Aquatic organisms are increasingly exposed to lowering of environmental pH due to anthropogenic pressure (e.g. acid rain, acid mine drainages). Such acute variations trigger imbalance of fish-associated microbiota, which in turn favour opportunistic diseases. We used the tambaqui (Colossoma macropomum), an Amazonian fish tolerant to significant pH variation in its natural environment, to assess the response of fish endogenous microbiota to acute short-term acid stress. We exposed 36 specimens of tambaquis to acidic water (pH 4.0) over 2 consecutive weeks and sampled cutaneous mucus, feces and water at 0, 7 & 14 days. The 16S RNA hypervariable region V4 was sequenced on Illumina MiSeq. After two weeks of acidic exposure, fecal and skin microbiota taxonomic structures exhibited different patterns: skin microbiota was still exhibiting a significantly disturbed composition whereas fecal microbiota recovered a similar composition to control group, thus suggesting a stronger resilience capacity of the intestinal microbiota than cutaneous microbiota.
Interactions between parasite, host and host-associated microbiota are increasingly understood as important determinants of disease progression and morbidity. Salmon lice, including the parasitic copepod Lepeophtheirus salmonis and related species, are perhaps the most important problem facing Atlantic Salmon aquaculture after feed sustainability. Salmon lice parasitize the surface of the fish, feeding off mucus, scales and underlying tissue. Secondary bacterial infections are a major source of associated morbidity. In this study we tracked the diversity and composition of Salmo salar skin surface microbiota throughout a complete L. salmonis infection cycle among 800 post-smolts as compared to healthy controls. Among infected fish we observed a significant reduction in microbial richness (Chao1, P = 0.0136), raised diversity (Shannon, P < 7.86e-06) as well as highly significant destabilisation of microbial community composition (Pairwise Unifrac, beta-diversity, P < 1.86e-05; P = 0.0132) by comparison to controls. While undetectable on an individual level, network analysis of microbial taxa on infected fish revealed the association of multiple pathogenic genera (Vibrio, Flavobacterium, Tenacibaculum, Pseudomonas) with high louse burdens. We discuss our findings in the context of ecological theory and colonisation resistance, in addition to the role microbiota in driving primary and secondary pathology in the host.
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.
Fish gut microbial communities play key functions for their hosts, but their ontogenesis is poorly understood. Recent studies on the zebrafish suggest that gut symbionts are recruited naturally through horizontal transmission from environmental water. We used an alternative fish model, the discus (Symphysodon aequifasciata), to identify the main factors driving fish gut microbiota ontogenesis. The discus exhibits a unique parenting behavior: both discus parents vertically feed their fry with a cutaneous mucus secretion during three weeks post-hatching. We hypothesized that vertical microbial transmission via parental mucus feeding, along with horizontal transmission of environmental microbial symbionts, helps to shape the taxonomic structure of the discus fry gut microbiota. To assess this premise, we thoroughly documented the gut microbiota ontogenesis of a discus progeny during 100 days post-hatching. The V4 16S rRNA gene was sequenced to assess taxonomic structure of fry gut, parent mucus, and water samples. Our main results suggest that specific microbial symbionts both from the parents skin mucus and environmental water play important roles in shaping the structure of the fry gut microbiota.
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.
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