Cargando…

Pangenomic analysis of Coxiella burnetii unveils new traits in genome architecture

Coxiella burnetii is the etiological agent of Q fever, a worldwide zoonosis able to cause large outbreaks. The disease is polymorphic. Symptomatic primary infection is named acute Q fever and is associated with hepatitis, pneumonia, fever, and auto-immune complications while persistent focalized inf...

Descripción completa

Detalles Bibliográficos
Autores principales: Abou Abdallah, Rita, Million, Matthieu, Delerce, Jeremy, Anani, Hussein, Diop, Awa, Caputo, Aurelia, Zgheib, Rita, Rousset, Elodie, Sidi Boumedine, Karim, Raoult, Didier, Fournier, Pierre-Edouard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9721466/
https://www.ncbi.nlm.nih.gov/pubmed/36478861
http://dx.doi.org/10.3389/fmicb.2022.1022356
_version_ 1784843782580076544
author Abou Abdallah, Rita
Million, Matthieu
Delerce, Jeremy
Anani, Hussein
Diop, Awa
Caputo, Aurelia
Zgheib, Rita
Rousset, Elodie
Sidi Boumedine, Karim
Raoult, Didier
Fournier, Pierre-Edouard
author_facet Abou Abdallah, Rita
Million, Matthieu
Delerce, Jeremy
Anani, Hussein
Diop, Awa
Caputo, Aurelia
Zgheib, Rita
Rousset, Elodie
Sidi Boumedine, Karim
Raoult, Didier
Fournier, Pierre-Edouard
author_sort Abou Abdallah, Rita
collection PubMed
description Coxiella burnetii is the etiological agent of Q fever, a worldwide zoonosis able to cause large outbreaks. The disease is polymorphic. Symptomatic primary infection is named acute Q fever and is associated with hepatitis, pneumonia, fever, and auto-immune complications while persistent focalized infections, mainly endocarditis, and vascular infections, occur in a minority of patients but are potentially lethal. In order to evaluate the genomic features, genetic diversity, evolution, as well as genetic determinants of antibiotic resistance, pathogenicity, and ability to cause outbreaks of Q fever, we performed a pangenomic analysis and genomic comparison of 75 C. burnetii strains including 63 newly sequenced genomes. Our analysis demonstrated that C. burnetii has an open pangenome, unique genes being found in many strains. In addition, pathogenicity islands were detected in all genomes. In consequence C. burnetii has a high genomic plasticity, higher than that of other intracellular bacteria. The core- and pan-genomes are made of 1,211 and 4,501 genes, respectively (ratio 0.27). The core gene-based phylogenetic analysis matched that obtained from multi-spacer typing and the distribution of plasmid types. Genomic characteristics were associated to clinical and epidemiological features. Some genotypes were associated to specific clinical forms and countries. MST1 genotype strains were associated to acute Q fever. A significant association was also found between clinical forms and plasmids. Strains harboring the QpRS plasmid were never found in acute Q fever and were only associated to persistent focalized infections. The QpDV and QpH1 plasmids were associated to acute Q fever. In addition, the Guyanese strain CB175, the most virulent strain to date, exhibited a unique MST genotype, a distinct COG profile and an important variation in gene number that may explain its unique pathogenesis. Therefore, strain-specific factors play an important role in determining the epidemiological and clinical manifestations of Q fever alongside with host-specific factors (valvular and vascular defects notably).
format Online
Article
Text
id pubmed-9721466
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-97214662022-12-06 Pangenomic analysis of Coxiella burnetii unveils new traits in genome architecture Abou Abdallah, Rita Million, Matthieu Delerce, Jeremy Anani, Hussein Diop, Awa Caputo, Aurelia Zgheib, Rita Rousset, Elodie Sidi Boumedine, Karim Raoult, Didier Fournier, Pierre-Edouard Front Microbiol Microbiology Coxiella burnetii is the etiological agent of Q fever, a worldwide zoonosis able to cause large outbreaks. The disease is polymorphic. Symptomatic primary infection is named acute Q fever and is associated with hepatitis, pneumonia, fever, and auto-immune complications while persistent focalized