Free-living, psychrotrophic bacteria of the genus Psychrobacter are descendents of pathobionts

Host-adapted microorganisms are generally assumed to have evolved
from free-living, environmental microorganisms, as examples of the reverse process
are rare. In the phylum Gammaproteobacteria, family Moraxellaceae, the genus
Psychrobacter includes strains from a broad ecological distribution including animal
bodies as well as sea ice and other nonhost environments. To elucidate the relationship
between these ecological niches and Psychrobacter’s evolutionary history, we
performed tandem genomic analyses with phenotyping of 85 Psychrobacter accessions.
Phylogenomic analysis of the family Moraxellaceae reveals that basal members of
the Psychrobacter clade are Moraxella spp., a group of often-pathogenic organisms.
Psychrobacter exhibited two broad growth patterns in our phenotypic screen: one group
that we called the “flexible ecotype” (FE) had the ability to grow between 4 and 37°C,
and the other, which we called the “restricted ecotype” (RE), could grow between 4 and
25°C. The FE group includes phylogenetically basal strains, and FE strains exhibit
increased transposon copy numbers, smaller genomes, and a higher likelihood to be
bile salt resistant. The RE group contains only phylogenetically derived strains and has
increased proportions of lipid metabolism and biofilm formation genes, functions that
are adaptive to cold stress. In a 16S rRNA gene survey of polar bear fecal samples, we
detect both FE and RE strains, but in in vivo colonizations of gnotobiotic mice, only FE
strains persist. Our results indicate the ability to grow at 37°C, seemingly necessary for
mammalian gut colonization, is an ancestral trait for Psychrobacter, which likely evolved
from a pathobiont.