Abstract

BackgroundThe 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.ResultsWe 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.ConclusionsThe 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.

Highlights

  • 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

  • We used examples of bona fide freshwater, brackish, and marine microbes, some of them retrieved as metagenome-assembled genome (MAG) (> 70% of completeness) from the environments compared in Fig. 1, and others as pure cultures

  • There is a large change in amino acid composition among microbes depending on whether they live in marine or freshwater habitats

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Summary

Introduction

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. One classic conundrum of microbiology, or of biology at large, is the marked borderline that exists between freshwater and marine habitats [1]. The phylum Actinobacteria and the class Betaproteobacteria are two notorious examples of taxa that are more abundant in freshwater [2,3,4], while classes Alphaproteobacteria and Gammaproteobacteria are Cabello-Yeves and Rodriguez-Valera Microbiome (2019) 7:117 multiple marine clades being detected, albeit in small numbers, in freshwater habitats [14,15,16], and the opposite is true for marine regions neighboring the continents, near large estuaries like the Amazon on the Atlantic coast of Brazil [17] or the Baltic Sea [18, 19]. Still, excluding some microbes that can survive and remain rare, such as Escherichia coli or Vibrio cholerae, there is no known example of microbes of the same species (with > 95% average nucleotide identity, ANI) being found in both types of aquatic environments

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