Abstract

Ixodes persulcatus, Ixodes pavlovskyi, and Dermacentor reticulatus ticks inhabiting Western Siberia are responsible for the transmission of a number of etiological agents that cause human and animal tick-borne diseases. Because these ticks are abundant in the suburbs of large cities, agricultural areas, and popular tourist sites and frequently attack people and livestock, data regarding the microbiomes of these organisms are required. Using metagenomic 16S profiling, we evaluate bacterial communities associated with I. persulcatus, I. pavlovskyi, and D. reticulatus ticks collected from the Novosibirsk region of Russia. A total of 1214 ticks were used for this study. DNA extracted from the ticks was pooled according to tick species and sex. Sequencing of the V3-V5 domains of 16S rRNA genes was performed using the Illumina Miseq platform. The following bacterial genera were prevalent in the examined communities: Acinetobacter (all three tick species), Rickettsia (I. persulcatus and D. reticulatus) and Francisella (D. reticulatus). B. burgdorferi sensu lato and B. miyamotoi sequences were detected in I. persulcatus and I. pavlovskyi but not in D. reticulatus ticks. The pooled samples of all tick species studied contained bacteria from the Anaplasmataceae family, although their occurrence was low. DNA from A. phagocytophilum and Candidatus Neoehrlichia mikurensis was first observed in I. pavlovskyi ticks. Significant inter-species differences in the number of bacterial taxa as well as intra-species diversity related to tick sex were observed. The bacterial communities associated with the I. pavlovskyi ticks displayed a higher biodiversity compared with those of the I. persulcatus and D. reticulatus ticks. Bacterial community structure was also diverse across the studied tick species, as shown by permutational analysis of variance using the Bray-Curtis dissimilarity metric (p = 0.002). Between-sex variation was confirmed by PERMANOVA testing in I. persulcatus (p = 0.042) and I. pavlovskyi (p = 0.042) ticks. Our study indicated that 16S metagenomic profiling could be used for rapid assessment of the occurrence of medically important bacteria in tick populations inhabiting different natural biotopes and therefore the epidemic danger of studied foci.

Highlights

  • Ticks belonging to the genera Ixodes and Dermacentor are capable of transmitting a number of bacteria and viruses to humans, including causative agents of Lyme disease, rickettsioses, ehrlichioses, relapsing fever borreliosis, tularemia, Q fever, and tick-borne encephalitis [1,2,3]

  • Since the beginning of this century, I. pavlovskyi ticks have been abundant in the green belts of the Novosibirsk and Tomsk cities, which are located more northward in the Western Siberian Plain, and currently, this tick species is more prevalent compared with the I. persulcatus ticks and accounts for 82 and 90% of the collected samples, respectively [17,18,19]

  • I. persulcatus, I. pavlovskyi, and D. reticulatus are abundant in the green belts of large Siberian cities, agricultural areas, and popular tourist sites, and little is currently known about the bacterial communities associated with these ticks which are able to transmit a number of infectious agents and frequently attack people and home animals, so the goal of this study was to assess the taxonomic structure of I. persulcatus, I. pavlovskyi, and D. reticulatus microbiomes using high-throughput sequencing

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Summary

Introduction

Ticks belonging to the genera Ixodes and Dermacentor (the family Ixodidae) are capable of transmitting a number of bacteria and viruses to humans, including causative agents of Lyme disease, rickettsioses, ehrlichioses, relapsing fever borreliosis, tularemia, Q fever, and tick-borne encephalitis [1,2,3]. In Western Siberia, I. persulcatus ticks are the main vector for tick-borne encephalitis and Kemerovo viruses [4,5,6] and many bacterial agents including Borrelia burgdorferi sensu lato, B. miyamotoi, “Candidatus Rickettsia tarasevichiae”, Anaplasma phagocytophilum, Ehrlichia muris, and Bartonella spp. Analysis of the 16S rRNA gene sequences allows for phylotyping of the prokaryotes, including the organisms unable to be cultivated [24], which is especially important when analyzing symbiotic communities This approach has been successfully used to examine the I. ricinus microbiome and allowed for the detection of various infectious agents within this species, including Borrelia species, Rickettsia spp., A. phagocytophilum, Ehrlichia spp., and “Candidatus Neoehrlichia mikurensis” [25,26,27]. This study indicated that bacterial communities in tick microbiomes were different between tick species [30]

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