The Recent Evolution of a Maternally-Inherited Endosymbiont of Ticks Led to the Emergence of the Q Fever Pathogen, Coxiella burnetii - PubMed (original) (raw)
. 2015 May 15;11(5):e1004892.
doi: 10.1371/journal.ppat.1004892. eCollection 2015 May.
Valérie Noël 1, Karen D McCoy 1, Matteo Bonazzi 2, Karim Sidi-Boumedine 3, Olivier Morel 4, Fabrice Vavre 4, Lionel Zenner 4, Elsa Jourdain 5, Patrick Durand 1, Céline Arnathau 1, François Renaud 1, Jean-François Trape 1, Abel S Biguezoton 6, Julie Cremaschi 1, Muriel Dietrich 1, Elsa Léger 1, Anaïs Appelgren 1, Marlène Dupraz 1, Elena Gómez-Díaz 7, Georges Diatta 8, Guiguigbaza-Kossigan Dayo 9, Hassane Adakal 10, Sébastien Zoungrana 9, Laurence Vial 11, Christine Chevillon 1
Affiliations
- PMID: 25978383
- PMCID: PMC4433120
- DOI: 10.1371/journal.ppat.1004892
The Recent Evolution of a Maternally-Inherited Endosymbiont of Ticks Led to the Emergence of the Q Fever Pathogen, Coxiella burnetii
Olivier Duron et al. PLoS Pathog. 2015.
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.
Conflict of interest statement
The authors have declared that no competing interests exist.
Figures
Fig 1. Geographic origin of the sampled ticks and distribution of Coxiella and Rickettsiella infections.
Square size indicates the number of populations sampled per geographic area. Numbers refer to the tick species whereas letters discriminate the different populations screened within a species; this nomenclature is detailed in Table 1. The colors within squares indicate the infection status of populations. Two tick species were infected by both Coxiella and Rickettsiella at the species level, but not at individual and population levels.
Fig 2. Phylogenetic network with concatenated 16S rRNA, 23S rRNA, GroEL, rpoB and dnaK sequences (3009 unambiguously aligned bp), including 71 _Coxiella_-like strains of ticks, 15 C. burnetii reference strains, and bacterial outgroups.
The four Coxiella clades are labeled A to D. A zoom on the A clade which contains C. burnetii isolates is shown in Supplementary Fig C in S1 Text. Each number corresponds to one tick species as detailed in Table 1. Blue—Coxiella_-like organisms; red—_C. burnetii; green—Rickettsiella; black- other bacteria. All multi-locus typing of Coxiella and Rickettsiella of ticks are new sequences from this study. The scale bar is in units of substitution/site.
Fig 3. Characterization of new Coxiella strains derived from whole-genome sequencing (WGS) of the cattle tick Rhipicephalus microplus.
(a) Percent identity of 50 genes uniquely attributable to Coxiella from R. microplus WGS versus 15 sequenced C. burnetii genomes and other reference genomes. (b) Bacterial phylogeny, comprising the Coxiella found in the R. microplus WGS data, reconstructed from the concatenated sequences of Fig 3A (19,304 unambiguously aligned bp) using maximum-likelihood (ML). Branch numbers indicate percent bootstrap support for major branches (1,000 replicates; only bootstrap values >90% are shown). The scale bar is in units of substitution/site.
References
- Madariaga MG, Rezai K, Trenholme GM, Weinstein RA. Q fever: a biological weapon in your backyard. Lancet Infect Dis. 2003;3: 709–721. - PubMed
- Raoult D, Marrie T, Mege J. Natural history and pathophysiology of Q fever. Lancet Infect Dis. 2005;5: 219–226. - PubMed
Publication types
MeSH terms
Grants and funding
Financial support was provided by the CNRS-INEE (Programme PEPS-Ecologie de la Santé 2014, ‘SYMPATTIQUES’: OD LZ; http://www.cnrs.fr/inee/outils/PEPS2014.htm), French Polar Institue (IPEV,programme no. 333: KDMcC; http://www.institut-polaire.fr/ipev/programmes_de_recherche), the CNRS–INEE/TAAF (Programme Iles Eparses “PathOrnithoTiques”: KDMcC; http://www.cnrs.fr/inee/recherche/programmes/iles_eparses.htm), and the Agence Nationale de la Recherche (ANR-11-BSV7-003-02: KDMcC, ANR-13-BSV7-0018-01: KDMcC, ANR-3215AO-3R077-STEV: FR, PD, CA, JFT, ANR-11-LABX-0048: FV, OM, LZ, EJ; http://www.agence-nationale-recherche.fr/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
LinkOut - more resources
Full Text Sources
Other Literature Sources
Medical
Molecular Biology Databases