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Free-living psychrophilic bacteria of the genus Psychrobacter are descendants of pathobionts

Daphne K. Welter, Albane Ruaud, Zachariah M. Henseler, Hannah N. De Jong, Peter van Coeverden de Groot, Johan Michaux, Linda Gormezano, Jillian L. Waters, View ORCID ProfileNicholas D. Youngblut, View ORCID ProfileRuth E. Ley
doi: https://doi.org/10.1101/2020.10.23.352302
Daphne K. Welter
1Department of Microbiome Science, Max Planck Institute for Developmental Biology, Tübingen, Germany
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Albane Ruaud
1Department of Microbiome Science, Max Planck Institute for Developmental Biology, Tübingen, Germany
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Zachariah M. Henseler
1Department of Microbiome Science, Max Planck Institute for Developmental Biology, Tübingen, Germany
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Hannah N. De Jong
1Department of Microbiome Science, Max Planck Institute for Developmental Biology, Tübingen, Germany
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Peter van Coeverden de Groot
2Department of Biology, Queen’s University, Kingston, Ontario, Canada
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Johan Michaux
3Conservation Genetics Laboratory, University of Liège, Liège, Belgium
4Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), UMR ASTRE, Montpellier, France
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Linda Gormezano
5Department of Vertebrate Zoology, American Museum of Natural History, New York, NY, USA
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Jillian L. Waters
1Department of Microbiome Science, Max Planck Institute for Developmental Biology, Tübingen, Germany
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Nicholas D. Youngblut
1Department of Microbiome Science, Max Planck Institute for Developmental Biology, Tübingen, Germany
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  • ORCID record for Nicholas D. Youngblut
Ruth E. Ley
1Department of Microbiome Science, Max Planck Institute for Developmental Biology, Tübingen, Germany
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  • ORCID record for Ruth E. Ley
  • For correspondence: rley@tuebingen.mpg.de
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Abstract

Host-adapted microbiota are generally thought to have evolved from free-living ancestors. This process is in principle reversible, but examples are few. The genus Psychrobacter (family Moraxellaceae, phylum Gamma-Proteobacteria) includes species inhabiting diverse and mostly polar environments, such as sea ice and marine animals. To probe Psychrobacter’s evolutionary history, we analyzed 85 Psychrobacter strains by comparative genomics and phenotyping under 24 different growth conditions. Genome-based phylogeny shows Psychrobacter are derived from Moraxella, which are warm-adapted pathobionts. Psychrobacter strains form two ecotypes based on growth temperature: flexible (FE, growth at 4 - 37°C), and restricted (RE, 4 - 25°C). FE strains, which can be either phylogenetically basal or derived, have smaller genomes and higher transposon copy numbers. RE strains have larger genomes, and show genomic adaptations towards a psychrophilic lifestyle and are phylogenetically derived only. We then assessed Psychrobacter abundance in 86 mostly wild polar bear stools and tested persistence of select strains in germfree mice. Psychrobacter (both FE and RE) was enriched in stool of polar bears feeding on mammals, but only FE strains persisted in germfree mice. Together these results indicate growth at 37°C is ancestral in Psychrobacter, lost in many derived species, and likely necessary to colonize the mammalian gut.

Competing Interest Statement

The authors have declared no competing interest.

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Posted October 25, 2020.
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Free-living psychrophilic bacteria of the genus Psychrobacter are descendants of pathobionts
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
bioRxiv 2020.10.23.352302; doi: https://doi.org/10.1101/2020.10.23.352302
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Free-living psychrophilic bacteria of the genus Psychrobacter are descendants of pathobionts
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
bioRxiv 2020.10.23.352302; doi: https://doi.org/10.1101/2020.10.23.352302

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