Lizard feeding enhances Ixodes pacificus vector competency to Borrelia burgdorferi

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Kacie Ring, Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA, Lisa I. Couper, Biology, Stanford University, Palo Alto, CA, Anne L. Sapiro, Biochemistry, University Of California, San Francisco, San Francisco, CA, Fauna Yarza, Biomedical sciences, University Of California, San Francisco, San Francisco, CA, Frank X Yang, School of Medicine, Indiana University, Keith Clay, Biology, Indiana University, Bloomington, IN, Seemay Chou, Biochemistry & Biophysics, University Of California, San Francisco, San Francisco, CA and Andrea Swei, Biology, San Francisco State University, San Francisco, CA

Background/Question/Methods
Vector competency, or a vector’s susceptibility and subsequent ability to transmit a pathogen, determines disease outcomes, yet the ecological factors influencing tick vector competence remain largely unknown. The tick vector of Borrelia burgdorferi (B.b.), the etiological agent of Lyme disease, in the western US, Ixodes pacificus, feeds predominately on two hosts, mice, Peromyscus spp, and the western fence lizard, Sceloporus occidentalis. While mice are reservoirs for B.b. and can infect juvenile ticks, lizards cannot. Specifically, the lizard bloodmeal is B.b-refractory and has been shown to significantly reduce microbiome diversity in I. pacificus after feeding. Here, we investigate the role of larval host bloodmeal of I. pacificus on nymphal B.b. acquisition. We used known bloodmeal-driven microbiome differences in I. pacificus, namely lizard-feeding or mouse-feeding during the larval stage, to generate naturally low or high levels of microbiome diversity, respectively. In the next life stage, we fed nymphal ticks on B.b.-infected mice and tested for successful pathogen acquisition in engorged ticks. As a first step towards understanding the putative role of host blood on tuning tick vector competence, we took a global transcriptomic approach to identify key genes or pathways modulated by mouse or lizard hosts by conducting the first RNA-seq analysis on whole-bodied I. pacificus ticks.
Results/Conclusions
Using a host-to-tick B.b. transmission experiment on I. pacificus, we found that larval blood meal history significantly affected pathogen acquisition, a key component of vector competency. When ticks that fed on either lizards or mice as larvae fed on B.b.-infected mice as nymphs, the previously lizard-fed ticks were three times more likely to acquire the pathogen than ticks with larval mouse blood meals. Our analysis of global gene expression in I. pacificus found that lizard-feeding up-regulates tick antioxidants and antimicrobial peptides (AMPs), which may play a role in altering tick vector competency to B.b. The production of AMPs specifically, may be a key contributor to the decreased gut microbiome diversity after lizard feeding, reducing microbes that compete with B.b. colonization in future blood meals. This finding highlights that prior and current host species identity matters in blood meal and upends prior conceptions about the western fence lizard being purely a dilution host.