Environmental plasticity and colonisation history in the Atlantic salmon microbiome: A translocation experiment

Abstract

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.

Microbiota in intestinal digesta of Atlantic salmon (Salmo salar), observed from late freshwater stage until one year in seawater, and effects of functional ingredients: a case study from a commercial sized research site in the Arctic region

“…Compared to fish at SW2 and SW3, the bacterial taxa of fish at SW1 were more similar to the taxa at FW. This may be related to the fact that it takes time to colonize the intestine [ 52 ]. There was only 7 weeks between the FW sampling time point and SW1, whereas the SW1 and SW2 samplings were conducted after 18 weeks intervals.…”

“…Increased levels of genus Mycoplasma with time may therefore be an important characteristic for gut microbiota of adult Atlantic salmon. As Mycoplasma is rarely [ 52 ] or not [ 19 , 59 ] observed in samples from surrounding seawater, their enrichment may be independent of rearing habitat. The reason for their colonization in the intestine is uncertain although they seem to be particularly well-adapted to the intestinal environment of Atlantic salmon.…”

Salmon gut microbiota correlates with disease infection status: potential for monitoring health in farmed animals

“…These practices, while helping to prevent infectious diseases outbreaks, may also compromise the colonization of the sh gut by other, potentially bene cial, bacteria. This, combined with a generally more uniform diet, might be responsible for the lower levels of alpha diversity observed in the investigated salmon when compared to their wild counterparts [79].…”

Salmon Gut Microbiota Correlates With Disease Infection Status: Potential for Monitoring Health in Farmed Animals  

“…The water sterilization procedures aimed to control pathogen infections may also compromise the colonization of the sh gut by other, potentially bene cial, bacteria. This, combined with a generally more uniform diet, might be responsible for the lower levels of alpha diversity observed in the investigated salmon when compared to their wild counterparts [87].…”