Interpopulation Variation in the Atlantic Salmon Microbiome Reflects Environmental and Genetic Diversity.
ABSTRACT: The microbiome has a crucial influence on host phenotype and is of broad interest to ecological and evolutionary research. Yet, the extent of variation that occurs in the microbiome within and between populations is unclear. We characterized the skin and gut microbiomes of seven populations of juvenile Atlantic salmon (Salmo salar) inhabiting a diverse range of environments, including hatchery-reared and wild populations. We found shared skin operational taxonomic units (OTUs) across all populations and core gut microbiota for all wild fish, but the diversity and structure of both skin and gut microbial communities were distinct between populations. There was a marked difference between the gut microbiomes of wild and captive fish. Hatchery-reared fish had lower intestinal microbial diversity, lacked core microbiota found in wild fish, and showed altered community structure and function. Skin and gut microbiomes were also less varied within captive populations, reflecting more uniform artificial rearing conditions. The surrounding water influenced the microbiome of the gut and, especially, the skin, but could not explain the degree of variation observed between populations. For both gut and skin, we found that there was greater difference in microbiome structures between more genetically distinct fish populations, and that population genetic diversity was positively correlated with microbiome diversity. However, diet is likely to be the major factor contributing to the large differences in gut microbiota between wild and captive fish. Our results highlight the scope of interpopulation variation in the Atlantic salmon microbiome and offer insights into the deterministic factors contributing to microbiome diversity and structure.IMPORTANCE Variation in the microbiome has a fundamental influence on host health, ecology, and evolution, but the scope and basis of this variation are not fully understood. We identified considerable variation in skin and gut microbial communities between seven wild and captive populations of Atlantic salmon, reflecting divergent environmental conditions and fish genetic diversity. In particular, we found very pronounced differences in the intestinal microbiomes of wild and hatchery-reared fish, likely reflecting differences in diet. Our results offer an insight into how the microbiome potentially contributes to the generation of local adaptations in this species and how domestication alters intestinal microbial communities, highlighting future research directions in these areas.
Project description:Microbial communities associated with the gut and the skin are strongly influenced by environmental factors, and can rapidly adapt to change. Historical processes may also affect the microbiome. In particular, variation in microbial colonisation in early life has the potential to induce lasting effects on microbial assemblages. However, little is known about the relative extent of microbiome plasticity or the importance of historical colonisation effects following environmental change, especially for nonmammalian species. To investigate this we performed a reciprocal translocation of Atlantic salmon between artificial and semi-natural conditions. Wild and hatchery-reared fry were transferred to three common garden experimental environments for 6 weeks: standard hatchery conditions, hatchery conditions with an enriched diet, and simulated wild conditions. We characterized the faecal and skin microbiome of individual fish before and after the environmental translocation, using a BACI (before-after-control-impact) design. We found evidence of extensive microbiome plasticity for both the gut and skin, with the greatest changes in alpha and beta diversity associated with the largest changes in environment and diet. Microbiome richness and diversity were entirely determined by environment, with no detectable effects of fish origin, and there was also a near-complete turnover in microbiome structure. However, we also identified, for the first time in fish, evidence of historical colonisation effects reflecting early-life experience, including ASVs characteristic of captive rearing. These results have important implications for host adaptation to local selective pressures, and highlight how conditions experienced during early life can have a long-term influence on the microbiome and, potentially, host health.
Project description:A number of recent studies have shown the importance of the mammalian gut microbiome in host health. In the context of endangered species, a few studies have examined the relationship between the gut microbiome in wild versus captive populations due to digestive and other health issues. Unfortunately, the results seem to vary across taxa in terms of captive animals having higher, lower, or equivalent microbiome diversity relative to their wild counterparts. Here, we focus on the black rhinoceros as captive animals suffer from a number of potentially dietary related health effects. We compared gut microbiomes of wild and captive black rhinos to test for differences in taxonomic diversity (alpha and beta) and in functional diversity of the microbiome. We incorporated a more powerful metagenomic shotgun sequencing approach rather than a targeted amplification of the 16S gene for taxonomic assignment of the microbiome. Our results showed no significant differences in the alpha diversity levels between wild and captive black rhinos, but significant differences in beta diversity. We found that bacterial taxa traditionally associated with ruminant guts of domesticated animals had higher relative abundances in captive rhinos. Our metagenomic sequencing results suggest that unknown gut microbes of wild rhinos are being replaced by those found in conventional human-domesticated livestock. Wild rhinos have significantly different functional bacterial communities compared to their captive counterparts. Functional profiling results showed greater abundance of glycolysis and amino acid synthesis pathways in captive rhino microbiomes, representing an animal receiving sub-optimal nutrition with a readily available source of glucose but possibly an imbalance of necessary macro and micronutrients. Given the differences observed between wild and captive rhino gut microbiomes, we make a number of recommendations for potentially modifying captive gut microbiome to better reflect their wild counterparts and thereby hopefully improve overall rhino health in captivity.
