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

International audienceQ 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

Update in the geographical distribution of the invasive tick <em>Hyalomma marginatum</em> in south of France; First attempts to identify factors favoring its establishment

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Strong evidence for the presence of the tick <em>Hyalomma marginatum</em> Koch, 1844 in southern continental France

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The Crimean‐Congo haemorrhagic fever tick vector Hyalomma marginatum in the south of France: Modelling its distribution and determination of factors influencing its establishment in a newly invaded area

International audienceWe developed a correlative model at high resolution for predicting the distribution of one of the main vectors of Crimean-Congo haemorrhagic fever virus (CCHFV), Hyalomma marginatum, in a recently colonised area, namely southern France. About 931 H. marginatum adult ticks were sampled on horses from 2016 to 2019 and 2021 in 14 southern French departments, which resulted in the first H. marginatum detection map on a large portion of the national territory. Such updated presence/absence data, as well as the mean number of H. marginatum per examined animal (mean parasitic load) as a proxy of tick abundance, were correlated to multiple parameters describing the climate and habitats characterising each collection site, as well as movements of horses as possible factors influencing tick exposure. In southern France, H. marginatum was likely detected in areas characterised by year-long warm temperatures and low precipitation, especially in summer and mostly concentrated in autumn, as well as moderate annual humidity, compared to other sampled areas. It confirms that even in newly invaded areas this tick remains exclusively Mediterranean and cannot expand outside this climatic range. Regarding the environment, a predominance of open natural habitats, such as sclerophyllous vegetated and sparsely vegetated areas, were also identified as a favourable factor, in opposition to urban or peri-urban and humid habitats, such as continuous urban areas and inland marshes, respectively, which were revealed to be unsuitable. Based on this model, we predicted the areas currently suitable for the establishment of the tick H. marginatum in the South of France, with relatively good accuracy using internal (AUC = 0.66) and external validation methods (AUC = 0.76 and 0.83). Concerning tick abundance, some correlative relationships were similar to the occurrence model, as well as the type of horse movements being highlighted as an important factor explaining mean parasitic load. However, the limitations of estimating and modelling H. marginatum abundance in a correlative model are discussed

Characterization of new <i>Coxiella</i> strains derived from whole-genome sequencing (WGS) of the cattle tick <i>Rhipicephalus microplus</i>.

<p>(a) Percent identity of 50 genes uniquely attributable to <i>Coxiella</i> from <i>R</i>. <i>microplus</i> WGS versus 15 sequenced <i>C</i>. <i>burnetii</i> genomes and other reference genomes. (b) Bacterial phylogeny, comprising the <i>Coxiella</i> found in the <i>R</i>. <i>microplus</i> 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.</p

List of tick species and populations included in the analysis, with details on their origin, the population sample size, and the prevalence of <i>Coxiella</i> spp. and <i>Rickettsiella</i> spp.

<p>List of tick species and populations included in the analysis, with details on their origin, the population sample size, and the prevalence of <i>Coxiella</i> spp. and <i>Rickettsiella</i> spp.</p

Phylogenetic network with concatenated 16S rRNA, 23S rRNA, <i>GroEL</i>, <i>rpoB</i> and <i>dnaK</i> sequences (3009 unambiguously aligned bp), including 71 <i>Coxiella</i>-like strains of ticks, 15 <i>C</i>. <i>burnetii</i> reference strains, and bacterial outgroups.

<p>The four <i>Coxiella</i> clades are labeled A to D. A zoom on the A clade which contains <i>C</i>. <i>burnetii</i> isolates is shown in Supplementary Fig C in <a href="http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004892#ppat.1004892.s001" target="_blank">S1 Text</a>. Each number corresponds to one tick species as detailed in <a href="http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004892#ppat.1004892.t001" target="_blank">Table 1</a>. Blue—<i>Coxiella</i>-like organisms; red—<i>C</i>. <i>burnetii</i>; green—<i>Rickettsiella</i>; black- other bacteria. All multi-locus typing of <i>Coxiella</i> and <i>Rickettsiella</i> of ticks are new sequences from this study. The scale bar is in units of substitution/site.</p