Francisella-Like Endosymbionts and Rickettsia Species in Local and Imported Hyalomma Ticks

Abstract

<i>Hyalomma</i> ticks (Acari: Ixodidae) are hosts for <i>Francisella</i>-like endosymbionts (FLE) and may serve as vectors of zoonotic disease agents. This study aimed to provide an initial characterization of the interaction between <i>Hyalomma</i> and FLE and to determine the prevalence of pathogenic <i>Rickettsia</i> in these ticks. <i>Hyalomma marginatum</i>, <i>Hyalomma rufipes</i>, <i>Hyalomma</i><i>dromedarii</i>, <i>Hyalomma</i><i>aegyptium</i>, and <i>Hyalomma</i><i>excavatum</i> ticks, identified morphologically and molecularly, were collected from different hosts and locations representing the distribution of the genus <i>Hyalomma</i> in Israel, as well as from migratory birds. A high prevalence of FLE was found in all <i>Hyalomma</i> species (90.6%), as well as efficient maternal transmission of FLE (91.8%), and the localization of FLE in Malpighian tubules, ovaries, and salivary glands in <i>H. marginatum</i> Furthermore, we demonstrated strong cophylogeny between FLE and their host species. Contrary to FLE, the prevalence of <i>Rickettsia</i> ranged from 2.4% to 81.3% and was significantly different between <i>Hyalomma</i> species, with a higher prevalence in ticks collected from migratory birds. Using <i>ompA</i> gene sequences, most of the <i>Rickettsia</i> spp. were similar to <i>Rickettsia</i><i>aeschlimannii</i>, while a few were similar to <i>Rickettsia</i><i>africae</i> of the spotted fever group (SFG). Given their zoonotic importance, 249 ticks were tested for Crimean Congo hemorrhagic fever virus infection, and all were negative. The results imply that <i>Hyalomma</i> and FLE have obligatory symbiotic interactions, indicating a potential SFG <i>Rickettsia</i> zoonosis risk. A further understanding of the possible influence of FLE on <i>Hyalomma</i> development, as well as on its infection with <i>Rickettsia</i> pathogens, may lead to novel ways to control tick-borne zoonoses.<b>IMPORTANCE</b> This study shows that <i>Francisella</i>-like endosymbionts were ubiquitous in <i>Hyalomma</i>, were maternally transmitted, and cospeciated with their hosts. These findings imply that the interaction between FLE and <i>Hyalomma</i> is of an obligatory nature. It provides an example of an integrative taxonomy approach to simply differentiate among species infesting the same host and to identify nymphal and larval stages to be used in further studies. In addition, it shows the potential of imported <i>Hyalomma</i> ticks to serve as a vector for spotted fever group rickettsiae. The information gathered in this study can be further implemented in the development of symbiont-based disease control strategies for the benefit of human health.