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 were or were not 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 quantitative polymerase chain reaction (qPCR), 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 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 CandidatusMidichloria mitochondrii. Results With the exception of Rickettsiella spp., all microorganisms 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 with each other. 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 have a large effect on 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 herein and merit further investigation. Graphical Abstract

Deep sequencing of 16Ixodes ricinusticks unveils insights into their interactions with endosymbionts

“…For example, Rickettsia has been shown to enhance tick motility in Dermacentor variabilis [106]. Secondly, the possibility of interactions with other symbionts within the tick host should be explored as R. helvetica has been shown to modulate the microbiome of I. ricinus [107] and it has been found to be negatively correlated with certain symbionts such as Spiroplasma ixodetis and M. mitochondrii [31, 2]. It has been hypothesised that perhaps the biological roles of S. ixodetis and R. helvetica overlap, making their simultaneous maintenance energetically superfluous for the tick host [31], but this theory has yet to be proven.…”

“…The most common tick-borne diseases associated with I. ricinus are Lyme disease (LB) which is caused by Borrelia burgdorferi sensu lato and tick-borne encephalitis (TBE), which is caused by tick-borne encephalitis virus [1]. In addition, I. ricinus transmits several emerging pathogens such as Rickettsia helvetica , Anaplasma phagocytophilum , Borrelia miyamotoi , Neoehrlichia mikurensis , and several Babesia species [2]. Infections with these pathogens have been associated with human disease in cross-sectional and case studies, but their pathogenic potential has not been fully understood [3, 4].…”

Changes in the Ixodes ricinus microbiome associated with artificial tick feeding

“…This negative association is suggestive of competition or niche partitioning between Spiroplasma and R . helvetica ( Krawczyk et al, 2022a , b ).…”

“…The same negative association was found in a previous study in which nearly 14,000 questing I . ricinus nymphs were screened by qPCR for tick-associated microorganisms ( Krawczyk et al, 2022b ). In contrast, other studies reported a positive association between Midichloria and Rickettsia spp., both in questing ticks and ticks collected from humans ( Budachetri et al, 2018 ; Lejal et al, 2021 ; Maitre et al, 2022 ).…”

Another tick bites the dust: exploring the association of microbial composition with a broad transmission competence of tick vector species

“…This bacterial genus is closely related to symbionts such as Midichloria mitochondrii . This species has been recently demonstrated to be positively associated with B. burgdorferi and Neoehrlichia mikurensis while being negatively associated with A. phagocytophilum ( 24 ). However, a method has been used which modeled co-occurrence of bacteria based on the chance of these bacteria being present together with M. mitochondrii .…”