Temporal variability of the Hyalomma marginatum-borne pathogens in a sentinel site of the Occitanie region (France), a focus on the intriguing dynamics of Rickettsia aeschlimannii

Abstract

Abstract Spatio-temporal scales have a clear influence on microbial community distribution and diversity and are thus essential to consider to identify and study the dynamics of microorganisms. The invasive tick species Hyalomma marginatum has recently become established in southern France. It carries pathogens of medical and veterinary interest including the Crimean-Congo hemorrhagic fever virus, Rickettsia aeschlimannii, Theileria equi and Anaplasma phagocytophilum among others. While the pathogenic communities of H. marginatum were identified and their spatial distribution characterised, their temporal dynamics are still unknown. We performed a monthly H. marginatum tick collection from February to September 2022 in a sentinel site in southern France in order to study their presence and temporal dynamics. On the 281 ticks analysed, we detected pathogens included R. aeschlimannii, A. phagocytophilum and T. equi with infection rates reaching 47.0%, 4.6% and 11.0% respectively. Overall, 14.6% of ticks were infected with at least Theileria or Anaplasma , with monthly fluctuations ranging from 2.9% to 28.6%. Strong temporal patterns were observed for each of the detected pathogens, particularly for R. aeschlimannii whose infection rates drastically increased at the beginning of summer, correlated with the monthly mean temperatures in the sentinel site. Based on these results, we hypothesized that R. aeschlimannii might be a secondary symbiont of H. marginatum that could play a role into stress response to temperature. The analysis of monthly and seasonal fluctuations in H. marginatum -borne pathogens allowed us to conclude that the risk of infection is present throughout H. marginatum activity period, but particularly in summer. Highlights Strong monthly fluctuations of pathogen infection rates were observed especially for Rickettsia aeschlimannii , currently identified as a human pathogen whose pathogenic status in humans and its symbiotic status in H. marginatum are both questioned. The increase in temperature is correlated with the increase in Rickettsia aeschlimannii infection rates, providing clues about its potential function as a symbiont in H. marginatum . Ticks are recurrently infected with at least one other pathogen belonging to Theileria or Anaplasma genera with monthly fluctuations ranging from 2.9% to 28.6%. The monthly dynamics of H. marginatum -borne pathogens are important to consider to assess the risk posed by this tick. Graphical abstract