Project description: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.<b>IMPORTANCE</b> 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.
Project description: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.
Project description:Although the gut microbiome benefits the host in several ways, how anthropogenic forces impact the gut microbiome of mammals is not yet completely known. Recent studies have noted reduced gut microbiome diversity in captive mammals due to changes in diet and living environment. However, no studies have been carried out to understand how the gut microbiome of wild mammals responds to domestication. We analyzed the gut microbiome of wild and captive gaur and domestic mithun (domestic form of gaur) to understand whether the gut microbiome exhibits sequential changes from wild to captivity and after domestication. Both captive and domestic populations were characterized by reduced microbial diversity and abundance as compared to their wild counterparts. Notably, two beneficial bacterial families, Ruminococcaceae and Lachnospiraceae, which are known to play vital roles in herbivores' digestion, exhibited lower abundance in captive and domestic populations. Consequently, the predicted bacterial functional pathways especially related to metabolism and immune system showed lower abundance in captive and domestic populations compared to wild population. Therefore, we suggest that domestication can impact the gut microbiome more severely than captivity, which might lead to adverse effects on host health and fitness. However, further investigations are required across a wide range of domesticates in order to understand the general trend of microbiome shifts in domestic animals.
Project description:Metagenomic analysis of 16S ribosomal RNA has been used to profile microbial communities at high resolution, and to examine their association with host diet or diseases. We examined the oral and gut microbiome composition of two captive koalas to determine whether bacterial communities are unusual in this species, given that their diet consists almost exclusively of Eucalyptus leaves. Despite a highly specialized diet, koala oral and gut microbiomes were similar in composition to the microbiomes from the same body regions of other mammals. Rectal swabs contained all of the diversity present in faecal samples, along with additional taxa, suggesting that faecal bacterial communities may merely subsample the gut bacterial diversity. Furthermore, the faecal microbiomes of the captive koalas were similar to those reported for wild koalas, suggesting that captivity may not compromise koala microbial health. Since koalas frequently suffer from ocular diseases caused by Chlamydia infection, we also examined the eye microbiome composition of two captive koalas, establishing the healthy baseline for this body part. The eye microbial community was very diverse, similar to other mammalian ocular microbiomes but with an unusually high representation of bacteria from the family Phyllobacteriaceae.
Project description:Captivity maybe the only choice for survival of many endangered vertebrates, and understanding its broad effects is important for animal management and conservation, including breeding endangered species for subsequent release. Extreme environmental changes during captivity may influence survival ability in the wild. Captivity decreases gut bacterial diversity in a wide range of animals. However, most studies directly compare animals living in captivity with those in the wild, and there is a lack of understanding of effects of gradient shift in lifestyle during species reintroduction based on the soft-release strategy, which involves a confinement period in a field enclosure. Here, we used 16S rRNA amplicon sequencing to analyze gut microbiomes of 11 captive and 12 semi-wild Przewalski's horses (PH; Equus ferus przewalskii) under the same captivity environment, using fecal samples. A subset of samples with abundant extracted DNA (including 3 captive and 3 semi-wild individuals) was selected for whole-genome shotgun sequencing. We found that community diversity did not differ between the semi-wild PH and captive PH, but the semi-wild PH had significantly higher bacterial richness than those in captivity. Relative abundances of all dominant phyla were similar across the semi-wild or captive horses, while those of the non-dominant phyla Tenericutes and Proteobacteria were significantly higher in semi-wild PH than in captive PH. Beta diversity results indicated that bacterial communities of captives and semi-wild horses were clearly separated distinct when considering only composition. Functional profiling of the microbiomes revealed that the semi-wild and captive gut microbiomes were largely similar. However, semi-wild horse microbiomes had higher abundance of bacterial genes related to core metabolic processes, such as carbohydrates, amino acids, and nucleic acid metabolism. The study revealed that semi-wild PH could retain specific non-dominant bacteria and harbor a more diverse microbiome than the captive counterpart, and thus have higher metabolic potential to utilize the complex plants efficiently. These results indicate that change in host lifestyle may play a role in microbiome differentiation in the process of reintroduction, suggesting that a short period of time in captivity is acceptable for PH from the perspective of maintaining the richness of intestinal bacterial flora to some extent.
