Time is a stronger predictor of microbiome community composition than tissue in external mucosal surfaces of Atlantic salmon (Salmo salar) reared in a semi-natural freshwater environment

The mucosal surfaces provide the first line of defence to opportunistic pathogens in the external environment as well as other physiological functions including osmoregulation, gas exchange or nutrient absorption in the gut. Atlantic salmon is the most valuable salmonid species cultured worldwide and its anadromous life cycle dictates periods of growth in both fresh and seawater. The transition of fish between these two habitats is often accompanied by high levels of mortality. Communities of commensal microbes inhabiting mucosal surfaces are vital in fish health and are also subjected to an abrupt change in salinity and often temperature during seawater transfer of Atlantic salmon. In this study we followed a cohort of Atlantic salmon through parr-smolt transformation in an open freshwater loch exposed to a natural decline in water temperature and during the first month post-transfer to sea. Mucus swabs were taken from gill and skin, and hindgut were collected from n = 6 fish from triplicate pens at four sampling points in freshwater (FW) and in the first- and fourth-weeks post transfer to sea (n = 18 total per sampling). Distinct temporal dynamics and communities were identified in the three mucosal surfaces. The hindgut microbiome diversity was stable and characterized by high inter-individual variability in terms of community composition. Microbiome diversity decreased in the skin throughout FW rearing and immediately post-transfer to sea but recovered to pre-transfer levels after one month at sea. Gill microbiome diversity also declined post-transfer but continued to decline further due to a single dominant taxon identified as Candidatus Clavichlamydia salmonicola, a member of the phylum Chlamydiae. Mucosal microbiome communities in all surfaces were largely distinct from the surrounding water. This study highlights the importance of considering the impact of time, in conjunction with water temperature and salinity, when determining microbiome composition in fish and urges caution when inferring general functionality of the microbiome from a single time point.