Microenvironments of black-tip reef sharks (Carcharhinus melanopterus) provide niche habitats for distinct bacterial communities

Abstract

Animal holobionts constitute diverse yet interconnected landscapes of microenvironments that harbor specific bacterial communities with distinct functions. An increasing body of literature suggests a partitioning and distinct functional profiles of bacterial communities across shark microenvironments, which has led to the proposition that beneficial bacterial functions may contribute to shark health. Here, we provide a first assessment of bacterial communities in different microenvironments of black-tip reef sharks ( Carcharhinus melanopterus ), the most abundant reef shark species across the Indo-West Pacific. Collecting samples from 34 sharks from the Amirante Islands, Seychelles, we characterized the corresponding bacterial communities of two external skin locations, within the buccal cavity, and of the cloaca (representing the gut microbiome) using 16S rRNA gene amplicon sequencing. Overall, shark-associated bacterial communities were distinct from seawater, and skin, buccal, and cloaca samples were distinct from each other. Shark cloaca samples and seawater exhibited lower bacterial alpha diversity and richness compared to the other microenvironments. Predicted functional profiles and Linear Discriminant Effect Size analysis suggest potential differences in metabolic pathways present in the different shark-associated bacterial communities and in the seawater. Taxonomy-based functional inference suggests cloaca-associated bacterial communities specialize in the consumption and breakdown of various food items. Taken together, our data suggest distinct bacterial niche habitats within the ‘microbial landscape’ of black-tip reef sharks, as indicated by distinct bacterial communities and their predicted metabolic functions. Future (meta)genomic and functional work will help reveal potential roles of bacteria in the health of their shark hosts.