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

Community structure, seasonal variations and interactions between native and invasive cattle tick species in Benin and Burkina Faso

International audienceBackground: The 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.Methods: A 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.Results: About 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.Conclusion: The 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

Influence des activités agricoles sur la végétation le long d’un gradient pluviométrique nord-sud du Burkina Faso

Evaluation of the ecological state of Burkina Faso landscapes is necessary to understand human action on environment. This study aimed at characterizing the study sites to understand interactions between climate, humans and ecosystems along a rainfall gradient. The study was carried out along anthropic gradients overlapping protected areas, cropping areas and grazing areas in four agro-sylvo-pastoral areas of Burkina Faso. Floristic inventories were conducted at ecological surveys sites, according to an itinerant inventory method. The floristic richness is decreasing along the rainfall gradient and anthropic gradients. Correspondence analysis of floristic surveys allowed us separating the sahelian to savannah area and representing three types of landscapes (protected, cropping and grazing areas) in each zone based on land use, thus proving human impacts on ecosystem. Human action and climate aridity seems to have the same effect on vegetation. Grazing areas appear as intermediate ecology zones between cropping areas and protected areas.Les écosystèmes subissent à la foi la pression humaine et climatique depuis des décennies, ainsi l’évaluation de l’état écologique des paysages agraires du Burkina Faso est nécessaire pour mettre en évidence l’action humaine sur l’environnement. Dans le cadre de cette étude, l’objectif est de caractériser quatre zones agro-sylvo-pastorales pour comprendre l’interaction entre le climat, l’action humaine et l’écosystème le long d’un gradient pluviométrique. L’étude a été réalisée sur des gradients anthropiques recoupant les aires protégées, les zones de cultures et les zones pâturées dans quatre zones agro-sylvo-pastorales du Burkina Faso. Des relevés floristiques ont été effectués au niveau des sites de suivis écologiques mis en place, selon la méthode d’inventaire itinérante. La richesse spécifique de la flore a été décroissante le long du gradient pluviométrique et du gradient anthropique. L’analyse factorielle des correspondances des relevés floristiques a permis de séparer le domaine sahélien de la savane. Elle a permis également de représenter 3 types de paysages (aires protégées, zones de cultures et zones pâturées) dans chaque zone agro-sylvo-pastorale. La répartition paysagère s’est faite en fonction de l’occupation du sol, mettant ainsi en évidence l’action humaine. Les zones pâturées se présentent comme des zones à écologie intermédiaire entre les zones de cultures et les aires protégées

Influence des activités agricoles sur la végétation le long d’un gradient pluviométrique nord-sud du Burkina Faso

Evaluation of the ecological state of Burkina Faso landscapes is necessary to understand human action on environment. This study aimed at characterizing the study sites to understand interactions between climate, humans and ecosystems along a rainfall gradient. The study was carried out along anthropic gradients overlapping protected areas, cropping areas and grazing areas in four agro-sylvo-pastoral areas of Burkina Faso. Floristic inventories were conducted at ecological surveys sites, according to an itinerant inventory method. The floristic richness is decreasing along the rainfall gradient and anthropic gradients. Correspondence analysis of floristic surveys allowed us separating the sahelian to savannah area and representing three types of landscapes (protected, cropping and grazing areas) in each zone based on land use, thus proving human impacts on ecosystem. Human action and climate aridity seems to have the same effect on vegetation. Grazing areas appear as intermediate ecology zones between cropping areas and protected areas

Ehrlichia ruminantium infects Rhipicephalus microplus in West Africa

International audienceBackground: The 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

The potential of Rhipicephalus microplus as a vector of Ehrlichia ruminantium in West Africa

