Tick-Borne Pathogens Shape the Native Microbiome Within Tick Vectors

Abstract

Ticks are blood-feeding arthropods and transmit a variety of medically important viral, bacterial, protozoan pathogens to animals and humans. Ticks also harbor a diverse community of microbes linked to their biological processes, such as hematophagy, and hence affect vector competence. The interactions between bacterial and/or protozoan pathogens and the tick microbiome is a black-box, and therefore we tested the hypothesis that the presence of a protozoan or bacterial pathogen will alter the microbial composition within a tick. Hence, this study was designed to define the microbial composition of two tick species, Hyalomma (H.) anatolicum and Rhipicephalus (R.) microplus. We used a combination of PCR based pathogen (Anaplasma marginale and Theileria species) and symbiont (Wolbachia species) identification followed by metagenomic sequencing and comparison of the microbial communities in PCR positive and negative ticks. A total of 1786 operational taxonomic units was identified representing 25 phyla, 50 classes, and 342 genera. The phylum Proteobacteria, Firmicutes, Actinobacteriota, and Bacteroidota were the most represented bacteria group. Alpha and beta diversity were not significantly affected in the presence or absence of Theileria sp. and A. marginale as see with H. anatolicum ticks. Interestingly, bacterial communities were significantly reduced in Theileria sp. infected R. microplus ticks, while also exhibiting a significant reduction in microbial richness and evenness. Putting these observations together, we referred to the effect the presence of Theileria sp. has on R. microplus a “pathogen-induced dysbiosis”. We also identify the presence of Plasmodium falciparum, the causative agent of human malaria from the microbiome of both H. anatolicum and R. microplus ticks. These findings support the presence of a “pathogen-induced dysbiosis” within the tick and further validation experiments are required to investigate how they are important in the vector competence of ticks. Understanding the mechanism of “pathogen-induced dysbiosis” on tick microbial composition may aid the discovery of intervention strategies for the control of emerging tick-borne infections.

Update on the intricate tango between tick microbiomes and tick‐borne pathogens

“…34,[81][82][83] Similarly, several Ornithodoros, Rhipicephalus and Amblyomma species are known to host Coxiellalike endosymbionts, 49,77,80,[84][85][86][87][88][89][90][91][92][93] in contrast to FLEs endosymbionts which are frequently identified in Hyalomma and Amblyomma tick species. 45,[47][48][49]94,95 Furthermore, as already observed for pathogens, [96][97][98][99] other members of the tick microbial community are dynamic and likely to vary with time. However, only a few long-term studies have investigated potential seasonal or annual patterns in tick microbiomes.…”

“…ticks, as highlighted in recent studies. 36,[45][46][47][48][49] At a finer scale, FLEs have been detected in large numbers in the ovaries and Malpighian tubules of the host ticks. 44…”

“…As an example, Clostridium is a common environmental bacterium detected in various Ixodid tick species. [70][71][72][73] While other environmentally acquired microbes such as Bacillus, Pseudomonas and Enterobacteriaceae might influence the presence of some pathogens in Ixodes ticks, 47,50,74 these microbes are not reliably vertically transmitted, and their ability to persist in the tick during moulting is unknown. Because we know that symbionts play a critical role in both tick physiology and pathogen acquisition and that NGS techniques produce large quantities of tick symbiont sequences, many studies have therefore focused their scientific questions and objectives on tick symbionts.…”

Multi‐country investigation of the diversity and associated microorganisms isolated from tick species from domestic animals, wildlife and vegetation in selected african countries

“…These results confirm the lability of the bacterial community structure hosted by this tick species, much differently that what seen in most other species (Duron et al 2017 ). There are various possible explanations, such as the influence of multiple ecological and geographical factors (Lalzar et al 2014 ; Abraham et al 2017 ; Bonnet et al 2017 ) as well as the host-feeding behavior of the ticks, the host’s immune system and the direct interaction of protozoan or bacterial pathogens (Adegoke et al 2020 ; Aivelo et al 2019 ; Hawley and Altizer 2011 ). Alternatively, or in conjunction, the possibility that the analysed individuals belong to different sibling species of the Rh.…”

Anti‐tick and pathogen transmission blocking vaccines

“…Recognizing the tick-host interface as playing an integral role in pathogen transmission, efforts focused on sequencing of tick genomes, proteomics analysis of tick saliva proteins and tick microbiome analysis are providing novel means to combat tick-borne diseases. [14][15][16][17] Studies with timed exposure to naïve and infected ticks have revealed a transient transcriptomic profile throughout the tick feeding cycle, in part regulated by pathogens residing in the saliva/ gut of the tick. In Ixodes scapularis nymphs, transcripts regulating water and ion movement were found to be upregulated throughout the first three days of feeding, whereas secreted attachment and salivary transcripts were most strongly upregulated during the first 24hrs.…”