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

ABSTRACT: 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.

SUBMITTER: Sylvain FE

PROVIDER: S-EPMC7414953 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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

Sylvain François-Étienne FÉ Holland Aleicia A Bouslama Sidki S Audet-Gilbert Émie É Lavoie Camille C Val Adalberto Luis AL Derome Nicolas N

Applied and environmental microbiology 20200803 16

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. T ...[more]

PMID: 32503908

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Project description:Teleost omnivorous fish that coexist partially sharing resources are likely to modify their gut traits and microbiome as a feedback mechanism between ecological processes and evolution. However, we do not understand how the core gut microbiome supports the metabolic capacity of the host and regulates digestive functions in specialized omnivorous fish gut traits. Therefore, we evaluated the gut microbiome of eight omnivorous fish from a single family (i.e., Cyprinidae) in the current study. We examined the correlation between host phylogeny, diet composition, and intestinal morphological traits related to the intestinal microbiome. The results indicated that cyprinid fish with similar relative gut lengths had considerable gut microbiome similarity. Notably, the SL (short relative gut length) group, as zoobenthos and zooplankton specialists, was abundant in Proteobacteria and was less abundant in Firmicutes than in the ML (medium relative gut length) and LL (long relative gut length) groups. These fish could extract nutrients from aquatic plants and algae. Additionally, we found the relative abundance of Clostridium and Romboutsia to be positively correlated with host relative gut length but negatively correlated with the relative abundance of Cetobacterium, Plesiomonas, Bacteroides, and Lactobacillus, and host-relative gut length. We also show a positive linear relationship between host gut microbiome carbohydrate metabolism and relative gut length, while the amino acid and lipid metabolism of the gut microbiome was negatively correlated with host-relative gut length. In addition, omnivorous species competing for resources improve their ecological adaptability through the specialization of gut length, which is closely related to variation in the synergy of the gut microbiome. Above all, specialized gut microbiota and associated gut morphologies enable fish to variably tolerate resource fluctuation and improve the utilization efficiency of nutrient extraction from challenging food resources.

Project description:BackgroundWhile many studies have reported that the structure of the gut and skin microbiota is driven by both species-specific and habitat-specific factors, the relative importance of host-specific versus environmental factors in wild vertebrates remains poorly understood. The aim of this study was to determine the diversity and composition of fish skin, gut, and surrounding water bacterial communities (hereafter referred to as microbiota) and assess the extent to which host habitat and phylogeny predict microbiota similarity. Skin swabs and gut samples from 334 fish belonging to 17 species were sampled in three Laurentian Great Lakes (LGLs) habitats (Detroit River, Lake Erie, Lake Ontario). We also collected and filtered water samples at the time of fish collection. We analyzed bacterial community composition using 16S metabarcoding and tested for community variation.ResultsWe found that the water microbiota was distinct from the fish microbiota, although the skin microbiota more closely resembled the water microbiota. We also found that environmental (sample location), habitat, fish diet, and host species factors shape and promote divergence or convergence of the fish microbiota. Since host species significantly affected both gut and skin microbiota (separately from host species effects), we tested for phylosymbiosis using pairwise host species phylogenetic distance versus bacterial community dissimilarity. We found significant phylogenetic effects on bacterial community dissimilarity, consistent with phylosymbiosis for both the fish skin and gut microbiota, perhaps reflecting the longstanding co-evolutionary relationship between the host species and their microbiomes.ConclusionsAnalyzing the gut and skin mucus microbiota across diverse fish species in complex natural ecosystems such as the LGLs provides insights into the potential for habitat and species-specific effects on the microbiome, and ultimately the health, of the host. Video Abstract.

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

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

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