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Evaporation-induced hydrodynamics promote conjugation-mediated plasmid transfer in microbial populations

Conjugative plasmids bestow important traits to microbial communities, such as virulence, antibiotic resistance, pollutant biotransformation, and biotechnology-relevant functions. While the biological mechanisms and determinants of plasmid conjugation are well established, the underlying physical an...

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Autores principales: Ruan, Chujin, Ramoneda, Josep, Chen, Guowei, Johnson, David R., Wang, Gang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9723580/
https://www.ncbi.nlm.nih.gov/pubmed/37938621
http://dx.doi.org/10.1038/s43705-021-00057-5
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author Ruan, Chujin
Ramoneda, Josep
Chen, Guowei
Johnson, David R.
Wang, Gang
author_facet Ruan, Chujin
Ramoneda, Josep
Chen, Guowei
Johnson, David R.
Wang, Gang
author_sort Ruan, Chujin
collection PubMed
description Conjugative plasmids bestow important traits to microbial communities, such as virulence, antibiotic resistance, pollutant biotransformation, and biotechnology-relevant functions. While the biological mechanisms and determinants of plasmid conjugation are well established, the underlying physical and ecological driving forces remain unclear. Microbial communities often inhabit unsaturated environments, such as soils and host surfaces (e.g., skin, teeth, leaves, roots), where water evaporation and associated small-scale hydrodynamic processes frequently occur at numerous air-water and solid-water interfaces. Here, we hypothesized that evaporation can induce water flows with profound effects on the spatial distribution and surface deposition of cells, and consequently on the extent of plasmid conjugation. Using droplet experiments with an antibiotic resistance-encoding plasmid, we show that evaporation-induced water flows reduce cell-cell distances and significantly increase the extent of plasmid conjugation. Counterintuitively, we found that evaporation results in lower expression levels of conjugation-related genes. This negative relationship between the extent of plasmid conjugation and the expression of conjugation-related genes could be attributed to increased conjugation efficiency during evaporation. This study provides new insights into the physical and ecological determinants of plasmid conjugation, with important implications for understanding the spread and proliferation of plasmid-encoded traits.
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spelling pubmed-97235802023-01-04 Evaporation-induced hydrodynamics promote conjugation-mediated plasmid transfer in microbial populations Ruan, Chujin Ramoneda, Josep Chen, Guowei Johnson, David R. Wang, Gang ISME Commun Brief Communication Conjugative plasmids bestow important traits to microbial communities, such as virulence, antibiotic resistance, pollutant biotransformation, and biotechnology-relevant functions. While the biological mechanisms and determinants of plasmid conjugation are well established, the underlying physical and ecological driving forces remain unclear. Microbial communities often inhabit unsaturated environments, such as soils and host surfaces (e.g., skin, teeth, leaves, roots), where water evaporation and associated small-scale hydrodynamic processes frequently occur at numerous air-water and solid-water interfaces. Here, we hypothesized that evaporation can induce water flows with profound effects on the spatial distribution and surface deposition of cells, and consequently on the extent of plasmid conjugation. Using droplet experiments with an antibiotic resistance-encoding plasmid, we show that evaporation-induced water flows reduce cell-cell distances and significantly increase the extent of plasmid conjugation. Counterintuitively, we found that evaporation results in lower expression levels of conjugation-related genes. This negative relationship between the extent of plasmid conjugation and the expression of conjugation-related genes could be attributed to increased conjugation efficiency during evaporation. This study provides new insights into the physical and ecological determinants of plasmid conjugation, with important implications for understanding the spread and proliferation of plasmid-encoded traits. Nature Publishing Group UK 2021-10-11 /pmc/articles/PMC9723580/ /pubmed/37938621 http://dx.doi.org/10.1038/s43705-021-00057-5 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Brief Communication
Ruan, Chujin
Ramoneda, Josep
Chen, Guowei
Johnson, David R.
Wang, Gang
Evaporation-induced hydrodynamics promote conjugation-mediated plasmid transfer in microbial populations
title Evaporation-induced hydrodynamics promote conjugation-mediated plasmid transfer in microbial populations
title_full Evaporation-induced hydrodynamics promote conjugation-mediated plasmid transfer in microbial populations
title_fullStr Evaporation-induced hydrodynamics promote conjugation-mediated plasmid transfer in microbial populations
title_full_unstemmed Evaporation-induced hydrodynamics promote conjugation-mediated plasmid transfer in microbial populations
title_short Evaporation-induced hydrodynamics promote conjugation-mediated plasmid transfer in microbial populations
title_sort evaporation-induced hydrodynamics promote conjugation-mediated plasmid transfer in microbial populations
topic Brief Communication
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9723580/
https://www.ncbi.nlm.nih.gov/pubmed/37938621
http://dx.doi.org/10.1038/s43705-021-00057-5
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