Fish microbiota 101: host traits, ecology, and environmental factors influence microbial diversity and biomass associated with marine fishes

Fish are the most diverse and widely distributed vertebrates, yet little is known about the microbial ecology of fishes nor the biological and environmental factors that influence fish microbiota. The microbiota from 101 species of Southern California marine fishes, spanning 22 orders, 55 families, and 83 genera representing ~25% of local marine fish diversity, was analyzed to identify factors that explain microbial diversity patterns in a geographical subset of marine fish biodiversity. We compared fish microbiota from (gill tissue, skin mucus, midgut digesta, and hindgut digesta) using alpha, beta, and gamma diversity while establishing a novel method to estimate microbial biomass associated with these host surfaces (Qiime2 plugin katharoseq). Body site (anatomy) was the strongest driver of microbial diversity but microbial biomass did not differ across body sites. Midgut had the highest diversity and was most influenced by environment (e.g. habitat), but not host phylogeny. Larger, pelagic fishes had lower microbial biomass and diversity in the gill. Patterns of phylosymbiosis were observed across the gill, skin, and hindgut. The majority of microbes from all fish body sites were of unknown origin but overall sea water generally contributes more microbes to fish microbiota compared to marine sediment. In a meta-analysis of vertebrate hindguts (569 species), mammals had the highest gamma diversity when controlling for host species number while fishes had the highest percent of unique microbial taxa (92%). In fishes, the midgut, gill, and skin contains the majority of microbial diversity which collectively can be 5.5 times higher than the hindgut. The composite dataset will be useful to vertebrate microbiota researchers and fish biologists interested in microbial ecology with applications in aquaculture and fisheries management.