Project description:Captive breeding has been used as an effective approach to protecting endangered animals but its effect on the gut microbiome and the conservation status of these species is largely unknown. The giant panda is a flagship species for the conservation of wildlife. With integrated efforts including captive breeding, this species has been recently upgraded from "endangered" to "vulnerable" (IUCN 2016). Since a large proportion (21.8%) of their global population is still captive, it is critical to understand how captivity changes the gut microbiome of these pandas and how such alterations to the microbiome might affect their future fitness and potential impact on the ecosystem after release into the wild. Here, we use 16S rRNA (ribosomal RNA) marker gene sequencing and shotgun metagenomics sequencing to demonstrate that the fecal microbiomes differ substantially between wild and captive giant pandas. Fecal microbiome diversity was significantly lower in captive pandas, as was the diversity of functional genes. Additionally, captive pandas have reduced functional potential for cellulose degradation but enriched metabolic pathways for starch metabolism, indicating that they may not adapt to a wild diet after being released into the wild since a major component of their diet in the wild will be bamboo. Most significantly, we observed a significantly higher level of amylase activity but a lower level of cellulase activity in captive giant panda feces than those of wild giant pandas, shown by an in vitro experimental assay. Furthermore, antibiotic resistance genes and virulence factors, as well as heavy metal tolerance genes were enriched in the microbiomes of captive pandas, which raises a great concern of spreading these genes to other wild animals and ecosystems when they are released into a wild environment. Our results clearly show that captivity has altered the giant panda microbiome, which could have unintended negative consequences on their adaptability and the ecosystem during the reintroduction of giant pandas into the wild.
Project description:Studies connecting microbiome composition and functional performance in wildlife have received little attention and understanding their connections with wildlife physical condition are sorely needed. We studied the variation in gut microbiota (hard fecal pellets) between allopatric subspecies of the European wild rabbit in wild populations and in captured individuals studied under captivity. We evaluated the influence of environmental and host-specific factors. The microbiome of wild rabbit populations reduced its heterogeneity under controlled conditions. None of the host-specific factors tested correlated with the microbiota composition. We only observed significant intra-group dispersion for the age factor. The most diverse microbiomes were rich in Ruminococcaceae potentially holding an enriched functional profile with dominance of cellulases and xylanases, and suggesting higher efficiency in the digestion of fiber-rich food. Conversely, low diversity gut microbiomes showed dominance of Enterobacteriaceae potentially rich in amylases. We preliminary noticed geographical variations in field populations with higher dominance of Ruminococcaceae in south-western than in north-eastern Spain. Spatial differences appeared not to be subspecies driven, since they were lost in captivity, but environmentally driven, although differences in social structure and behavior may also play a role that deserve further investigations. A marginally significant relationship between the Ruminococcaceae/Enterobacteriaceae ratio and potential life expectancy was observed in captive rabbits. We hypothesize that the gut microbiome may determine the efficiency of feeding resource exploitation, and can also be a potential proxy for life expectancy, with potential applications for the management of declining wild herbivorous populations. Such hypotheses remain to be explored in the future.
Project description:Much of animal-associated microbiome research has been conducted in species for which little is known of their natural ecology and evolution. Microbiome studies that combine population genetic, environment, and geographic data for wild organisms can be very informative, especially in situations where host genetic variation and the environment both influence microbiome variation. The few studies that have related population genetic and microbiome variation in wild populations have been constrained by observation-based kinship data or incomplete genomic information. Here we integrate population genomic and microbiome analyses in wild threespine stickleback fish distributed throughout western Oregon, USA. We found that gut microbiome diversity and composition partitioned more among than within wild host populations and was better explained by host population genetic divergence than by environment and geography. We also identified gut microbial taxa that were most differentially abundant across environments and across genetically divergent populations. Our findings highlight the benefits of studies that investigate host-associated microbiomes in wild organisms.