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

PLoS Pathogens

Guiguigbaza-Kossigan Dayo¹  Matteo Bonazzi²  Christine Chevillon³  François Renaud⁴  Olivier Duron⁴  Jean-François Trape⁴  Marlène Dupraz⁴  Elsa Léger⁴  Valérie Noël⁴  Karen D. McCoy⁴  Georges Diatta⁴  Elena Gómez-Díaz⁴  Patrick Durand⁴  Abel S. Biguezoton⁴  Muriel Dietrich⁴  Anaïs Appelgren⁴  Céline Arnathau⁴  Lionel Zenner⁵  Olivier Morel⁵  Fabrice Vavre⁵  Karim Sidi-Boumedine⁶  Elsa Jourdain⁷  Sébastien Zoungrana⁸  Julie Cremaschi⁸  Laurence Vial⁸  Hassane Adakal⁹ 

[1] Biology Department, O. Wayne Rollins Research Center, Emory University, Atlanta, Georgia, United States of America;Centre d’études d’agents Pathogènes et Biotechnologies pour la Santé (CPBS), Centre National de la Recherche Scientifique (UMR5236)—Université de Montpellier, Montpellier, France;Département des Sciences et Techniques de l’Elevage (DSTE/FASE), Université Dan Dicko Dan Koulodo, Maradi, Niger;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;Laboratoire de Biométrie et Biologie Évolutive (LBBE), Centre National de la Recherche Scientifique (UMR5558)—Université Claude Bernard Lyon 1, Villeurbanne, France;National Reference Laboratory on Q Fever, French Agency for Food, Environmental and Occupational Health Safety (ANSES), Sophia-Antipolis, France;Unité d'Epidémiologie Animale, Institut National de le Recherche Agronomique (UR346), Saint Genès Champanelle, 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;Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes (URMITE), Centre National de la Recherche Scientifique (UMR6236)—Aix Marseille Université, Dakar, Sénégal

关键词: Coxiella burnetii;    Rodents;    Vertebrates;    Sequence alignment;    Ribosomal RNA;    Livestock;    Polymerase chain reaction;    Ticks;   

DOI  :  10.1371/journal.ppat.1004892

学科分类：生物科学（综合）

来源: Public Library of Science

【 摘 要 】

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.

【 授权许可】

CC BY