infections, mainly endocarditis, and vascular infections, occur in a minority of patients but are potentially lethal. In order to evaluate the genomic features, genetic diversity, evolution, as well as genetic determinants of antibiotic resistance, pathogenicity, and ability to cause outbreaks of Q fever, we performed a pangenomic analysis and genomic comparison of 75 C. burnetii strains including 63 newly sequenced genomes. Our analysis demonstrated that C. burnetii has an open pangenome, unique genes being found in many strains. In addition, pathogenicity islands were detected in all genomes. In consequence C. burnetii has a high genomic plasticity, higher than that of other intracellular bacteria. The core- and pan-genomes are made of 1,211 and 4,501 genes, respectively (ratio 0.27). The core gene-based phylogenetic analysis matched that obtained from multi-spacer typing and the distribution of plasmid types. Genomic characteristics were associated to clinical and epidemiological features. Some genotypes were associated to specific clinical forms and countries. MST1 genotype strains were associated to acute Q fever. A significant association was also found between clinical forms and plasmids. Strains harboring the QpRS plasmid were never found in acute Q fever and were only associated to persistent focalized infections. The QpDV and QpH1 plasmids were associated to acute Q fever. In addition, the Guyanese strain CB175, the most virulent strain to date, exhibited a unique MST genotype, a distinct COG profile and an important variation in gene number that may explain its unique pathogenesis. Therefore, strain-specific factors play an important role in determining the epidemiological and clinical manifestations of Q fever alongside with host-specific factors (valvular and vascular defects notably). Frontiers Media S.A. 2022-11-21 /pmc/articles/PMC9721466/ /pubmed/36478861 http://dx.doi.org/10.3389/fmicb.2022.1022356 Text en Copyright © 2022 Abou Abdallah, Million, Delerce, Anani, Diop, Caputo, Zgheib, Rousset, Sidi Boumedine, Raoult and Fournier. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Abou Abdallah, Rita
Million, Matthieu
Delerce, Jeremy
Anani, Hussein
Diop, Awa
Caputo, Aurelia
Zgheib, Rita
Rousset, Elodie
Sidi Boumedine, Karim
Raoult, Didier
Fournier, Pierre-Edouard
Pangenomic analysis of Coxiella burnetii unveils new traits in genome architecture
title Pangenomic analysis of Coxiella burnetii unveils new traits in genome architecture
title_full Pangenomic analysis of Coxiella burnetii unveils new traits in genome architecture
title_fullStr Pangenomic analysis of Coxiella burnetii unveils new traits in genome architecture
title_full_unstemmed Pangenomic analysis of Coxiella burnetii unveils new traits in genome architecture
title_short Pangenomic analysis of Coxiella burnetii unveils new traits in genome architecture
title_sort pangenomic analysis of coxiella burnetii unveils new traits in genome architecture
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9721466/
https://www.ncbi.nlm.nih.gov/pubmed/36478861
http://dx.doi.org/10.3389/fmicb.2022.1022356
work_keys_str_mv AT abouabdallahrita pangenomicanalysisofcoxiellaburnetiiunveilsnewtraitsingenomearchitecture
AT millionmatthieu pangenomicanalysisofcoxiellaburnetiiunveilsnewtraitsingenomearchitecture
AT delercejeremy pangenomicanalysisofcoxiellaburnetiiunveilsnewtraitsingenomearchitecture
AT ananihussein pangenomicanalysisofcoxiellaburnetiiunveilsnewtraitsingenomearchitecture
AT diopawa pangenomicanalysisofcoxiellaburnetiiunveilsnewtraitsingenomearchitecture
AT caputoaurelia pangenomicanalysisofcoxiellaburnetiiunveilsnewtraitsingenomearchitecture
AT zgheibrita pangenomicanalysisofcoxiellaburnetiiunveilsnewtraitsingenomearchitecture
AT roussetelodie pangenomicanalysisofcoxiellaburnetiiunveilsnewtraitsingenomearchitecture
AT sidiboumedinekarim pangenomicanalysisofcoxiellaburnetiiunveilsnewtraitsingenomearchitecture
AT raoultdidier pangenomicanalysisofcoxiellaburnetiiunveilsnewtraitsingenomearchitecture
AT fournierpierreedouard pangenomicanalysisofcoxiellaburnetiiunveilsnewtraitsingenomearchitecture