The biogeography of the atlantic salmon (Salmo salar) gut microbiome

Abstract

Although understood in many vertebrate systems, the natural diversity of host-associated microbiota has been little studied in teleosts. For migratory fishes, successful exploitation of multiple habitats may affect and be affected by the composition of the intestinal microbiome. We collected 96 Salmo salar from across the Atlantic encompassing both freshwater and marine phases. Dramatic differences between environmental and gut bacterial communities were observed. Furthermore, community composition was not significantly impacted by geography. Instead life-cycle stage strongly defined both the diversity and identity of microbial assemblages in the gut, with evidence for community destabilisation in migratory phases. Mycoplasmataceae phylotypes were abundantly recovered in all life-cycle stages. Patterns of Mycoplasmataceae phylotype recruitment to the intestinal microbial community among sites and life-cycle stages support a dual role for deterministic and stochastic processes in defining the composition of the S. salar gut microbiome.

Figure 1

Alpha and beta diversity comparisons of Atlantic Salmon intestinal microbiota. (a) Box plot showing alpha diversity (Chao1 richness estimator) variation across sites and life-cycle stages: blue bars—Burrishoole, Ireland; pale blue bars—Erriff, Ireland; red bars—St Jean, Canada; pink bars—Trinite, Canada. Marine adults from West Greenland are represented in green. (b) Mean beta diversity distances (unweighted unifrac) among individuals grouped by site and life-cycle stage. Error bars represent s.e.m. (c) Principal coordinate analysis of pairwise unweighted unifrac distances between all salmon and environmental samples. Axes represent the two synthetic variables explaining the greatest proportion of variation in the data set.

Figure 2

Taxonomic composition of the Atlantic Salmon intestinal microbiome. (a) Phlyum-level composition of total OTU abundances among distinct life-cycle stages and environmental samples. (b) Core (present in ⩾85% of individuals) 97% identity OTUs assigned to genus level from each life-cycle stage are represented by red-outlined ellipses. Black-outlined ellipses denote the presence of these ‘core' OTUs among other life-cycle stages. Ellipse area is proportional to the mean abundance of OTUs assigned to each genus over all samples from each life-cycle stage. Core genera that occur at a mean frequency >1000 in each sample time are bold (adults), underlined (parr) or italicised (freshwater). (c) Heatmap displaying the frequency distribution of OTUs belonging to family Mycoplasmataceae across distinct life-cycle stages and countries of origin. Genera within the Mycoplasmataceae are indicated on the maximum likelihood phylogeny (left) on which values indicated the percentage of bootstrap support for the respective clades. Single asterisk indicates the Candidatus OTU also recovered from a sympatric environmental sample. Double asterisk indicates the most abundant core Mycoplasma OTU recovered from adult life-cycle stages.