Seasonal Cycling of Atlantic Salmon Gill Microbiomes Disrupted by Ca. Branchiomonas sp. Associated Evenness Collapses

Increasing prevalence of multifactorial gill disease in salmonid aquaculture has resulted in a need to better understand gill associated microbiomes of farmed Atlantic Salmon. The dynamics of these communities remain poorly understood. Here we report the findings of a study tracking gill communities from stocking in seawater to harvest, in 613 salmon, across four Scottish marine farms. We identify seawater farm site alongside a lasting influence of hatchery system type (Recirculating aquaculture system (RAS) or Loch-based systems) through to harvest on the gill microbiome of marine stage salmon (PERMANOVA, R2 = 0.029, p<0.001). We observe robust seasonal cyclicity in gill microbiomes (PERMANOVA, R2 = 0.204 - 0.406, p<0.001) as well as a collapse in community evenness at all sites (ANOVA, p<0.001). This collapse was driven by the dominance (>90% relative abundance) of Candidatus Branchiomonas sp., observed consistently at all farms, independent of disease occurrence or on-site activities such as disease treatments. A novel qPCR approach was designed to quantify the contribution of bacterial and host DNA in microbiome samples finding significant temporal variability in 16S rRNA gene abundances at two farms (ANOVA, p<0.001), 18S rRNA at three farms (ANOVA, p<0.001) and in their ratio to each other at all farms (ANOVA, p<0.01) which was seemingly unrelated to fish growth. Together these findings indicate that gill microbiome dynamics are not random, and a better understanding may lead to improved mitigation of gill disease.