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PLoS Pathog. 2015 May 15;11(5):e1004892. doi: 10.1371/journal.ppat.1004892. eCollection 2015 May.

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

Author information

1
Laboratoire MIVEGEC (Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle), Centre National de la Recherche Scientifique (UMR5290)-Université de Montpellier-Institut pour la Recherche et le Développement (UR 224), Montpellier, France.
2
Centre d'études d'agents Pathogènes et Biotechnologies pour la Santé (CPBS), Centre National de la Recherche Scientifique (UMR5236)-Université de Montpellier, Montpellier, France.
3
National Reference Laboratory on Q Fever, French Agency for Food, Environmental and Occupational Health Safety (ANSES), Sophia-Antipolis, France.
4
Laboratoire de Biométrie et Biologie Évolutive (LBBE), Centre National de la Recherche Scientifique (UMR5558)-Université Claude Bernard Lyon 1, Villeurbanne, France.
5
Unité d'Epidémiologie Animale, Institut National de le Recherche Agronomique (UR346), Saint Genès Champanelle, France.
6
Laboratoire MIVEGEC (Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle), Centre National de la Recherche Scientifique (UMR5290)-Université de Montpellier-Institut pour la Recherche et le Développement (UR 224), Montpellier, France; Unité de Recherche sur les Bases Biologiques de la lutte intégrée (URBIO), Centre International de Recherche-Développement sur l'Elevage en zone Subhumide (CIRDES), Bobo-Dioulasso, Burkina Faso.
7
Laboratoire MIVEGEC (Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle), Centre National de la Recherche Scientifique (UMR5290)-Université de Montpellier-Institut pour la Recherche et le Développement (UR 224), Montpellier, France; Biology Department, O. Wayne Rollins Research Center, Emory University, Atlanta, Georgia, United States of America.
8
Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes (URMITE), Centre National de la Recherche Scientifique (UMR6236)-Aix Marseille Université, Dakar, Sénégal.
9
Unité de Recherche sur les Bases Biologiques de la lutte intégrée (URBIO), Centre International de Recherche-Développement sur l'Elevage en zone Subhumide (CIRDES), Bobo-Dioulasso, Burkina Faso.
10
Unité de Recherche sur les Bases Biologiques de la lutte intégrée (URBIO), Centre International de Recherche-Développement sur l'Elevage en zone Subhumide (CIRDES), Bobo-Dioulasso, Burkina Faso; Département des Sciences et Techniques de l'Elevage (DSTE/FASE), Université Dan Dicko Dan Koulodo, Maradi, Niger.
11
Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), Prades-le-Lez, France.

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.

PMID:
25978383
PMCID:
PMC4433120
DOI:
10.1371/journal.ppat.1004892
[Indexed for MEDLINE]
Free PMC Article

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