Phylogroup-specific variation shapes the clustering of antimicrobial resistance genes and defence systems across regions of genome plasticity in Pseudomonas aeruginosa.

Antibiotic resistance CRISPR-Cas systems Defence systems Pangenome Pseudomonas aeruginosa Regions of genome plasticity

Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Apr 2023
Historique:
received: 30 06 2022
revised: 02 03 2023
accepted: 07 03 2023
medline: 18 4 2023
pubmed: 24 3 2023
entrez: 23 3 2023
Statut: ppublish

Résumé

Pseudomonas aeruginosa is an opportunistic pathogen consisting of three phylogroups (hereafter named A, B, and C). Here, we assessed phylogroup-specific evolutionary dynamics across available and also new P. aeruginosa genomes. In this genomic analysis, we first generated new genome assemblies for 18 strains of the major P. aeruginosa clone type (mPact) panel, comprising a phylogenetically diverse collection of clinical and environmental isolates for this species. Thereafter, we combined these new genomes with 1991 publicly available P. aeruginosa genomes for a phylogenomic and comparative analysis. We specifically explored to what extent antimicrobial resistance (AMR) genes, defence systems, and virulence genes vary in their distribution across regions of genome plasticity (RGPs) and "masked" (RGP-free) genomes, and to what extent this variation differs among the phylogroups. We found that members of phylogroup B possess larger genomes, contribute a comparatively larger number of pangenome families, and show lower abundance of CRISPR-Cas systems. Furthermore, AMR and defence systems are pervasive in RGPs and integrative and conjugative/mobilizable elements (ICEs/IMEs) from phylogroups A and B, and the abundance of these cargo genes is often significantly correlated. Moreover, inter- and intra-phylogroup interactions occur at the accessory genome level, suggesting frequent recombination events. Finally, we provide here the mPact panel of diverse P. aeruginosa strains that may serve as a valuable reference for functional analyses. Altogether, our results highlight distinct pangenome characteristics of the P. aeruginosa phylogroups, which are possibly influenced by variation in the abundance of CRISPR-Cas systems and are shaped by the differential distribution of other defence systems and AMR genes. German Science Foundation, Max-Planck Society, Leibniz ScienceCampus Evolutionary Medicine of the Lung, BMBF program Medical Infection Genomics, Kiel Life Science Postdoc Award.

Sections du résumé

BACKGROUND BACKGROUND
Pseudomonas aeruginosa is an opportunistic pathogen consisting of three phylogroups (hereafter named A, B, and C). Here, we assessed phylogroup-specific evolutionary dynamics across available and also new P. aeruginosa genomes.
METHODS METHODS
In this genomic analysis, we first generated new genome assemblies for 18 strains of the major P. aeruginosa clone type (mPact) panel, comprising a phylogenetically diverse collection of clinical and environmental isolates for this species. Thereafter, we combined these new genomes with 1991 publicly available P. aeruginosa genomes for a phylogenomic and comparative analysis. We specifically explored to what extent antimicrobial resistance (AMR) genes, defence systems, and virulence genes vary in their distribution across regions of genome plasticity (RGPs) and "masked" (RGP-free) genomes, and to what extent this variation differs among the phylogroups.
FINDINGS RESULTS
We found that members of phylogroup B possess larger genomes, contribute a comparatively larger number of pangenome families, and show lower abundance of CRISPR-Cas systems. Furthermore, AMR and defence systems are pervasive in RGPs and integrative and conjugative/mobilizable elements (ICEs/IMEs) from phylogroups A and B, and the abundance of these cargo genes is often significantly correlated. Moreover, inter- and intra-phylogroup interactions occur at the accessory genome level, suggesting frequent recombination events. Finally, we provide here the mPact panel of diverse P. aeruginosa strains that may serve as a valuable reference for functional analyses.
INTERPRETATION CONCLUSIONS
Altogether, our results highlight distinct pangenome characteristics of the P. aeruginosa phylogroups, which are possibly influenced by variation in the abundance of CRISPR-Cas systems and are shaped by the differential distribution of other defence systems and AMR genes.
FUNDING BACKGROUND
German Science Foundation, Max-Planck Society, Leibniz ScienceCampus Evolutionary Medicine of the Lung, BMBF program Medical Infection Genomics, Kiel Life Science Postdoc Award.

Identifiants

pubmed: 36958270
pii: S2352-3964(23)00097-X
doi: 10.1016/j.ebiom.2023.104532
pmc: PMC10053402
pii:
doi:

Substances chimiques

Anti-Bacterial Agents 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104532

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests We declare no competing interests.

Auteurs

João Botelho (J)

Antibiotic Resistance Group, Max-Planck Institute for Evolutionary Biology, Plön, Germany; Evolutionary Ecology and Genetics, University of Kiel, Kiel, Germany. Electronic address: botelho@evolbio.mpg.de.

Leif Tüffers (L)

Evolutionary Ecology and Genetics, University of Kiel, Kiel, Germany; Department of Infectious Diseases and Microbiology, University of Lübeck, Lübeck, Germany.

Janina Fuss (J)

Institute of Clinical Molecular Biology, Christian Albrechts University and University Hospital Schleswig-Holstein, Kiel, Germany.

Florian Buchholz (F)

Evolutionary Ecology and Genetics, University of Kiel, Kiel, Germany.

Christian Utpatel (C)

Molecular and Experimental Mycobacteriology, Research Center Borstel, Borstel, Germany; German Center for Infection Research, Partner Site Hamburg-Lübeck-Borstel-Riems, Borstel, Germany.

Jens Klockgether (J)

Clinic for Paediatric Pneumology, Allergology, and Neonatology, Hannover Medical School (MHH), Hannover, Germany.

Stefan Niemann (S)

Molecular and Experimental Mycobacteriology, Research Center Borstel, Borstel, Germany; German Center for Infection Research, Partner Site Hamburg-Lübeck-Borstel-Riems, Borstel, Germany.

Burkhard Tümmler (B)

Clinic for Paediatric Pneumology, Allergology, and Neonatology, Hannover Medical School (MHH), Hannover, Germany; Biomedical Research in Endstage and Obstructive Lung Disease Hannover (BREATH), German Center for Lung Research, Hannover Medical School, Hannover, Germany.

Hinrich Schulenburg (H)

Antibiotic Resistance Group, Max-Planck Institute for Evolutionary Biology, Plön, Germany; Evolutionary Ecology and Genetics, University of Kiel, Kiel, Germany. Electronic address: hschulenburg@zoologie.uni-kiel.de.

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Classifications MeSH