Detection of tick-borne bacteria and babesia with zoonotic potential in Argas (Carios) vespertilionis (Latreille, 1802) ticks from British bats

Abstract

Ticks host a wide range of zoonotic pathogens and are a significant source of diseases that affect humans and livestock. However, little is known about the pathogens associated with bat ticks. We have collected ectoparasites from bat carcasses over a seven year period. Nucleic acids (DNA and RNA) were extracted from 296 ticks removed from bats and the species designation was confirmed in all ticks as Argas (Carios) vespertilionis. A subset of these samples (n = 120) were tested for the presence of zoonotic pathogens by molecular methods. Babesia species, Rickettsia spp., within the spotted fever group (SFG), and Ehrlichia spp. were detected in ticks removed from 26 bats submitted from 14 counties across England. The prevalence of Rickettsia spp. was found to be highest in Pipistrellus pipistrellus from southern England. This study suggests that the tick species that host B. venatorum may include the genus Argas in addition to the genus Ixodes. As A. vespertilionis has been reported to feed on humans, detection of B. venatorum and SFG Rickettsia spp. could present a risk of disease transmission in England. No evidence for the presence of flaviviruses or Issyk-Kul virus (nairovirus) was found in these tick samples.

Figure 1

Map of Great Britain showing locations where bats were submitted and the ectoparasites sampled. The collection sites for bat ticks are marked with yellow dots, for other parasites such as fleas and mites with black dots. Numbers in yellow or black dots indicate the number of bats sampled from each county. This figure is not included in the Creative Commons licence for the article; all rights reserved. Taken from the Beijing Zcool Internet Technology Co., Ltd.

Figure 2

Species identification of bat ticks through morphology and Neighbor Joining phylogenetic analyses based on COI and 16S rRNA. (A) A representative image of bat ticks removed from a UK bat. (B) Neighbor Joining phylogenetic analysis based on partial tick 16S rRNA sequence, (C) Neighbor Joining phylogenetic analysis based on partial tick COI sequence. Bootstrap values are indicated at the nodes. Scale bar indicates the degree of divergence represented by a given length of branch. The red dots indicate the sequences acquired in this study.

Figure 3

Detection and analysis of piroplasm DNA detected in ticks removed from UK bats. (A) Map showing the sampling sites of piroplasm-positive bat ticks. The red dot indicates the site of B. vesperuginis positive A. vespertilionis and the blue dot indicates the site of B. venatorum positive A. vesperitilionis. This figure is not included in the Creative Commons licence for the article; all rights reserved. Taken from Beijing Zcool Internet Technology Co., Ltd. (B) Neighbor Joining phylogenetic analysis based on partial 18S rRNA sequence of Babesia spp. Bootstrap values are indicated at the nodes. Scale bar indicates the degree of divergence represented by a given length of branch. The red dot indicates the sequence of B. vesperuginis and the blue dot indicates the sequence of B. venatorum acquired in this study.

Figure 4

Detection and analysis of Rickettsia spp. from UK bat ticks. (A) Map showing the sampling sites of Rickettsia spp. positive bat ticks. The red dots indicate the sites of Rickettsia spp positive A. vespertilionis. This figure is not included in the Creative Commons licence for the article; all rights reserved. Taken from Beijing Zcool Internet Technology Co., Ltd. (B) Neighbor Joining phylogenetic analysis based on a partial sequence of the 17 K Da protein gene of Rickettsia spp. Bootstrap values are indicated at the nodes. Scale bar indicates the degree of divergence represented by a given length of branch. The red dot indicates the sequence of Rickettsia spp. acquired in this study. Numbers in red dots indicate the number of bats with Rickettsia spp. positive ticks, sampled from each county.

Figure 5

Detection and analysis of Ehrlichia/Anaplasma spp. from UK bat ticks. (A) Map showing the sampling sites of Ehrlichia spp. positive A. vespertilionis (yellow dots). This figure is not included in the Creative Commons licence for the article; all rights reserved. Taken from Beijing Zcool Internet Technology Co., Ltd. (B) Neighbor Joining phylogenetic analysis based on a partial 16S rRNA sequence of Ehrlichia spp. Bootstrap values are indicated at the nodes. Scale bar indicates the degree of divergence represented by a given length of branch. The yellow dot indicates the sequence of Ehrlichia spp. acquired in this study.