Marine-freshwater prokaryotic transitions require extensive changes in the predicted proteome

BACKGROUND: The adaptation of a marine prokaryote to live in freshwater environments or vice versa is generally believed to be an unusual and evolutionary demanding process. However, the reasons are not obvious given the similarity of both kinds of habitats. RESULTS: We have found major differences at the level of the predicted metaproteomes of marine and freshwater habitats with more acidic values of the isoelectric points (pI) in marine microbes. Furthermore, by comparing genomes of marine-freshwater phylogenetic relatives, we have found higher pI values (basic shift) in the freshwater ones. This difference was sharper in secreted > cytoplasmic > membrane proteins. The changes are concentrated on the surface of soluble proteins. It is also detectable at the level of total amino acid composition and involves similarly core and flexible genome- encoded proteins. CONCLUSIONS: The marked changes at the level of protein amino acid composition and pI provide a tool to predict the preferred habitat of a culture or a metagenome-assembled genome (MAG). The exact physiological explanation for such variations in the pIs and electrostatic surface potentials is not known yet. However, these changes might reflect differences in membrane bioenergetics derived from the absence of significant Na(+) concentrations in most freshwater habitats. In any case, the changes in amino acid composition in most proteins imply that a long evolutionary time is required to adapt from one type of habitat to the other. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-019-0731-5) contains supplementary material, which is available to authorized users.