Free-Living, Psychrotrophic Bacteria of the Genus Psychrobacter Are Descendants of Pathobionts

Abstract

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. IMPORTANCE Host-associated microbes are generally assumed to have evolved from free-living ones. The evolutionary transition of microbes in the opposite direction, from host associated toward free living, has been predicted based on phylogenetic data but not studied in depth. Here, we provide evidence that the genus Psychrobacter, particularly well known for inhabiting low-temperature, high-salt environments such as sea ice, permafrost soils, and frozen foodstuffs, has evolved from a mammalian-associated ancestor. We show that some Psychrobacter strains retain seemingly ancestral genomic and phenotypic traits that correspond with host association while others have diverged to psychrotrophic or psychrophilic lifestyles.

Longitudinal, Multi-Platform Metagenomics Yields a High-Quality Genomic Catalog and Guides an In Vitro Model for Cheese Communities

“…5B ). This question was of particular interest because Psychrobacter species are found in a variety of environments, both free-living and host-associated, and they show habitat-dependent adaptations ( 34 ). We identified an enrichment of iron acquisition genes and type VI secretion genes in cheese-associated Psychrobacter .…”

Current levels of microplastic pollution impact wild seabird gut microbiomes

“…Notably, as microplastic count increased, the abundance of resident microbiota associated with healthy hosts decreased, while the abundance of microbes known to be involved in disease, antibiotic resistance and plastic degradation and those considered to be zoonotic pathogens increased. For example, Pseudoalteromonas, which comprises marine bacteria usually associated with healthy organisms 26 , was negatively associated with microplastic count, as were known members of (sea)bird microbiota, such as Psychrobacter 26,27 , Enterococcus 28,29 , Catellicoccus 30,31 and Staphylococcus 32,33 . In contrast, Corynebacterium xerosis was positively associated with microplastic count and has been identified as an emerging pathogen with potential to become zoonotic 34,35 , with its genus having shown plastic-degrading capabilities (database in ref.…”

Comparative Study of Microbial Diversity in Different Coastal Aquifers: Determining Factors

“…Both in the genus Planococcus and in Bacillus, numerous species tolerant to these higher salinity conditions have been described in the literature [100,101]. Psychrobacter also shares similar characteristics with respect to saline environments [102], so its presence in the samples from these aquifers seems to point to salinity as one of the factors responsible for the structure of its microbial community.…”