Co-infections with multiple pathogens in natural populations of Ixodes persulcatus ticks in Mongolia

Abstract

Background In Mongolia, the taiga tick Ixodes persulcatus is the major vector of tick-borne pathogens. Knowledge about co-infections of these pathogens in ticks is necessary both for understanding their persistence in nature and for diagnosing and treating tick-borne diseases. Methods The prevalence of seven tick-borne infections in 346 I. persulcatus collected from the Selenge and Bulgan provinces of Mongolia was evaluated using real-time PCR. Quantification of Borrelia spp. was performed using multiplex quantitative PCR targeting the 16S rRNA gene. Genetic analysis of Borrelia spp. in 11 ticks infected with Borrelia miyamotoi, including six ticks co-infected with Borrelia burgdorferi sensu lato (s.l.), was performed by high-throughput sequencing of the flaB gene fragment. Results Six ticks (1.7%) were infected with tick-borne encephalitis virus (TBEV); 171 (49.4%), with B. burgdorferi sensu lato; 17 (4.9%), with B. miyamotoi; 47 (13.6%), with Anaplasma phagocytophilum; and 56 (16.2%), with Ehrlichia sp. Neither Rickettsia sibirica nor R. heilongjiangensis were detected. Borrelia burgdorferi s.l. occurred as co-infection in 55 (32.2%) of all infected ticks. The other pathogens co-infected ticks in 58.8–70.2% of cases. No pairwise associations between co-infecting pathogens were observed, with the exception of a positive association between A. phagocytophilum and Ehrlichia sp. infections. The spirochete loads of B. miyamotoi were significantly higher than those of B. burgdorferi s.l. (mean: 5.2 vs 4.0 log10 genome copies/tick, respectively). Ten isolates of B. miyamotoi belonged to the Siberian lineage. Borrelia burgdorferi s.l was represented by nine isolates of B. afzelii, B. bavariensis and B. garinii. Conclusions In populations of I. persulcatus inhabiting the Selenge and Bulgan provinces of Mongolia, five vector-borne pathogens, i.e. TBEV, B. burgdorferi s.l., B. miyamotoi, A. phagocytophilum and Ehrlichia sp., persist independently from each other, with the exception of A. phagocytophilum and Ehrlichia sp. which seem to share the circulation mode. The discrepancies in B. burgdorferi s.l. and B. miyamotoi prevalence and spirochete load per tick suggest that different ecological niches are occupied by Lyme disease and relapsing fever agents. High-throughput sequencing allows genetic identification of borreliae species in co-infected ticks. Graphical Abstract

Serological Analysis of IgG and IgM Antibodies against Anaplasma spp. in Various Animal Species of the Qinghai-Tibetan Plateau

“…Tick-borne pathogens (TBPs) are considered emergent because they cause severe tick-borne diseases that threaten the health of humans and animals during tick feeding [ 1 , 2 , 3 ]. Anaplasma spp.…”

Seroprevalence and risk factors of tick-borne encephalitis in Mongolia between 2016 and 2022

“…Selenge province was found to have the highest prevalence of I. persulcatus ticks carrying TBEV ( Muto et al, 2015 ; Khasnatinov et al, 2010c ; Boldbaatar et al, 2017 ).Therefore, most parts of Selenge and Bulgan provinces are high-risk TBEV infection areas ( Černý et al, 2019 ).This may be the primary reason for the high TBEV seroprevalence in Selenge (40%) and Bulgan provinces (11%) compared with that in other provinces between 2016 and 2022. Furthermore, vaccination and education interventions are mainly concentrated in the Selenge and Bulgan provinces, which have the largest population of I. persulcatus and arethe Taiga-covered parts of Mongolia ( Muto et al, 2015 ; Boldbaatar et al, 2017 ; Lagunova et al, 2022 ). This result shows that Selenge and Bulgan provinces are at a higher risk than other provinces.…”

Relapsing Review: A Research Update on <em>Borrelia miyamotoi</em>

“…There is still much to learn about the intricacies of B. miyamotoi tick colonization and transmission. France I. ricinus [77,82,83] Germany I. ricinus [72,84] Ireland I. ricinus [85] Italy I. ricinus [72] Japan I. persulcatus [4], I. ovatus [86] Moldova I. ricinus [87] Mongolia I. persulcatus [86,88] Netherlands I. ricinus [72,77,89,90] Norway I. ricinus [91] Poland I. ricinus [92,93] Portugal I. ricinus [94] Russia I. persulcatus [95] Serbia I. ricinus [96] Slovakia I. ricinus [97,98] South Korea I. nipponensis [99] Spain I. ricinus [100] Sweden I. ricinus [63,72] Switzerland I. ricinus [101] Turkey I. ricinus [102] Ukraine I. ricinus [103] United Kingdom I. ricinus [72] United States I. scapularis [104] a adapted from Hoornstra et al 2022 [27] under creative commons license CC BY 4.0.…”

“…The multiple reservoir species identified for B. miyamotoi, all of which are rodents, are Peromyscus, Apodemus, and Myodes species [65,105,108,109]. Reservoir species have been identified carrying B. miyamotoi in both rural and urban environments, posing an increased public health risk [86][87][88]. A notable potential new reservoir species in North America is the jumping mouse, Napaeozapus insignis.…”