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 non-mammalian species. To investigate this we performed a reciprocal translocation of Atlantic salmon between captive and semi-natural conditions. Wild and hatchery-reared fry were transferred to three common garden experimental environments for six weeks: standard hatchery conditions, hatchery conditions with an enriched diet, and simulated wild conditions. We characterised 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 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 environment, with no detectable historical 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 colonisation history, including a number of OTUs characteristic of captive rearing. These results may have important implications for host adaptation to local selective pressures, and also highlight how conditions during early life can have a long-term influence on the microbiome and, potentially, host health.

Neutral Processes Dominate Microbial Community Assembly in Atlantic Salmon, Salmo salar

“…These data corresponded broadly with increasingly negative NTI values among later lifecycle stages and suggest that a subset of host-adapted, taxonomically-related OTUs come to dominate the S. salar microbiome as it matures. The declining trend in OTU richness observed across lifecycle stages in our study is also consistent with observations that gut OTU richness declines with age in juvenile Atlantic salmon (45). As we noted in a previous study based on the wild salmon dataset (4), Mycoplasma sp.…”

Dissecting the factors shaping fish skin microbiomes in a heterogeneous inland water system

“…appear to constitute small fractions of normal microbiomes and culture dependent techniques grossly overrepresent them [20]. Additional studies identified stress indicators [21] and probiotics candidates [22], both with conceivable applications in aquaculture and nature conservation, as well as the finding that captivity reduces the skin microbiome biodiversity [18,23,24]. Consistent salinity bioindicators were also recovered in an experimental system utilizing euryhaline fish [25].…”

“…Amazon River fish were also found to have high Alphaproteobacteria under certain physicochemical conditions [31]. In stark contrast, Gammaproteobacteria dominated the skin microbiome in wild S. salar fry [24], and also that of Silurus glanis, catfish caught in the wild [16]. Of the five instances, the catfish is the only strictly-freshwater inhabitant, but it lacks scales.…”

Spatial Structure of Marine Host-Associated Microbiomes: Effect of Taxonomy, Species Traits, and Study Design

“…Three species' microbiomes were tested for more than one tissue type; for example one species where the skin microbiome showed spatial structure but the gut microbiome did not (the fish Elacatinus prochilos) 0.5 was scored for presence and 0.5 for absence. salmon skin and gut microbiomes are strongly influenced by environmental conditions, but that developmental history also influences microbiome structure (Uren Webster et al, 2019). Similarly, returning adult Atlantic salmon in Canadian and Irish sites shared similar gut microbiomes to oceanic adult salmon from Greenland, but adult microbiomes were distinct from those of juvenile freshwater life stages (Llewellyn et al, 2015).…”