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

Abstract

Fishes host a diverse microbiome in their gills, but a broad characterization of this microbiome at the metagenomic level is lacking. Here, we apply genome-resolved metagenomics to the gills of the hamlets (Hypoplectrus spp), a group of reef fishes from the Greater Caribbean. The analysis of 353 gill samples from 15 hamlet species collected at eight locations over 13 years revealed a stark contrast between the gill microbiota and reef water microbial communities, indicating a distinct and specific gill microbiome. A total of 70 gill-associated metagenome-assembled genomes (MAGs) were recovered. These MAGs belong to 17 lineages, most of which are novel. They relate to known fish gill pathogens, fish gut microbes, free-living and biofilm-associated taxa, indicating that the gill microbiome was assembled from a collection of distinct eco-evolutionary trajectories. The MAGs harbor diverse metabolic modules, involved notably in nitrogen cycling, antibiotic production and biofilm formation, revealing a highly dynamic microbial ecosystem. One lineage in the Burkholderiaceae family was outstandingly prevalent across fish host species, sampling locations and years. Its genome encoded complete metabolic modules for carbon fixation and sulfur oxidation, indicating chemosynthetic potential. To the best of our knowledge, this is the first line of evidence that fishes may host sulfur-oxidizing chemosynthetic bacteria in their gills. The functional significance of this chemosynthetic potential for the fish host or other members of the gill microbiome remains to be established. The high prevalence of this lineage allowed to build a pangenome. It revealed large-scale geographic structure (western Caribbean, eastern Caribbean and Gulf of Mexico), which parallels the phylogenomic pattern observed in the hamlets. Overall, our findings point to complex fish host-microbe and microbe-microbe eco-evolutionary interactions in the gills that may influence fish physiology, homeostasis and immune response.