The gills of reef fish support a distinct microbiome influenced by hostspecific factors

Abstract

Teleost fish represent the most diverse of the vertebrate groups and play important roles in food webs, as ecosystem engineers, and as vectors for microorganisms. However, the microbial ecology of fishes remains underexplored for most host taxa and for certain niches on the fish body. This is particularly true for the gills, the key sites of respiration and waste exchange in fishes. Here we provide a comprehensive analysis of the gill microbiome. We focus on ecologically diverse taxa from coral reefs around Moorea, sampling the gills and intestines of adults and juveniles representing 15 families. The gill microbiome composition differed significantly from that of the gut for both adults and juveniles, with fish-associated niches having lower alpha diversity values and higher beta diversity values than those for seawater, sediment, and alga-associated microbiomes. Of ~45,000 operational taxonomic units (OTUs) detected across all samples, 11% and 13% were detected only in the gill and the intestine, respectively. OTUs most enriched in the gill included members of the gammaproteobacterial genus Shewanella and the family Endozoicimonaceae. In adult fish, both gill and intestinal microbiomes varied significantly among host species grouped by diet category. Gill and intestinal microbiomes from the same individual were more similar to one another than to gill and intestinal microbiomes from different individuals. These results demonstrate that distinct body sites are jointly influenced by host-specific organizing factors operating at the level of the host individual. The results also identify taxonomic signatures unique to the gill and the intestine, confirming fish-associated niches as distinct reservoirs of marine microbial diversity.