Genomic changes during the evolution of the Coxiella genus along the parasitism-mutualism continuum

10.24072/pcjournal.269 - Peer Community Journal, Volume 3 (2023), article no. e41.

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The Coxiellaceae family is composed of five genera showing lifestyles ranging from free-living to symbiosis. Among them, Coxiella burnetii is a well-known pathogen causing Q fever in humans. This bacterium presents both intracellular (parasitic) and environmental (resistant) forms. Recently, several environmental Coxiella genomes have been reported, among which several have come from intracellular mutualistic symbionts of ticks, termed Coxiella-like endosymbionts. We sequenced two new Coxiella-LE genomes from Dermacentor marginatus (CLEDm) and Ornithodoros maritimus (CLEOmar) ticks, the latter belonging to the C. burnetii lineage. Using these newly sequenced Coxiella-LEs and 43 Coxiellaceae genomes, we conducted comparative genomic and phylogenomic analyses to increase our knowledge of C. burnetii pathogenicity and the emergence of Coxiella-LEs. Results highlight the probably parasitic nature of the common ancestor of the Coxiellaceae. Indeed, the virulence factor Dot/Icm T4 Secretion System is present in most, but not all, Coxiellaceae. Whereas it is part of a putative pathogenic island in C. burnetii, it has been entirely lost or inactivated in Coxiella-LEs, suggesting its importance in pathogenesis. Additionally, we found that a Sha/Mrp antiporter was laterally acquired in the C. burnetii lineage. This antiporter might be involved in alkali resistance and the development of the resistant form that is able to persist in the environment for long periods of time. The Sha operon is eroded or absent in Coxiella-LEs. Finally, we found that all Coxiella representatives produce B vitamins and co-factors indicating a pre-adaptation of Coxiella to mutualism with hematophagous arthropods. Accordingly, the ancestor of C. burnetii and Coxiella-LEs was likely a parasitic bacterium able to manipulate its host cell and to produce vitamins and co-factors for its own use.

Published online:
DOI: 10.24072/pcjournal.269
Keywords: Coxiella; Q fever; endosymbiosis; ticks; pathogenic island; pH homeostasis
Santos-Garcia, Diego 1, 2; Morel, Olivier 1; Henri, Hélène 1; El Filali, Adil 1; Buysse, Marie 3; Noël, Valérie 3; McCoy, Karen D. 3; Gottlieb, Yuval 4; Klasson, Lisa 5; Zenner, Lionel 1; Duron, Olivier 3; Vavre, Fabrice 1

1 University of Lyon, University Lyon 1, CNRS, VetAgro Sup, Laboratory of Biometry and Evolutionary Biology, UMR5558, Villeurbanne, France.
2 Present address: Center for Biology and Management of Populations (CBGP) INRAe UMR1062, Montferrier-sur-Lez, France.
3 MIVEGEC, University of Montpellier, CNRS, IRD, Montpellier, France.
4 Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel.
5 Molecular evolution, Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, Uppsala, Sweden.
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Santos-Garcia, Diego and Morel, Olivier and Henri, H\'el\`ene and El Filali, Adil and Buysse, Marie and No\"el, Val\'erie and McCoy, Karen D. and Gottlieb, Yuval and Klasson, Lisa and Zenner, Lionel and Duron, Olivier and Vavre, Fabrice},
     title = {Genomic changes during the evolution of the {\protect\emph{Coxiella}} genus along the parasitism-mutualism continuum
     journal = {Peer Community Journal},
     eid = {e41},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.269},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.269/}
AU  - Santos-Garcia, Diego
AU  - Morel, Olivier
AU  - Henri, Hélène
AU  - El Filali, Adil
AU  - Buysse, Marie
AU  - Noël, Valérie
AU  - McCoy, Karen D.
AU  - Gottlieb, Yuval
AU  - Klasson, Lisa
AU  - Zenner, Lionel
AU  - Duron, Olivier
AU  - Vavre, Fabrice
TI  - Genomic changes during the evolution of the Coxiella genus along the parasitism-mutualism continuum

JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.269/
DO  - 10.24072/pcjournal.269
ID  - 10_24072_pcjournal_269
ER  - 
%0 Journal Article
%A Santos-Garcia, Diego
%A Morel, Olivier
%A Henri, Hélène
%A El Filali, Adil
%A Buysse, Marie
%A Noël, Valérie
%A McCoy, Karen D.
%A Gottlieb, Yuval
%A Klasson, Lisa
%A Zenner, Lionel
%A Duron, Olivier
%A Vavre, Fabrice
%T Genomic changes during the evolution of the Coxiella genus along the parasitism-mutualism continuum

%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.269/
%R 10.24072/pcjournal.269
%F 10_24072_pcjournal_269
Santos-Garcia, Diego; Morel, Olivier; Henri, Hélène; El Filali, Adil; Buysse, Marie; Noël, Valérie; McCoy, Karen D.; Gottlieb, Yuval; Klasson, Lisa; Zenner, Lionel; Duron, Olivier; Vavre, Fabrice. Genomic changes during the evolution of the Coxiella genus along the parasitism-mutualism continuum
. Peer Community Journal, Volume 3 (2023), article  no. e41. doi : 10.24072/pcjournal.269. https://peercommunityjournal.org/articles/10.24072/pcjournal.269/

Peer reviewed and recommended by PCI : 10.24072/pci.microbiol.100003

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

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