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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 Candidatus Midichloria 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 Positive and negative associations between and within horizontally and vertically transmitted symbionts

Abstract Background Borrelia miyamotoi is a spirochete transmitted by several ixodid tick species. It causes a relapsing fever in humans and is currently considered as an emerging pathogen. In Europe, B. miyamotoi seems to occur at low prevalence in Ixodes ricinus ticks but has a wide distribution. Here we report the first detection of B. miyamotoi in Ixodes ricinus ticks collected in two independent studies conducted in 2016 in the north-eastern and north-western Alps, Italy. Results Three out of 405 nymphs (0.74%) tested positive for Borrelia miyamotoi. In particular, B. miyamotoi was found in 2/365 nymphs in the western and in 1/40 nymphs in the eastern alpine area. These are the first findings of B. miyamotoi in Italy. Conclusions Exposure to B. miyamotoi and risk of human infection may occur through tick bites in northern Italy. Relapsing fever caused by Borrelia miyamotoi has not yet been reported in Italy, but misdiagnoses with tick-borne encephalitis, human granulocytic anaplasmosis or other relapsing fever can occur. Our findings suggest that B. miyamotoi should be considered in the differential diagnosis of febrile patients originating from Lyme borreliosis endemic regions. The distribution of this pathogen and its relevance to public health need further investigation.