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Anatomy promotes neutral coexistence of strains in the human skin microbiome

View ORCID ProfileArolyn Conwill, Anne C. Kuan, Ravalika Damerla, Alexandra J. Poret, View ORCID ProfileJacob S. Baker, View ORCID ProfileA. Delphine Tripp, Eric J. Alm, View ORCID ProfileTami D. Lieberman
doi: https://doi.org/10.1101/2021.05.12.443817
Arolyn Conwill
1Institute for Medical Engineering and Sciences, Massachusetts Institute of Technology, Cambridge MA, USA
2Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge MA, USA
3Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge MA, USA
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  • ORCID record for Arolyn Conwill
Anne C. Kuan
3Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge MA, USA
4Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge MA, USA
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Ravalika Damerla
1Institute for Medical Engineering and Sciences, Massachusetts Institute of Technology, Cambridge MA, USA
2Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge MA, USA
3Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge MA, USA
4Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge MA, USA
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Alexandra J. Poret
1Institute for Medical Engineering and Sciences, Massachusetts Institute of Technology, Cambridge MA, USA
2Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge MA, USA
3Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge MA, USA
4Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge MA, USA
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Jacob S. Baker
1Institute for Medical Engineering and Sciences, Massachusetts Institute of Technology, Cambridge MA, USA
2Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge MA, USA
3Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge MA, USA
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A. Delphine Tripp
1Institute for Medical Engineering and Sciences, Massachusetts Institute of Technology, Cambridge MA, USA
2Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge MA, USA
3Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge MA, USA
5Department of Systems Biology, Harvard University, Cambridge, MA 02138
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  • ORCID record for A. Delphine Tripp
Eric J. Alm
3Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge MA, USA
4Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge MA, USA
6Broad Institute of MIT and Harvard, Cambridge MA, 02139
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Tami D. Lieberman
1Institute for Medical Engineering and Sciences, Massachusetts Institute of Technology, Cambridge MA, USA
2Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge MA, USA
3Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge MA, USA
6Broad Institute of MIT and Harvard, Cambridge MA, 02139
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  • ORCID record for Tami D. Lieberman
  • For correspondence: tami@mit.edu
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Abstract

What enables strains of the same species to coexist in a microbiome? Here, we investigate if host anatomy can explain strain co-residence of Cutibacterium acnes, the most abundant species on human skin. We reconstruct on-person evolution and migration using 947 C. acnes colony genomes acquired from 16 subjects, including from individual skin pores, and find that pores maintain diversity by limiting competition. Although strains with substantial fitness differences coexist within centimeter-scale regions, each pore is dominated by a single strain. Moreover, colonies from a pore typically have identical genomes. An absence of adaptive signatures suggests a genotype-independent source of low within-pore diversity. We therefore propose that pore anatomy imposes random single-cell bottlenecks during migration into pores and subsequently blocks new migrants; the resulting population fragmentation reduces competition and promotes coexistence. Our findings imply that therapeutic interventions involving pore-dwelling species should focus on removing resident populations over optimizing probiotic fitness.

Competing Interest Statement

The authors have declared no competing interest.

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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-NC-ND 4.0 International license.
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Posted May 14, 2021.
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Anatomy promotes neutral coexistence of strains in the human skin microbiome
Arolyn Conwill, Anne C. Kuan, Ravalika Damerla, Alexandra J. Poret, Jacob S. Baker, A. Delphine Tripp, Eric J. Alm, Tami D. Lieberman
bioRxiv 2021.05.12.443817; doi: https://doi.org/10.1101/2021.05.12.443817
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Anatomy promotes neutral coexistence of strains in the human skin microbiome
Arolyn Conwill, Anne C. Kuan, Ravalika Damerla, Alexandra J. Poret, Jacob S. Baker, A. Delphine Tripp, Eric J. Alm, Tami D. Lieberman
bioRxiv 2021.05.12.443817; doi: https://doi.org/10.1101/2021.05.12.443817

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