form associations with chemosynthetic bacteria, but to the best of our knowledge this has not been documented in fishes. Here, we apply genome-resolved metagenomics to the hamlets (Hypoplectrus spp), a model system for the study of speciation in the sea. The analysis of 304 gill samples from 12 hamlet species collected at six locations over 13 years revealed a stark contrast between the gill microbiota and ambient water microbial communities. One novel lineage in the Burkholderiaceae-B family was particularly prevalent across host species, sampling locations and years. Its genome encoded highly complete metabolic modules for carbon fixation and sulfur oxidation, indicating chemosynthetic potential. Its pangenome revealed large-scale geographic structure (western Caribbean, eastern Caribbean and Gulf of Mexico), paralleling the phylogenomic pattern observed in the hamlet radiation. Our survey also identified genomes of multiple novel gill-associated lineages related to known fish gill pathogens, fish gut microbes and free-living seawater taxa. These lineages harbor diverse metabolic modules, involved notably in nitrogen cycling, antibiotic production and biofilm formation, revealing a highly dynamic microbial ecosystem. Overall, our findings suggest complex host-microbe and microbe-microbe eco-evolutionary interactions that may influence fish physiology, homeostasis and immune response.