Tick microbial associations at the crossroad of horizontal and vertical transmission pathways

Abstract

Background: Microbial communities can affect disease risk by interfering with the transmission or maintenance of pathogens in blood-feeding arthropods. Here, we investigated whether bacterial communities vary between Ixodes ricinus nymphs, which are (un)infected with horizontally-transmitted human pathogens. Methods: Ticks from eight forest sites were tested for the presence of Borrelia burgdorferi sensu lato, Babesia spp., Anaplasma phagocytophilum, and Neoehrlichia mikurensis by qPCR, pooled, and their microbiomes were determined by 16S rRNA amplicon sequencing. Tick bacterial communities clustered poorly by pathogen infection status but better by geography. As a second approach, we analysed variation in tick microorganism community structure (in terms of species co-infection) across space using hierarchical modelling of species communities. For that, we analysed almost 14,000 nymphs, which were tested with targeted qPCR for the presence of horizontally-transmitted pathogens B. burgdorferi s.l., A. phagocytophilum, and N. mikurensis, and the vertically-transmitted tick symbionts Rickettsia helvetica, Rickettsiella spp., Spiroplasma ixodetis and Midichloria mitochondrii. Results: All microorganisms but Rickettsiella spp. had either significant negative (R. helvetica and A. phagocytophilum) or positive (S. ixodetis, N. mikurensis, and B. burgdorferi s.l.) associations with M. mitochondrii. Two tick symbionts, R. helvetica and S. ixodetis, were negatively associated. As expected, both B. burgdorferi s.l. and N. mikurensis had a significant positive association with each other and a negative association with A. phagocytophilum. Although these few specific associations do not appear to affect much the entire microbiome composition, they can still be relevant for tick-borne pathogen dynamics. Conclusions: Based on our results, we propose that M. mitochondrii alters the propensity of ticks to acquire or maintain horizontally-acquired pathogens. The underlying mechanisms for some of these remarkable interactions are discussed and merit further investigation.

No evidence for a dilution effect of high vertebrate diversity on tick-borne disease hazard in Dutch forests

“…[42] and Midichloria midichondrii [43]. Although the transmission of symbionts preliminary relies on vertical transmission, most, if not all, are also transmitted horizontally, and thus may be affected by vertebrate community composition [44]. In a previous study, we monitored wildlife communities from 19 forest sites by camera trapping and live-trapping [13,45,46].…”