“Temporal variability of theHyalomma marginatum-borne pathogens in a sentinel site of the Occitanie region (France), a focus on the intriguing dynamics ofRickettsia aeschlimannii”

Abstract

AbstractSpatio-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 speciesHyalomma marginatumhas recently become established in southern France. It carries pathogens of medical and veterinary interest including the Crimean-Congo hemorrhagic fever virus,Rickettsia aeschlimannii, Theileria equiandAnaplasma phagocytophilumamong others. While the pathogenic communities ofH. marginatumwere identified and their spatial distribution characterised, their temporal dynamics are still unknown. We performed a monthlyH. marginatumtick 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 includedR. aeschlimannii, A. phagocytophilumandT. equiwith infection rates reaching 47.0%, 4.6% and 11.0% respectively. Overall, 14.6% of ticks were infected with at leastTheileriaorAnaplasma, with monthly fluctuations ranging from 2.9% to 28.6%. Strong temporal patterns were observed for each of the detected pathogens, particularly forR. aeschlimanniiwhose 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 thatR. aeschlimanniimight be a secondary symbiont ofH. marginatumthat could play a role into stress response to temperature. The analysis of monthly and seasonal fluctuations inH. marginatum-borne pathogens allowed us to conclude that the risk of infection is present throughoutH. marginatumactivity period, but particularly in summer.HighlightsStrong monthly fluctuations of pathogen infection rates were observed especially forRickettsia aeschlimannii, currently identified as a human pathogen whose pathogenic status in humans and its symbiotic status inH. marginatumare both questioned.The increase in temperature is correlated with the increase inRickettsia aeschlimanniiinfection rates, providing clues about its potential function as a symbiont inH. marginatum.Ticks are recurrently infected with at least one other pathogen belonging toTheileriaorAnaplasmagenera with monthly fluctuations ranging from 2.9% to 28.6%.The monthly dynamics ofH. marginatum-borne pathogens are important to consider to assess the risk posed by this tick.Graphical abstract