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The genetic and ecological landscape of plasmids in the human gut

View ORCID ProfileMichael K. Yu, View ORCID ProfileEmily C. Fogarty, View ORCID ProfileA. Murat Eren
doi: https://doi.org/10.1101/2020.11.01.361691
Michael K. Yu
1Toyota Technological Institute at Chicago; Chicago, IL 60637, USA
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  • For correspondence: mikeyu@ttic.edu meren@uchicago.edu
Emily C. Fogarty
2Department of Medicine, University of Chicago; Chicago, IL 60637, USA
3Graduate Program in the Biological Sciences, University of Chicago; Chicago, IL 60637, USA
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A. Murat Eren
2Department of Medicine, University of Chicago; Chicago, IL 60637, USA
3Graduate Program in the Biological Sciences, University of Chicago; Chicago, IL 60637, USA
4Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory; Woods Hole, MA 02543, USA
5Helmholtz Institute for Functional Marine Biodiversity, Ammerländer Heerstraße 231, 26129 Oldenburg, Germany
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  • For correspondence: mikeyu@ttic.edu meren@uchicago.edu
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Abstract

Plasmids are mobile genetic elements found across all domains of life. As plasmids often encode determinants of fitness, their evolution is intertwined with their hosts. However, naturally occurring plasmids remain far less understood than their hosts due to the lack of frameworks to recognize plasmids and to classify them into evolutionary groups. Here we trained a machine learning model that recognizes plasmids based on genetic architecture with state-of-the-art accuracy. We applied this model to a global collection of human gut metagenomes to identify 68,350 unique plasmids, 13,280 of which had a very high model confidence and represent more than an order of magnitude increase over the number of known plasmids that we detected in this environment. To understand the evolution of these plasmids, we developed a generalizable approach that enabled us to define 1,169 ‘plasmid systems’. Each system consists of plasmids that share a backbone sequence containing core plasmid functions, such as replication and conjugation, but vary in cargo genes that are often critical to the host, such as antibiotic resistance, amino acid biosynthesis, and tRNA modification. Members of the same system are often found in geographically distinct human populations, revealing cargo genes that likely respond to environmental selection. The ecological patterns of plasmids we observed could not be explained by microbial taxonomy. This work uncovers the tremendous diversity of plasmids and demonstrates the need to characterize them as a separate component of microbiomes distinct from their hosts.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Updated several sections for clarity and to add new results; Updated Figure 1; Updated Supplementary Figure S2; Added Supplementary Figures S12-S15; Updated Supplementary Tables S3 and S4; Added Supplementary Tables S9-S12

  • https://github.com/michaelkyu/plasx

  • https://github.com/michaelkyu/mobmess

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-NC-ND 4.0 International license.
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Posted December 18, 2022.
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The genetic and ecological landscape of plasmids in the human gut
Michael K. Yu, Emily C. Fogarty, A. Murat Eren
bioRxiv 2020.11.01.361691; doi: https://doi.org/10.1101/2020.11.01.361691
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The genetic and ecological landscape of plasmids in the human gut
Michael K. Yu, Emily C. Fogarty, A. Murat Eren
bioRxiv 2020.11.01.361691; doi: https://doi.org/10.1101/2020.11.01.361691

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