International audienceHeartwater, or cowdriosis, is a virulent tick-borne rickettsial disease of ruminants caused by Ehrlichia ruminantium, biologically transmitted by Amblyomma species (A. variegatum in West Africa). In West Africa, this bacterium was recently reported to naturally infect the invasive cattle tick, Rhipicephalus microplus (Rm) through trans-ovarian transmission from replete adult females to offspring. A ‘sheep-tick-sheep’ cycle was set up to determine whether feeding the progeny of these ticks on naïve sheep could lead to infection, and to compare clinical outcomes resulting from this transmission with those observed following infection by the natural A. variegatum (Av) vector. Using local strains of ticks (KIMINI-Rm and KIMINI-Av) and of E. ruminantium (BK242), we recorded, using the PCR technique, the presence of bacterial DNA in ticks (larvae for Av and females for Rm) engorged on sheep inoculated by BK242-infected blood. The bacterial DNA was also detected in the next stages of the lifecycle of R. microplus (eggs and larvae), and in sheep infested either by those R. microplus larvae or by A. variegatum nymphs moulted from larvae engorged on blood-inoculated sheep. Bacterial infection in these sheep was demonstrated by detecting antibodies to E. ruminantium using the MAP1-B ELISA and by isolation of the bacterium on cell culture from blood. The sequences of PCS20 gene detected in ticks and sheep were identical to that of the BK242 strain. Our results confirm that R. microplus can acquire and transmit E. ruminantium to the next stage. However, this transmission resulted in a mild subclinical disease whereas severe clinical disease was observed in sheep infested by A. variegatum infected nymphs, suggesting differences in the tick/bacteria relationship. Future studies will focus on replicating these findings with ticks of different isolates and life stages to determine if R. microplus is playing a role in the epidemiology of heartwater in West Africa. Additionally, studies will investigate whether sheep that are seropositive due to infestation by E. ruminantium-infected R. microplus are subsequently protected against heartwater. Such data will add to our understanding of the possible impact of R. microplus in areas where it has become recently established

The potential of Rhipicephalus microplus as a vector of Ehrlichia ruminantium in West Africa

International audienceHeartwater, or cowdriosis, is a virulent tick-borne rickettsial disease of ruminants caused by Ehrlichia ruminantium, biologically transmitted by Amblyomma species (A. variegatum in West Africa). In West Africa, this bacterium was recently reported to naturally infect the invasive cattle tick, Rhipicephalus microplus (Rm) through trans-ovarian transmission from replete adult females to offspring. A ‘sheep-tick-sheep’ cycle was set up to determine whether feeding the progeny of these ticks on naïve sheep could lead to infection, and to compare clinical outcomes resulting from this transmission with those observed following infection by the natural A. variegatum (Av) vector. Using local strains of ticks (KIMINI-Rm and KIMINI-Av) and of E. ruminantium (BK242), we recorded, using the PCR technique, the presence of bacterial DNA in ticks (larvae for Av and females for Rm) engorged on sheep inoculated by BK242-infected blood. The bacterial DNA was also detected in the next stages of the lifecycle of R. microplus (eggs and larvae), and in sheep infested either by those R. microplus larvae or by A. variegatum nymphs moulted from larvae engorged on blood-inoculated sheep. Bacterial infection in these sheep was demonstrated by detecting antibodies to E. ruminantium using the MAP1-B ELISA and by isolation of the bacterium on cell culture from blood. The sequences of PCS20 gene detected in ticks and sheep were identical to that of the BK242 strain. Our results confirm that R. microplus can acquire and transmit E. ruminantium to the next stage. However, this transmission resulted in a mild subclinical disease whereas severe clinical disease was observed in sheep infested by A. variegatum infected nymphs, suggesting differences in the tick/bacteria relationship. Future studies will focus on replicating these findings with ticks of different isolates and life stages to determine if R. microplus is playing a role in the epidemiology of heartwater in West Africa. Additionally, studies will investigate whether sheep that are seropositive due to infestation by E. ruminantium-infected R. microplus are subsequently protected against heartwater. Such data will add to our understanding of the possible impact of R. microplus in areas where it has become recently established