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.

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BackgroundThe variation of tick abundance on ruminants had received little attention in West Africa before Rhipicephalus (Boophilus) microplus started to invade this region in the early 2000s. Ten years later, R. microplus was suspected to have replaced the native ticks. In addition to testing this hypothesis, this study investigated the interactions between native and invasive ticks and the relative role of climatic and geographical variables in the variations of tick community composition (beta diversity) on cattle herds.MethodsA one-year-long survey was performed in Benin and Burkina Faso during which adult ticks were collected from 144 steers from 12 localities in four different areas once a month. Morphological features were used to assign the collected ticks to different species (A. variegatum, R. annulatus, R. decoloratus, R. microplus and R. geigyi). Beta diversity analyses and generalized linear models allowed characterizing the geographical variations in species assemblage and the effect of co-infestation patterns on the seasonal variations in the abundance and incidence rates of each taxon.ResultsAbout 68 % (22,491/32,148) of all the adult ticks collected in one year were R. microplus. The most heterogeneously distributed taxa were Hyalomma spp and R. microplus and the lowest specific diversity was found in Central Burkina Faso. Although climatic variables did not provide any additional information on the variation in species assemblages compared with the sampling geography, adult tick abundance tended to peak during the late (Boophilus subgenus) or early (other taxa) rainy season. In most taxon-per-locality analyses, the abundance and incidence rate of a given tick taxon significantly increased when the host was co-infested by other taxa. The comparison with previous estimates (when possible) did not support the hypothesis that R. microplus invasion led to a decrease in native tick species abundance.ConclusionsThe co-infestation patterns among native and invasive tick species are key factors for the determination of the community structure and the infestation dynamics of each tick taxon in West African cattle.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-016-1305-z) contains supplementary material, which is available to authorized users.

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BackgroundThe invasion of West Africa by Rhipicephalus microplus during the past decade has changed the ecological situation of the agent of heartwater Ehrlichia ruminantium in this area. Before, its local vector, Amblyomma variegatum, was the most abundant tick species found on livestock. Today, the abundance of the R. microplus is one magnitude higher than that of A. variegatum in many west-African localities. We investigated the potential of this new ecological situation to impact the circulation of E. ruminantium in West Africa.MethodsEhrlichia ruminantium infections were assessed with the specific PCR-diagnosis targeting the PCS20 region. This screening was applied on field samples of 24 R. microplus adults, on four females from a laboratory strain that had been blood-fed since larvae on one E. ruminantium-infected steer as well as on the offspring of these females at egg and larval stages.ResultsThe PCR detected E. ruminantium in 29 % of the field-collected R. microplus, i.e. twice as much as reported for A. variegatum with the same protocol. Regarding the laboratory strain, the PCR-diagnosis performed showed that all females were infected and passed the rickettsia to their progeny. Sequencing of the PCR product confirmed that the maternally inherited rickettsia was E. ruminantium.ConclusionAccording to the present findings, the invasive dynamic of R. microplus in West Africa is currently impacting the local evolutionary conditions of E. ruminantium since it offers new transmission roads such as maternal transmission in R. microplus.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-016-1651-x) contains supplementary material, which is available to authorized users.

Article type : Original Article First digital characterization of the transhumance corridors through Benin used by cattle herds from Burkina Faso and associated risk scoring regarding the invasion of Rhipicephalus (Boophilus) microplus

After the introduction of the invasive cattle tick Rhipicephalus microplus in West Africa in the last decade, farmers encounter ticks resistance to the use of acaricides in different region in Benin. In order to evaluate the level of resistance, an in vitro study was performed on five samples of R. (Boophilus) microplus collected from five farms in four of the eight agro-ecological zone of Benin. The districts concerned with the study in the agro-ecological zone were Houeyogbe (Kpinnou), Zangnanado (Samiondji), Tchaourou (Okpara), Gogounou (Fana) and Bassila (Manigri). A toxicological test, the Larval Packet Test (LPT) was performed in the laboratory of Biotechnology Research Unit of the Animal Production and Health (URBPSA) at the Polytechnic School of University of Abomey-Calavi in Benin with the susceptible, Rhipicephalus geigyi strain from Hounde in Burkina Faso. Three (3) acaricides commonly used by farmers in Benin to control ticks were evaluated: alpha-cypermethrin, deltamethrin and amitraz. The results showed that the resistance ratio at 50% (RR 50 95% CI) for the whole experiment varies from 1.96 to 338.5. Based on RR 50 and RR 90 values, only the population of Samiondji's state farm was susceptible to the alpha-cypermethrin with a resistance ratio RR 50 = 1.64 (95% CI: 0.2 to 12.6), all the other resistance tests conducted on moderate or high resistance Bassila and Kpinnou appear to host the most resistant samples. Moreover, a certain high variability of dose response relationship has been noticed with amitraz on the base of the higher slope of the related curves.