Tick-microbe interactions and virome transmission in Ixodes persulcatus and Dermacentor silvarum

Abstract

Ticks are versatile vectors of pathogens and affect livestock and humans worldwide. The wide host spectrum and long-lasting blood feeding of ticks are believed to facilitate the transmission of many pathogenic microbes identified in them. This thesis aims to investigate the interactions among ticks, their microbiome, and their hosts, through metagenomic and meta-transcriptomic analyses. The research focused on the vertical and horizontal transmission of pathogens carried by Ixodes persulcatus and Dermacentor silvarum ticks and the related changes in their microbiomes during development and investigates the extent of their virome. The research aims to generate new knowledge of tick interaction with microbes to combat tick-borne pathogens.

Tick colonies carrying out experimental vertical transmission of pathogenic Rickettsia in laboratory was studied for the microbiome change in different life stages. In pathogenic Rickettsia infected colonies of both tick species the diversity of the microbiome was relatively stable across life stages, with significantly higher egg hatched rate. Notably infected D. silvarum has significantly higher microbiome diversity than the uninfected colonies. These findings suggest that the diversity of tick microbiome might have positive correlations with the vertical transmission of pathogens.

Variations in the microbiome and response of ticks under different natural blood-meal conditions were studied by metagenomic and meta-transcriptomic analysis. The results suggest bacterial diversity and the level of antimicrobial peptides increased with the duration of the blood meal, while reactive oxygen species decreased which might avoid heme-mediated oxidative stress in the ticks during the blood meal process. In addition, nine viruses with distant similarity to previously reported viruses were discovered, and the COX1 genes of five animals, including bats, were identified. These finding indicate potential threats to public health and a wide range of sources for potential pathogens.

Horizontal transmission of microbes between ticks and patients was studied by examining the microbial compositions in ticks, at patient tick-bite sites and in patient’s blood. Pseudomonas and Acinetobacter were found in all tick-patient cases while Rickettsia, Coxiella, and Roseomonas were also found to infect patients. The Jingmen tick virus was found on skin and blood, and Suffolk virus was found on skin, indicating a potential risk to public health. The skin meta-transcriptomics analysis at the tick-bite site showed down-regulation of the bacterial vitamin metabolism and immune pathways, which might favor transmission of tick-borne pathogens.

Large-scale meta-transcriptomic analyses of I. persulcatus and D. silvarum revealed their different virome compositions with unique core viruses. The composition of the virome was not affected by gender but by ecology found in D.silvarum. The total of 107 novel viruses from 10 families related to vertebrate, plant and fungal viruses were identified, highlighting the wide spectrum of vector competence in these two tick species.

This thesis has identified new roles for and novel components of the tick microbiome and virome. Many potential pathogens were identified, emphasizing the public health risks associated with ticks and the need for ongoing surveillance. The microbial pathways and compositional changes in tick microbiomes identified here open new opportunities for the control measures.