Temporal patterns inIxodes ricinusmicrobial communities: an insight into tick-borne microbe interactions

Abstract

BackgroundTicks transmit pathogens of medical and veterinary importance, and represent an increasing threat for human and animal health. Important steps in assessing disease risk and developing possible new future control strategies involve identifying tick-borne microbes, their temporal dynamics and interactions.MethodsUsing high throughput sequencing, we studied the microbiota dynamics of Ixodes ricinus from 371 nymphs collected monthly over three consecutive years in a peri-urban forest. After adjusting a Poisson Log Normal model to our data set, the implementation of a principal component analysis as well as sparse network reconstruction and differential analysis allowed us to assess inter-annual, seasonal and monthly variability of I. ricinus microbial communities as well as their interactions.ResultsAround 75% of the detected sequences belonged to five genera known to be maternally inherited bacteria in arthropods and potentially circulating in ticks: Candidatus Midichloria, Rickettsia, Spiroplasma, Arsenophonus and Wolbachia. The structure of the I. ricinus microbiota was temporally variable with interannual recurrence and seemed to be mainly driven by OTUs belonging to environmental genera. The total network analysis revealed a majority of positive (partial) correlations. We identified strong relationships between OTUs belonging to Wolbachia and Arsenophonus, betraying the presence of the parasitoid wasp Ixodiphagus hookeri in ticks, and the well known arthropod symbiont Spiroplasma, previously documented to be involved in the defense against parasitoid wasp in Drosophila melanogaster. Other associations were observed between the tick symbiont Candidatus Midichloria and pathogens belonging to Rickettsia, probably Rickettsia helvetica. More specific network analysis finally suggested that the presence of pathogens belonging to genera Borrelia, Anaplasma and Rickettsia might disrupt microbial interactions in I. ricinus.ConclusionsHere, we identified the I. ricinus microbiota and documented for the first time the existence and recurrence of marked temporal shifts in the tick microbial community dynamics. We statistically showed strong relationships between the presence of some pathogens and the structure of the I. ricinus non-pathogenic microbes. We interestingly detected close links between some tick symbionts and the potential presence of either pathogenic Rickettsia or a parasitoid in ticks. All these new findings might be very promising for the future development of new control strategies of ticks and tick-borne diseases.

Update on the intricate tango between tick microbiomes and tick‐borne pathogens

“…111,112 It is important to note here that several studies have demonstrated that microbial communities in female ticks were frequently less diverse than in males and that microbial composition varied according to tick sex. 50,76,105,106 Finally, and as has already been emphasized by Pollet et al, 75 while endosymbionts are mainly known to be vertically transmitted to progeny and thus be strongly detected in tick ovaries, 70,113 multiple studies suggest their presence in other tick organs such as Malpighian tubules, salivary glands or the midgut. 6,84,86,[114][115][116] Clear variations in tick microbial communities can be observed according to the anatomical region within the tick when comparing these studies.…”

“…densities. 86 Similarly, Lejal et al 50 documented the existence and annual recurrence of marked temporal shifts in tick microbial community dynamics in I ricinus. Excluding results from Clow et al, 72 prior works also demonstrated the strong influence of biogeography on tick microbiome structure and composition from different tick species, both at state or regional scales 71,76,91,100-102 and at more local scales, between ticks collected from either the forest or the ecotone.…”

“…36 However, it has recently been identified as the most abundant bacterial endosymbiont in the soft tick O turicata, collected on Bolson tortoises. 40 This endosymbiont is also particularly common to Ixodes ricinus, 25,50 with wild adult females regularly found to have greater infection prevalence than males, 51,52 suggesting a nutritional role, as only females take a blood meal in this tick species, 36 or a role during the egg-laying as an additional ATP source for the host cell during oogenesis. 53 The bacterium has also been ascribed a possible helper role in tick moulting processes.…”

“…As an example, Clostridium is a common environmental bacterium detected in various Ixodid tick species. [70][71][72][73] While other environmentally acquired microbes such as Bacillus, Pseudomonas and Enterobacteriaceae might influence the presence of some pathogens in Ixodes ticks, 47,50,74 these microbes are not reliably vertically transmitted, and their ability to persist in the tick during moulting is unknown. Because we know that symbionts play a critical role in both tick physiology and pathogen acquisition and that NGS techniques produce large quantities of tick symbiont sequences, many studies have therefore focused their scientific questions and objectives on tick symbionts.…”

“…74,76 While several endosymbionts such as C M. mitochondrii, CLEs and Rickettsiella sp. are known to inhabit I ricinus, I hexagonus and Ixodes uriae ticks, 23,36,50,71,[77][78][79][80] FLEs and Rickettsia-like are more often detected in Ixodes scapularis and Dermacentor species. 34,[81][82][83] Similarly, several Ornithodoros, Rhipicephalus and Amblyomma species are known to host Coxiellalike endosymbionts, 49,77,80,[84][85][86][87][88][89][90][91][92][93] in contrast to FLEs endosymbionts which are frequently identified in Hyalomma and Amblyomma tick species.…”