Environmental plasticity and historical colonisation effects in the Atlantic salmon microbiome: a translocation experiment

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 dynamics in early life has the potential to induce lasting effects on microbiome assembly. However, little is known about the relative extent of microbiome plasticity and/or persistence of historical colonisation effects following environmental change, especially for non-mammalian species. To investigate this we performed a reciprocal translocation experiment of Atlantic salmon between captive and semi-natural conditions. Wild and hatchery-reared fry were transferred to three experimental treatments for six weeks: standard hatchery conditions, hatchery conditions with an enriched diet or simulated wild conditions. We characterised the faecal and skin microbiome of individual fish before and after the experimental treatment, using a BACI (before-after-control-impact) experimental design. We found evidence of extensive plasticity in both gut and skin microbiota, 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 experimental treatment, with no detectable lasting effects of fish origin. Microbiome structure was also strongly influenced by current environmental conditions, but for the first time in fish we also found evidence of historical colonisation effects, including a number of OTUs signatory of captive rearing. These results may have important implications for the conservation of natural Atlantic salmon populations, including host adaptation to local selective pressures and stocking success. They also highlight how aquaculture husbandry can have a long-term influence on the microbiome and, potentially, host health.