Fish Skin and Gut Microbiomes Show Contrasting Signatures of Host Species and Habitat.

Teleost fish represent an invaluable repertoire of host species to study the factors shaping animal-associated microbiomes. Several studies have shown that the phylogenetic structure of the fish gut microbiome is driven by species-specific (e.g., host ancestry, genotype, or diet) and habitat-specific (e.g., hydrochemical parameters and bacterioplankton composition) factors. However, our understanding of other host-associated microbial niches, such as the skin mucus microbiome, remains limited. The goal of our study was to explore simultaneously the phylogenetic structure of the fish skin mucus and gut microbiome and compare the effect of species- and habitat-specific drivers on the structure of microbial communities in both tissues. We sampled 114 wild fish from 6 populations of 3 ecologically and phylogenetically contrasting Amazonian teleost species. Water samples were collected at each site, and 10 physicochemical parameters were characterized. The skin mucus, gut, and water microbial communities were characterized using a metabarcoding approach targeting the V3-V4 regions of the 16S rRNA. Our results showed a significant distinction between the phylogenetic profile and diversity of the microbiome from each microbial niche. Skin mucus and bacterioplankton communities were significantly closer in composition than gut and free-living communities. Species-specific factors mostly modulated gut bacterial communities, while the skin mucus microbiome was predominantly associated with environmental physicochemistry and bacterioplankton community structure. These results suggest that the variable skin mucus community is a relevant target for the development of microbial biomarkers of environmental status, while the more conserved gut microbiome is better suited to study long-term host-microbe interactions over evolutionary time scales.IMPORTANCE Whether host-associated microbiomes are mostly shaped by species-specific or environmental factors is still unresolved. In particular, it is unknown to what extent microbial communities from two different host tissues from the same host respond to these factors. Our study is one of the first to focus on the microbiome of teleost fish to shed a light on this topic as we investigate how the phylogenetic structure of microbial communities from two distinct fish tissues are shaped by species- and habitat-specific factors. Our study showed that in contrast to the teleost gut microbiome, skin mucus communities are highly environment dependent. This result has various implications: (i) the skin mucus microbiome should be used, rather than the gut, to investigate bacterial biomarkers of ecosystem perturbance in the wild, and (ii) the gut microbiome is better suited for studies of the drivers of phylosymbiosis, or the coevolution of fish and their symbionts.

Amazon fish bacterial communities show structural convergence along widespread hydrochemical gradients.

The world's richest freshwater fish community thrives in gradients of contrasting environments in Amazonia, ranging from ion-poor acidic black waters, to ion-rich circumneutral white waters. These hydrochemical gradients structure Amazonian fish assemblages via ecological speciation events. Fish bacterial communities contain an important genetic heritage essential for their hosts' survival and are also involved in adaptive divergence via niche adaptation processes, but the extent to which they evolve in response to hydrochemical gradients in Amazonia is unknown. Here we investigated bacterial communities (gut and skin mucus) of two ecologically and phylogenetically divergent host species (Mesonauta festivus and Serrasalmus rhombeus) distributed throughout these hydrochemical gradients. The goal was to characterize intra- and interspecific Amazonian fish microbiome variations across multiple scales. Using a 16S metabarcoding approach, we investigated the microbiota of 43 wild M. festivus, 32 S. rhombeus and seven water samples, collected at seven sampling sites encompassing both water colours. Taxonomical structures of bacterial communities from both host species were significantly correlated to the environmental continua of magnesium, sodium, dissolved organic carbon, calcium, dissolved O2 , pH, potassium, hardness and chloride. Analysis of discriminating features in community structures across multiple scales demonstrated intra- and interspecific structural parallelisms in the response to the hydrochemical gradients. Together, these parallelisms suggest the action of selection on bacterial community structures along Amazonian hydrochemical gradients. Functional approaches along with reciprocal transplant experiments will provide further insights on the potential contribution of Amazonian fish microbiomes in host adaptation and ecological speciation events.