Co-diversification of an intestinal Mycoplasma and its salmonid host

Abstract

Understanding the evolutionary relationships between a host and its intestinal resident bacteria can transform how we understand adaptive phenotypic traits. The interplay between hosts and their resident bacteria inevitably affects the intestinal environment and, thereby, the living conditions of both the host and the microbiota. Thereby this co-existence likely influences the fitness of both bacteria and host. Whether this co-existence leads to evolutionary co-diversification in animals is largely unexplored, mainly due to the complexity of the environment and microbial communities and the often low host selection. We present the gut metagenome from wild Atlantic salmon (Salmo salar), a new wild organism model with an intestinal microbiota of low complexity and a well-described population structure, making it well-suited for investigating co-evolution. Our data reveal a strong host selection of a core gut microbiota dominated by a single Mycoplasma species. We found a clear co-diversification between the population structure of Atlantic salmon and nucleotide variability of the intestinal Mycoplasma populations conforming to expectations from co-evolution between host and resident bacteria. Our results show that the stable microbiota of Atlantic salmon has evolved with its salmonid host populations while potentially providing adaptive traits to the salmon host populations, including defence mechanisms, biosynthesis of essential amino acids, and metabolism of B vitamins. We highlight Atlantic salmon as a novel model for studying co-evolution between vertebrate hosts and their resident bacteria.

The Salmon Microbial Genome Atlas enables novel insights into bacteria-host interactions via functional mapping

“…Most of the genomes encoded CAZymes, with an average number of 115 genes per genome. MAGs with the smallest number of CAZymes were affiliated with the order Mycoplasmatales (average number of CAZyme = 7, Supplementary Table S4 ), which is in line with previous studies 8,9 , and imply their limited contribution to metabolism of dietary components in salmon. The dominant CAZy family within the SMGA was GH13, which has been proven to have the capacity to metabolize starch 35 .…”

“…We additionally assembled two MAGs from previously published metagenomes obtained from gut samples of salmons also farmed in Norway 24 . Finally, we included 10 previously published medium to high-quality MAGs, which had been derived from gut samples of wild salmons caught along the coast of northern Norway 9 . Taken together, the SMGA thereby feature a collection of 80 MAGs, including 31 of high-quality (>90% completeness, <5% contamination) according to the standards described in the “Minimum Information about a Metagenome-Assembled Genome” (MIMAG) 23 .…”

“…10 MAGs were obtained from a previous study of gut microbes from wild-salmon populations 9 . A total of 70 MAGs from gut samples of farmed salmon were assembled in this study, including 2 MAGs from re-assembling previously published metagenomes 24 and 68 MAGs from sequencing data generated in this study in 1) one sequencing run at NMBU and 2) three sequencing runs at SLU and SciLifeLab (Uppsala, Sweden).…”

Active colonisers of the gastrointestinal tract of Atlantic salmon farmed in a warm water region

“…Our focus on the V1-V3 region of 16S rRNA genes supported by addition of gene variants from isolate genome sequences helped to improve pinpointing colonising taxa and de ning their diversity. This approach was successful for Aliivibrio but much more work is needed to examine other possible colonists , besides Mycoplasma [25]. Full length 16S rRNA gene sequences is required for such analysis, in particular for A. si ae, A.logei, A. salmonicida and related species with placeholder designations [34].…”

“…Bacteria in the gut that are autochthonous would typically be highly predominant, associated with the mucosal layer and/or the digesta to different degrees. A major autochthonous species present in wild Atlantic salmon is "Candidatus Mycoplasma salmoninae salar" [25]. In sea farmed salmon this species and other members of the Mycoplasmatales can be readily detected [16,20,21,23,24].…”