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

Abstract

Teleost fishes represent an invaluable repertoire of host species to study the factors shaping animal-associated microbiomes. Several studies have shown that the phylogenetic structure of 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 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 to environmental physicochemistry and bacterioplankton community structure. These results suggest that the variable skin mucus community is a relevant target to develop 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. Especially, 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 fishes 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 different implications: (1) the skin mucus microbiome should be used, rather than the gut, to investigate bacterial biomarkers of ecosystem perturbance in the wild; (2) the gut microbiome is better suited for studies on the drivers of phylosymbiosis, or the co-evolution of fish and their symbionts.

Ecological Specialization Within a Carnivorous Fish Family Is Supported by a Herbivorous Microbiome Shaped by a Combination of Gut Traits and Specific Diet

“…Overall, we found little support for the existence of gut phylosymbiosis in Sparidae fishes, i.e., we did not observe significant relationships between host phylogenetic relatedness and microbiome dissimilarity (using both Mantel tests and CAP analysis). Such result is in agreement with the observation of weak phylosymbiosis signal in skin microbiome of teleost fishes (Chiarello et al, 2018;Doane et al, 2020;Sylvain et al, 2020). In our case, the absence of phylosymbiosis, despite inter-species differences, is driven by the fact that the 10 carnivorous species are spread on the two main branches of the Sparidae phylogeny while they have similar gut traits and microbiome.…”

Skin bacteria of rainbow trout antagonistic to the fish pathogen Flavobacterium psychrophilum

“…Instead, manipulating the skin microbiome to increase their abundance is promising. The skin microbiome of fish is known to be more influenced by surrounding water compared to the gut microbiome 32 , 46 , which was also suggested by our data (Supplementary Fig. S3 online).…”

Ecology Impacts The Decrease of Spirochaetes and Prevotella In The Fecal Gut Microbiota of Urban Humans

“…Having samples from seven different locations available for analysis we could also demonstrate that host location only has a minor in uence on the bacterial community structure. More precisely, location/geography appears to in uence only individual bacterial families in most animals, whereas the broad taxonomic levels are dictated by host phylogeny as has been shown in previous studies [34][35][36]. We could not observe any bacterial clades that were location-speci c and prevalent, most probably due to the central role of host phylogeny for bacterial prevalence patterns as well as the wellde ned and shared dietary information throughout German zoos.…”