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The Recent Evolution of a Maternally-Inherited Endosymbiont of Ticks Led to the Emergence of the Q Fever Pathogen, Coxiella burnetii

Olivier Duron 1 Valérie Noël 2 Karen D. Mccoy 1 Matteo Bonazzi 3 Karim Sidi-Boumedine 4 Olivier Morel 5 Fabrice Vavre 6, 5 Lionel Zenner 5, 7 Elsa Jourdain 8 Durand Patrick 9 Céline Arnathau 9 François Renaud 10 Jean-François Trape 10 Abel S. Biguezoton 10 Julie Cremaschi 10 Muriel Dietrich 10 Elsa Léger 11 Anaïs Appelgren 10 Marlène Dupraz 12 Elena Gómez-Díaz 10 Georges Diatta 13 Guiguigbaza-Kossigan Dayo 14, 15 Hassane Adakal 16, 17 Sébastien Zoungrana 16 Laurence Vial 18 Christine Chevillon 1
1 MIVEGEC-EVCO - Evolution of host-microbe communities
PEEC - Processus Écologiques et Évolutifs au sein des Communautés
2 MIVEGEC-ETE - Evolution Théorique et Expérimentale
PEV - Perturbations, Evolution, Virulence
5 Génétique et évolution des interactions hôtes-parasites
GINSENG - Département génétique, interactions et évolution des génomes [LBBE]
9 MIVEGEC-HEAT - Health, Emergence, Adaptation and Transmission
PEEC - Processus Écologiques et Évolutifs au sein des Communautés
Abstract : Q fever is a highly infectious disease with a worldwide distribution. Its causative agent, the intracellular bacterium Coxiella burnetii, infects a variety of vertebrate species, including humans. Its evolutionary origin remains almost entirely unknown and uncertainty persists regarding the identity and lifestyle of its ancestors. A few tick species were recently found to harbor maternally-inherited Coxiella-like organisms engaged in symbiotic interactions, but their relationships to the Q fever pathogen remain unclear. Here, we extensively sampled ticks, identifying new and atypical Coxiella strains from 40 of 58 examined species, and used this data to infer the evolutionary processes leading to the emergence of C. burnetii. Phylogenetic analyses of multi-locus typing and whole-genome sequencing data revealed that Coxiella-like organisms represent an ancient and monophyletic group allied to ticks. Remarkably, all known C. burnetii strains originate within this group and are the descendants of a Coxiella-like progenitor hosted by ticks. Using both colony-reared and field-collected gravid females, we further establish the presence of highly efficient maternal transmission of these Coxiella-like organisms in four examined tick species, a pattern coherent with an endosymbiotic lifestyle. Our laboratory culture assays also showed that these Coxiella-like organisms were not amenable to culture in the vertebrate cell environment, suggesting different metabolic requirements compared to C. burnetii. Altogether, this corpus of data demonstrates that C. burnetii recently evolved from an inherited symbiont of ticks which succeeded in infecting vertebrate cells, likely by the acquisition of novel virulence factors.
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Olivier Duron, Valérie Noël, Karen D. Mccoy, Matteo Bonazzi, Karim Sidi-Boumedine, et al.. The Recent Evolution of a Maternally-Inherited Endosymbiont of Ticks Led to the Emergence of the Q Fever Pathogen, Coxiella burnetii. PLoS Pathogens, Public Library of Science, 2015, 11 (5), ⟨10.1371/journal.ppat.1004892⟩. ⟨hal-01250470⟩

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