Abstract
The identification of micro-organisms carried by ticks is an important issue for human and animal health. In addition to their role as pathogen vectors, ticks are also the hosts for symbiotic bacteria whose impact on tick biology is poorly known. Among these, the bacterium Wolbachia pipientis has already been reported associated with Ixodes ricinus and other tick species. However, the origins of Wolbachia in ticks and their consequences on tick biology (known to be very diverse in invertebrates, ranging from nutritional symbionts in nematodes to reproductive manipulators in insects) are unknown. Here we report that the endoparasitoid wasp Ixodiphagus hookeri (Hymenoptera, Chalcidoidea, Encyrtidae) – strictly associated with ticks for their development - is infested at almost 100% prevalence by a W. pipientis strain belonging to a Wolbachia supergroup that has already been reported as associated with other hymenopteran parasitoids. In a natural population of I. ricinus that suffers high parasitism rates due to I. hookeri, we used specific PCR primers for both hymenopteran and W. pipientis gene fragments to show that all unfed tick nymphs parasitized by I. hookeri also harbored Wolbachia, while unparasitized ticks were Wolbachia-free. We demonstrated experimentally that unfed nymphs obtained from larvae exposed to I. hookeri while gorging on their vertebrate host also harbor Wolbachia. We hypothesize that previous studies that have reported W. pipientis in ticks are due to the cryptic presence of the endoparasitoid wasp I. hookeri. This association has remained hidden until now because parasitoids within ticks cannot be detected until engorgement of the nymphs brings the wasp eggs out of diapause. Finally, we discuss the consequences of this finding for our understanding of the tick microbiome, and their possible role in horizontal gene transfer among pathogenic and symbiotic bacteria.
Highlights
As ticks are considered to be second only to mosquitoes as vectors of human infectious diseases in the world, the identification of micro-organisms carried by ticks is an important issue for human or animal health [1]
The parasitoid Ixodiphagus hookeri harbors endosymbiotic Wolbachia pipientis Based on both (i) engorged nymphs collected on roe-deer and (ii) host-seeking nymphs collected on vegetation that were subsequently engorged in the lab, a total of 54 ticks collected in 4 natural populations were found to be parasitized by I. hookeri (Table 2; Figure 1)
By the use of specific PCR primers for the parasitoid I. hookeri and for the endosymbiotic bacteria W. pipientis, we demonstrated that almost all (99,2%) of the I. hookeri individuals investigated, emerging from 5 different natural french populations of the tick I. ricinus, harbored W. pipientis
Summary
As ticks are considered to be second only to mosquitoes as vectors of human infectious diseases in the world, the identification of micro-organisms carried by ticks is an important issue for human or animal health [1]. While Coxiella burnetti is known as the etiological agent of the Q-Fever responsible for recent outbreaks in Europe, an unnamed Coxiella species has been found in 100% of the individuals of Amblyomma americanum [7] Antibiotic treatment of these ticks resulted in reduced reproductive fitness, suggesting that the Coxiella sp. Midichloria mitochondrii is an endosymbiotic alpha-proteobacterium found in the ovarian tissues of almost all Ixodes ricinus females from natural populations [9,10] This bacterium has a unique intramitochondrial lifestyle [11,12,13] but its consequences on tick fitness or reproduction remain unknown [13]. The recent development of metagenomic approaches on ticks will probably allow the identification of numerous new bacteria species [15,16]
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