Combining Citizen Science and Genomics to Investigate Tick, Pathogen, and Commensal Microbiome at Single-Tick Resolution

Abstract

The prevalence of tickborne diseases worldwide is increasing virtually unchecked due to the lack of effective control strategies. The transmission dynamics of tickborne pathogens are influenced by the tick microbiome, tick co-infection with other pathogens, and environmental features. Understanding this complex system could lead to new strategies for pathogen control, but will require large-scale, high-resolution data. Here, we introduce Project Acari, a citizen science-based project to assay, at single-tick resolution, species, pathogen infection status, microbiome profile, and environmental conditions of tens of thousands of ticks collected from numerous sites across the United States. In the first phase of the project, we collected more than 2,400 ticks wild-caught by citizen scientists and developed high-throughput methods to process and sequence them individually. Applying these methods to 192 Ixodes scapularis ticks collected in a region with a high incidence of Lyme disease, we found that 62% were colonized by Borrelia burgdorferi, the Lyme disease pathogen. In contrast to previous reports, we did not find an association between the microbiome diversity of a tick and its probability of carrying B. burgdorferi. However, we did find undescribed associations between B. burgdorferi carriage and the presence of specific microbial taxa within individual ticks. Our findings underscore the power of coupling citizen science with highthroughput processing to reveal pathogen dynamics. Our approach can be extended for massively parallel screening of individual ticks, offering a powerful tool to elucidate the ecology of tickborne disease and to guide pathogen-control initiatives.

Microbiome Composition and Borrelia Detection in Ixodes scapularis Ticks at the Northwestern Edge of Their Range

“…In contrast to our results, three recent studies have shown no significant difference in bacterial diversity associated with Borrelia infection status [ 58 , 73 , 74 ], and a fourth study was ambiguous [ 28 ]. However, one of these studies reported results for a mix of females and males [ 73 ], which would have increased the variance in an already noisy system [ 17 ]. A second study [ 74 ] analyzed nymphs of Ixodes pacificu s and found no significant differences in richness or evenness.…”

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

“…This strongly influences the final result, as prior to computationally removing the Rickettsia symbiont in the former study, Kwan et al 107 also did not observe significant differences in either species richness or evenness. This latest observation was recently confirmed by Chauhan et al 122 which analysed the microbial communities of I scapularis collected via citizen scientific approaches in the USA. They did not find any association between the microbiome diversity of a tick and its probability of carrying B burgdorferi .…”

Grappling with the tick microbiome

“…Many microbiome studies have documented a pattern of increasing relative abundance of endosymbionts through development of Ixodes spp. from larva, to nymph, to adult stages [35,47,[55][56][57]. Rickettsia accumulation by adult female ticks is thought to be an adaptation to facilitate transovarial transmission of the endosymbiont to eggs, underlining the importance of endosymbionts to tick survival and development [46,51,58].…”

“…In multiple studies of I. scapularis that examined the relative abundance within sequenced 16S rRNA amplicons, adult female ticks were observed to exhibit a higher proportion of Rickettsia endosymbionts than males and to have lower microbiome diversity as measured by Shannon diversity or overall richness [35,47,55,56]. However, Tokarz et al performed detailed qPCR analysis of male and female ticks separately and did not observe significant differences in bacterial abundance between male and female I. scapularis [47].…”