Repeated evolutionary transitions of flavobacteria from marine to non‐marine habitats

Summary The taxonomy of marine and non‐marine organisms rarely overlap, but the mechanisms underlying this distinction are often unknown. Here, we predicted three major ocean‐to‐land transitions in the evolutionary history of Flavobacteriaceae , a family known for polysaccharide and peptide degradation. These unidirectional transitions were associated with repeated losses of marine signature genes and repeated gains of non‐marine adaptive genes. This included various Na + ‐dependent transporters, osmolyte transporters and glycoside hydrolases (GH) for sulfated polysaccharide utilization in marine descendants, and in non‐marine descendants genes for utilizing the land plant material pectin and genes facilitating terrestrial host interactions. The K + scavenging ATPase was repeatedly gained whereas the corresponding low‐affinity transporter repeatedly lost upon transitions, reflecting K + ions are less available to non‐marine bacteria. Strikingly, the central metabolism Na + ‐translocating NADH: quinone dehydrogenase gene was repeatedly gained in marine descendants, whereas the H + ‐translocating counterpart was repeatedly gained in non‐marine lineages. Furthermore, GH genes were depleted in isolates colonizing animal hosts but abundant in bacteria inhabiting other non‐marine niches; thus relative abundances of GH versus peptidase genes among Flavobacteriaceae lineages were inconsistent with the marine versus non‐marine dichotomy. We suggest that phylogenomic analyses can cast novel light on mechanisms explaining the distribution and ecology of key microbiome components.