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

Author:

Martínez Arbas SusanaORCID,Narayanasamy ShamanORCID,Herold Malte,Lebrun Laura A.,Hoopmann Michael R.ORCID,Li SujunORCID,Lam Tony J.,Kunath Benoît J.ORCID,Hicks Nathan D.,Liu Cindy M.ORCID,Price Lance B.,Laczny Cedric C.ORCID,Gillece John D.,Schupp James M.,Keim Paul S.ORCID,Moritz Robert L.ORCID,Faust KarolineORCID,Tang Haixu,Ye Yuzhen,Skupin AlexanderORCID,May PatrickORCID,Muller Emilie E. L.ORCID,Wilmes PaulORCID

Abstract

AbstractViruses 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.

Funder

Fonds National de la Recherche Luxembourg

European Union Joint Programming in Neurodegenerative Diseases grant (INTER/JPND/12/01) Union ERASysAPP grant

Publisher

Springer Science and Business Media LLC

Subject

Cell Biology,Microbiology (medical),Genetics,Applied Microbiology and Biotechnology,Immunology,Microbiology

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