Artificial Rearing of Atlantic Salmon Juveniles for Supportive Breeding Programs Induces Long-Term Effects on Gut Microbiota after Stocking.

In supportive breeding programs for wild salmon populations, stocked parr experience higher mortality rates than wild ones. Among other aspects of phenotype, the gut microbiota of artificially raised parr differs from that of wild parr before stocking. Early steps of microbiota ontogeny are tightly dependent upon environmental conditions, both of which exert long-term effects on host physiology. Therefore, our objective was to assess to what extent the resilience capacity of the microbiota of stocked salmon may prevent taxonomic convergence with that of their wild congeners after two months in the same natural environment. Using the 16S SSU rRNA marker gene, we tested the general hypothesis that environmental conditions during the very first steps of microbiota ontogeny imprint a permanent effect on later stages of microbiota recruitment. Our results first showed that gut microbiota composition of stocked and wild parr from the same genetic population, and sharing the same environment, was dependent on the early rearing environment. In contrast, skin microbiota in stocked individuals converged to that of wild individuals. Taxonomic composition and co-occurrence network analyses suggest an impairment of wild bacteria recruitment and a higher instability for the gut microbiota of stocked parr. This study is the first to demonstrate the long-term effect of early microbiota ontogeny in artificial rearing for natural population conservation programs, raising the need to implement microbial ecology.

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.

Structural and compositional mismatch between captive and wild Atlantic salmon (Salmo salar) parrs' gut microbiota highlights the relevance of integrating molecular ecology for management and conservation methods.

Stocking methods are used in the Province of Quebec to restore Salmo salar populations. However, Atlantic salmon stocked juveniles show higher mortality rates than wild ones when introduced into nature. Hatchery environment, which greatly differs from the natural environment, is identified as the main driver of the phenotypic mismatch between captive and wild parrs. The latter is also suspected to impact the gut microbiota composition, which can be associated with essential metabolic functions for their host. We hypothesized that hatchery-raised parrs potentially recruit gut microbial communities that are different from those recruited in the wild. This study evaluated the impacts of artificial rearing on gut microbiota composition in 0+ parrs meant for stocking in two distinct Canadian rivers: Rimouski and Malbaie (Quebec, Canada). Striking differences between hatchery and wild-born parrs' gut microbiota suggest that microbiota could be another factor that could impact their survival in the targeted river, because the microbiome is narrowly related to host physiology. For instance, major commensals belonging to Enterobacteriaceae and Clostridiacea from wild parrs' gut microbiota were substituted in captive parrs by lactic acid bacteria from the Lactobacillaceae family. Overall, captive parrs host a generalist bacterial community whereas wild parrs' microbiota is much more specialized. This is the very first study demonstrating extensive impact of captive rearing on intestinal microbiota composition in Atlantic salmon intended for wild population stocking. Our results strongly suggest the need to implement microbial ecology concepts into conservation management of endangered salmon stocks supplemented with hatchery-reared parrs.