Free-Living, Psychrotrophic Bacteria of the Genus <italic toggle="yes">Psychrobacter</italic> 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 distributi...

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Autores principales:	Daphne K. Welter, Albane Ruaud, Zachariah M. Henseler, Hannah N. De Jong, Peter van Coeverden de Groot, Johan Michaux, Linda Gormezano, Jillian L. Waters, Nicholas D. Youngblut, Ruth E. Ley
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	genomics phylogeny Psychrobacter psychrophiles Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c660ed721be045e1b67e170775ee9bd6
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spelling	oai:doaj.org-article:c660ed721be045e1b67e170775ee9bd62021-12-02T19:22:27ZFree-Living, Psychrotrophic Bacteria of the Genus <italic toggle="yes">Psychrobacter</italic> Are Descendants of Pathobionts10.1128/mSystems.00258-212379-5077https://doaj.org/article/c660ed721be045e1b67e170775ee9bd62021-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00258-21https://doaj.org/toc/2379-5077ABSTRACT 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.Daphne K. WelterAlbane RuaudZachariah M. HenselerHannah N. De JongPeter van Coeverden de GrootJohan MichauxLinda GormezanoJillian L. WatersNicholas D. YoungblutRuth E. LeyAmerican Society for MicrobiologyarticlegenomicsphylogenyPsychrobacterpsychrophilesMicrobiologyQR1-502ENmSystems, Vol 6, Iss 2 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	genomics phylogeny Psychrobacter psychrophiles Microbiology QR1-502
spellingShingle	genomics phylogeny Psychrobacter psychrophiles Microbiology QR1-502 Daphne K. Welter Albane Ruaud Zachariah M. Henseler Hannah N. De Jong Peter van Coeverden de Groot Johan Michaux Linda Gormezano Jillian L. Waters Nicholas D. Youngblut Ruth E. Ley Free-Living, Psychrotrophic Bacteria of the Genus <italic toggle="yes">Psychrobacter</italic> Are Descendants of Pathobionts
description	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.
format	article
author	Daphne K. Welter Albane Ruaud Zachariah M. Henseler Hannah N. De Jong Peter van Coeverden de Groot Johan Michaux Linda Gormezano Jillian L. Waters Nicholas D. Youngblut Ruth E. Ley
author_facet	Daphne K. Welter Albane Ruaud Zachariah M. Henseler Hannah N. De Jong Peter van Coeverden de Groot Johan Michaux Linda Gormezano Jillian L. Waters Nicholas D. Youngblut Ruth E. Ley
author_sort	Daphne K. Welter
title	Free-Living, Psychrotrophic Bacteria of the Genus <italic toggle="yes">Psychrobacter</italic> Are Descendants of Pathobionts
title_short	Free-Living, Psychrotrophic Bacteria of the Genus <italic toggle="yes">Psychrobacter</italic> Are Descendants of Pathobionts
title_full	Free-Living, Psychrotrophic Bacteria of the Genus <italic toggle="yes">Psychrobacter</italic> Are Descendants of Pathobionts
title_fullStr	Free-Living, Psychrotrophic Bacteria of the Genus <italic toggle="yes">Psychrobacter</italic> Are Descendants of Pathobionts
title_full_unstemmed	Free-Living, Psychrotrophic Bacteria of the Genus <italic toggle="yes">Psychrobacter</italic> Are Descendants of Pathobionts
title_sort	free-living, psychrotrophic bacteria of the genus <italic toggle="yes">psychrobacter</italic> are descendants of pathobionts
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/c660ed721be045e1b67e170775ee9bd6
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Free-Living, Psychrotrophic Bacteria of the Genus <italic toggle="yes">Psychrobacter</italic> Are Descendants of Pathobionts

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