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Cobamide sharing drives skin microbiome dynamics

View ORCID ProfileMary Hannah Swaney, Shelby Sandstrom, View ORCID ProfileLindsay R Kalan
doi: https://doi.org/10.1101/2020.12.02.407395
Mary Hannah Swaney
1Department of Medical Microbiology and Immunology, School of Medicine and Public Health, University of Wisconsin, Madison, WI, USA
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Shelby Sandstrom
1Department of Medical Microbiology and Immunology, School of Medicine and Public Health, University of Wisconsin, Madison, WI, USA
2Department of Bacteriology, College of Agricultural and Life Sciences, University of Wisconsin, Madison, WI, USA
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Lindsay R Kalan
1Department of Medical Microbiology and Immunology, School of Medicine and Public Health, University of Wisconsin, Madison, WI, USA
3Department of Medicine, School of Medicine and Public Health, University of Wisconsin, Madison, WI, USA
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  • For correspondence: lkalan@wisc.edu
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ABSTRACT

The human skin microbiome is a key player in human health, with diverse functions ranging from defense against pathogens to education of the immune system. While recent studies have begun to shed light on the valuable role that skin microorganisms have in maintaining a healthy skin barrier, a detailed understanding of the complex interactions that shape healthy skin microbial communities is limited. Cobamides, the vitamin B12 class of cofactor, are essential for organisms across the tree of life. Because this vitamin is only produced by a limited fraction of prokaryotes, cobamide sharing has been shown to mediate community dynamics within microbial communities. Here, we provide the first large-scale unbiased metagenomic assessment of cobamide biosynthesis and utilization in the skin microbiome. We show that while numerous and diverse taxa across the major bacterial phyla on the skin are cobamide dependent, relatively few species encode for de novo cobamide biosynthesis. We find that cobamide sharing shapes the network structure in microbial communities across the different microenvironments of the skin and that changes in community structure and microbiome diversity are driven by the abundance of cobamide producers in the Corynebacterium genus, in both healthy and disease skin states. Lastly, we find that de novo cobamide biosynthesis is enriched only in host-associated Corynebacterium species, including those prevalent on human skin. We confirm that the cofactor is produced in excess through quantification of cobamide production by skin-associated species isolated in the laboratory. Taken together, our results support a role for cobamide sharing within skin microbial communities, which we predict stabilizes the microbiome and mediates host interactions.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • New analysis exploring the biosynthesis and use of cobamides in skin metagenomes from three independent studies has been added. A new author has been added that contributed to the generation of metagenomics sequence data.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted November 10, 2021.
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Cobamide sharing drives skin microbiome dynamics
Mary Hannah Swaney, Shelby Sandstrom, Lindsay R Kalan
bioRxiv 2020.12.02.407395; doi: https://doi.org/10.1101/2020.12.02.407395
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Cobamide sharing drives skin microbiome dynamics
Mary Hannah Swaney, Shelby Sandstrom, Lindsay R Kalan
bioRxiv 2020.12.02.407395; doi: https://doi.org/10.1101/2020.12.02.407395

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