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

被引：219

作者：

Duron, Olivier ^{[1
]}

Noel, Valerie ^{[1
]}

McCoy, Karen D. ^{[1
]}

Bonazzi, Matteo ^{[2
]}

Sidi-Boumedine, Karim ^{[3
]}

Morel, Olivier ^{[4
]}

Vavre, Fabrice ^{[4
]}

Zenner, Lionel ^{[4
]}

Jourdain, Elsa ^{[5
]}

Durand, Patrick ^{[1
]}

Arnathau, Celine ^{[1
]}

Renaud, Francois ^{[1
]}

Trape, Jean-Francois ^{[1
]}

Biguezoton, Abel S. ^{[1
]}

Cremaschi, Julie ^{[1
]}

Dietrich, Muriel ^{[1
]}

Leger, Elsa ^{[1
]}

Appelgren, Anais ^{[1
]}

Dupraz, Marlene ^{[1
]}

Gomez-Diaz, Elena ^{[1
,7
]}

Diatta, Georges ^{[8
]}

Dayo, Guiguigbaza-Kossigan ^{[6
]}

Adakal, Hassane ^{[6
,9
]}

Zoungrana, Sebastien ^{[6
]}

Vial, Laurence ^{[10
]}

Chevillon, Christine ^{[1
]}

机构：

[1] Univ Montpellier, Lab MIVEGEC Malad Infect & Vecteurs Ecol Genet Ev, Inst Rech & Dev UR 224, CNRS,UMR5290, F-34059 Montpellier, France

[2] Univ Montpellier, CNRS, UMR5236, Ctr Etud Agents Pathogenes & Biotechnol Sante CPB, F-34059 Montpellier, France

[3] French Agcy Food Environm & Occupat Hlth Safety A, Natl Reference Lab Fever Q, Sophia Antipolis, France

[4] Univ Lyon 1, CNRS, UMR5558, LBBE, F-69622 Villeurbanne, France

[5] INRA, UR346, Unite Epidemiol Anim, St Genes Champanelle, France

[6] Ctr Int Rech Dev Elevage Zone Subhumide CIRDES, Unite Rech Bases Biol Lutte Integree URBIO, Bobo Dioulasso, Burkina Faso

[7] Emory Univ, Dept Biol, O Wayne Rollins Res Ctr, Atlanta, GA 30322 USA

[8] Aix Marseille Univ, URMITE, CNRS, UMR6236, Dakar, Senegal

[9] Univ Dan Dicko Dan Koulodo, Dept Sci & Tech Elevage DSTE FASE, Maradi, Niger

[10] Ctr Cooperat Int Rech Agron Dev CIRAD, Prades Le Lez, France

来源：

PLOS PATHOGENS | 2015年 / 11卷 / 05期

关键词：

LONE STAR TICK; RHIPICEPHALUS-SANGUINEUS; INTRACELLULAR SYMBIONTS; GENOME SEQUENCE; DIVERSITY; WOLBACHIA; BACTERIUM; ARSENOPHONUS; INFECTION; TRANSMISSION;

D O I：

10.1371/journal.ppat.1004892

中图分类号：

Q93 [微生物学];

学科分类号：

071005 ; 100705 ;

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.

引用

页数：23

共 68 条

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