Vector competence of the African argasid tick Ornithodoros moubata for the Q fever agent Coxiella burnetii

Abstract

Q fever is a widespread zoonotic disease caused by the intracellular bacterium Coxiella burnetii. While transmission is primarily but not exclusively airborne, ticks are usually thought to act as vectors on the basis of early microscopy studies. However, recent observations revealed that endosymbionts of ticks have been commonly misidentified as C. burnetii, calling the importance of tick-borne transmission into question. In this study, we re-evaluated the vector competence of the African soft tick Ornithodoros moubata for an avirulent strain of C. burnetii. To this end, we used an artificial feeding system to initiate infection of ticks, specific molecular tools to monitor further infections, and culture assays in axenic and cell media to check for the viability of C. burnetii excreted by ticks. We observed typical traits associated with vector competence: The exposure to an infected blood meal resulted in viable and persistent infections in ticks, trans-stadial transmissions of infection from nymphs to adults and the ability of adult ticks to transmit infectious C. burnetii. However, in contrast to early studies, we found that infection differed substantially between tick organs. In addition, while adult female ticks were infected, we did not observe C. burnetii in eggs, suggesting that transovarial transmission is not effective. Finally, we detected only a sporadic presence of C. burnetii DNA in tick faeces, but no living bacterium was further isolated in culture assays, suggesting that excretion in faeces is not a common mode of transmission in O. moubata.

Lifestyle transitions in endosymbiosis

“…We detected the Dot/Icm T4SS (or signatures of it) in all Coxiellaceae, including the environmental Coxiella MAGs, confirming its universal presence across this family (Brenner et al, 2021). While most Coxiella-LEs have lost all relevant genes, some pseudogenes are still detectable in Coxiella-LEs from Ornithodoros soft (Brenner et al (2021) and this work) and hard ticks lineages (Buysse, Duhayon, et al, 2021;Gottlieb et al, 2015). Similar to mon, et al, 2016;Oakeson et al, 2014;Yamamura, 1993).…”

Genomic Changes During the Evolution of theCoxiellaGenus Along the Parasitism-Mutualism Continuum

“…We detected the Dot/Icm SS (or signatures of it) in all Coxiellaceae, including the environmental Coxiella MAGs, confirming its universal presence across this family (Brenner et al, 2021). While most Coxiella-LEs have lost all relevant genes, some pseudogenes are still detectable in Coxiella-LEs from Ornithodoros soft (Brenner et al (2021) and this work) and hard ticks lineages (Buysse, Duhayon, et al, 2021;Gottlieb et al, 2015). Similar to Brenner et al (2021), we conclude that the C. burnetii/Coxiella-LE MRCA encoded a functional Dot/Icm SS and was able to parasitize different hosts, including amoeba (La Scola and Raoult, 2001).…”

Impact of endosymbionts on tick physiology and fitness

“…Relatedly, another aspect of tick biology that we do not fully understand is how CEs and FEs evolved from pathogenic ancestors (Gerhart et al ., 2016 ; Brenner et al ., 2021 ). For example, pathogens such as C. burnetii and F. tularensis are not vertically transmitted (Genchi et al ., 2015 ; Buysse et al ., 2021 a ), but maternal transmission is a critical step in endosymbiosis. Thus, understanding how this process arose and is maintained in ticks would provide new insights into the biology of highly integrated tick–endosymbiont systems.…”