Spatial patterns of Hyalomma marginatum-borne pathogens in the Occitanie region (France), a focus on the intriguing dynamics of Rickettsia aeschlimannii

Hyalomma marginatum is an invasive tick species recently established in mainland southern France. This tick is known to host a diverse range of human and animal pathogens such as Rickettsia aeschlimannii, Theileria equi, Anaplasma phagocytophilum, Anaplasma marginale, Ehrlichia minasensis, Crimean-Congo hemorrhagic fever and West Nile virus. While information about the dynamics of these pathogens is crucial to assess disease risk and develop effective monitoring strategies, few data on the spatial dynamics of these pathogens are currently available. We thus collected ticks in 27 sites in the Occitanie region to characterize spatial patterns of H. marginatum- borne pathogens. Several pathogens have been detected: Theileria equi (9.2%), Theileria orientalis (0.2%), Anaplasma phagocytophilum (1.6%), Anaplasma marginale (0.8%) and Rickettsia aeschlimannii (87.3%). Interestingly, we found a spatial clustered distribution for the pathogen R. aeschlimannii between two geographically isolated areas with infection rates and bacterial loads significantly lower in Herault/Gard departments (infection rate 78.6% in average) compared to Aude/Pyrenees-Orientales departments (infection rate 92.3% in average). At a smaller scale, R. aeschlimannii infection rates varied from one site to another, ranging from 29% to 100%. Overall, such high infection rates (87.3% in average) and the effective maternal transmission of R. aeschlimannii might suggest a role as a tick symbiont in H. marginatum. Moreover, currently identified as a human pathogen, such results also question about its pathogenic status in humans given the low number of human cases. Further studies are thus needed to understand both the status and the role of R. aeschlimannii in H. marginatum ticks. IMPORTANCETicks are obligatory hematophagous arthropods which transmit pathogens of medical and veterinary importance. Their infections cause serious health issues in humans and considerable economic loss in domestic animals. Information about the presence of pathogens in ticks and their dynamics is crucial to assess disease risk for public and animal health. Analysing tick-borne pathogens in ticks collected in 27 sites in the regions Occitanie, our results highlight clear spatial patterns in the Hyalomma marginatum-borne pathogen distribution and strengthen the postulate that it is essential to develop effective monitoring strategies and consider the spatial scale to better characterize the circulation of tick-borne pathogens.