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Roles of bacteriophages, plasmids and CRISPR immunity in microbial community dynamics revealed using time-series integrated meta-omics

Viruses and plasmids (invasive mobile genetic elements (iMGEs)) have important roles in shaping microbial communities, but their dynamic interactions with CRISPR-based immunity remain unresolved. We analysed generation-resolved iMGE–host dynamics spanning one and a half years in a microbial consorti...

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Autores principales: Martínez Arbas, Susana, Narayanasamy, Shaman, Herold, Malte, Lebrun, Laura A., Hoopmann, Michael R., Li, Sujun, Lam, Tony J., Kunath, Benoît J., Hicks, Nathan D., Liu, Cindy M., Price, Lance B., Laczny, Cedric C., Gillece, John D., Schupp, James M., Keim, Paul S., Moritz, Robert L., Faust, Karoline, Tang, Haixu, Ye, Yuzhen, Skupin, Alexander, May, Patrick, Muller, Emilie E. L., Wilmes, Paul
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7752763/
https://www.ncbi.nlm.nih.gov/pubmed/33139880
http://dx.doi.org/10.1038/s41564-020-00794-8
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author Martínez Arbas, Susana
Narayanasamy, Shaman
Herold, Malte
Lebrun, Laura A.
Hoopmann, Michael R.
Li, Sujun
Lam, Tony J.
Kunath, Benoît J.
Hicks, Nathan D.
Liu, Cindy M.
Price, Lance B.
Laczny, Cedric C.
Gillece, John D.
Schupp, James M.
Keim, Paul S.
Moritz, Robert L.
Faust, Karoline
Tang, Haixu
Ye, Yuzhen
Skupin, Alexander
May, Patrick
Muller, Emilie E. L.
Wilmes, Paul
author_facet Martínez Arbas, Susana
Narayanasamy, Shaman
Herold, Malte
Lebrun, Laura A.
Hoopmann, Michael R.
Li, Sujun
Lam, Tony J.
Kunath, Benoît J.
Hicks, Nathan D.
Liu, Cindy M.
Price, Lance B.
Laczny, Cedric C.
Gillece, John D.
Schupp, James M.
Keim, Paul S.
Moritz, Robert L.
Faust, Karoline
Tang, Haixu
Ye, Yuzhen
Skupin, Alexander
May, Patrick
Muller, Emilie E. L.
Wilmes, Paul
author_sort Martínez Arbas, Susana
collection PubMed
description Viruses and plasmids (invasive mobile genetic elements (iMGEs)) have important roles in shaping microbial communities, but their dynamic interactions with CRISPR-based immunity remain unresolved. We analysed generation-resolved iMGE–host dynamics spanning one and a half years in a microbial consortium from a biological wastewater treatment plant using integrated meta-omics. We identified 31 bacterial metagenome-assembled genomes encoding complete CRISPR–Cas systems and their corresponding iMGEs. CRISPR-targeted plasmids outnumbered their bacteriophage counterparts by at least fivefold, highlighting the importance of CRISPR-mediated defence against plasmids. Linear modelling of our time-series data revealed that the variation in plasmid abundance over time explained more of the observed community dynamics than phages. Community-scale CRISPR-based plasmid–host and phage–host interaction networks revealed an increase in CRISPR-mediated interactions coinciding with a decrease in the dominant ‘Candidatus Microthrix parvicella’ population. Protospacers were enriched in sequences targeting genes involved in the transmission of iMGEs. Understanding the factors shaping the fitness of specific populations is necessary to devise control strategies for undesirable species and to predict or explain community-wide phenotypes.
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spelling pubmed-77527632020-12-29 Roles of bacteriophages, plasmids and CRISPR immunity in microbial community dynamics revealed using time-series integrated meta-omics Martínez Arbas, Susana Narayanasamy, Shaman Herold, Malte Lebrun, Laura A. Hoopmann, Michael R. Li, Sujun Lam, Tony J. Kunath, Benoît J. Hicks, Nathan D. Liu, Cindy M. Price, Lance B. Laczny, Cedric C. Gillece, John D. Schupp, James M. Keim, Paul S. Moritz, Robert L. Faust, Karoline Tang, Haixu Ye, Yuzhen Skupin, Alexander May, Patrick Muller, Emilie E. L. Wilmes, Paul Nat Microbiol Article Viruses and plasmids (invasive mobile genetic elements (iMGEs)) have important roles in shaping microbial communities, but their dynamic interactions with CRISPR-based immunity remain unresolved. We analysed generation-resolved iMGE–host dynamics spanning one and a half years in a microbial consortium from a biological wastewater treatment plant using integrated meta-omics. We identified 31 bacterial metagenome-assembled genomes encoding complete CRISPR–Cas systems and their corresponding iMGEs. CRISPR-targeted plasmids outnumbered their bacteriophage counterparts by at least fivefold, highlighting the importance of CRISPR-mediated defence against plasmids. Linear modelling of our time-series data revealed that the variation in plasmid abundance over time explained more of the observed community dynamics than phages. Community-scale CRISPR-based plasmid–host and phage–host interaction networks revealed an increase in CRISPR-mediated interactions coinciding with a decrease in the dominant ‘Candidatus Microthrix parvicella’ population. Protospacers were enriched in sequences targeting genes involved in the transmission of iMGEs. Understanding the factors shaping the fitness of specific populations is necessary to devise control strategies for undesirable species and to predict or explain community-wide phenotypes. Nature Publishing Group UK 2020-11-02 2021 /pmc/articles/PMC7752763/ /pubmed/33139880 http://dx.doi.org/10.1038/s41564-020-00794-8 Text en © The Author(s) 2020 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/.
spellingShingle Article
Martínez Arbas, Susana
Narayanasamy, Shaman
Herold, Malte
Lebrun, Laura A.
Hoopmann, Michael R.
Li, Sujun
Lam, Tony J.
Kunath, Benoît J.
Hicks, Nathan D.
Liu, Cindy M.
Price, Lance B.
Laczny, Cedric C.
Gillece, John D.
Schupp, James M.
Keim, Paul S.
Moritz, Robert L.
Faust, Karoline
Tang, Haixu
Ye, Yuzhen
Skupin, Alexander
May, Patrick
Muller, Emilie E. L.
Wilmes, Paul
Roles of bacteriophages, plasmids and CRISPR immunity in microbial community dynamics revealed using time-series integrated meta-omics
title Roles of bacteriophages, plasmids and CRISPR immunity in microbial community dynamics revealed using time-series integrated meta-omics
title_full Roles of bacteriophages, plasmids and CRISPR immunity in microbial community dynamics revealed using time-series integrated meta-omics
title_fullStr Roles of bacteriophages, plasmids and CRISPR immunity in microbial community dynamics revealed using time-series integrated meta-omics
title_full_unstemmed Roles of bacteriophages, plasmids and CRISPR immunity in microbial community dynamics revealed using time-series integrated meta-omics
title_short Roles of bacteriophages, plasmids and CRISPR immunity in microbial community dynamics revealed using time-series integrated meta-omics
title_sort roles of bacteriophages, plasmids and crispr immunity in microbial community dynamics revealed using time-series integrated meta-omics
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7752763/
https://www.ncbi.nlm.nih.gov/pubmed/33139880
http://dx.doi.org/10.1038/s41564-020-00794-8
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