The relapsing fever spirochete Borrelia turicatae persists in the highly oxidative environment of its soft‐bodied tick vector

Abstract

The relapsing fever spirochete Borrelia turicatae possesses a complex life cycle in its soft‐bodied tick vector, Ornithodoros turicata . Spirochetes enter the tick midgut during a blood meal, and, during the following weeks, spirochetes disseminate throughout O. turicata . A population persists in the salivary glands allowing for rapid transmission to the mammalian hosts during tick feeding. Little is known about the physiological environment within the salivary glands acini in which B. turicatae persists. In this study, we examined the salivary gland transcriptome of O. turicata ticks and detected the expression of 57 genes involved in oxidant metabolism or antioxidant defences. We confirmed the expression of five of the most highly expressed genes, including glutathione peroxidase ( gpx ), thioredoxin peroxidase ( tpx ), manganese superoxide dismutase ( sod‐1 ), copper‐zinc superoxide dismutase ( sod‐2 ), and catalase ( cat ) by reverse‐transcriptase droplet digital polymerase chain reaction (RT‐ddPCR). We also found distinct differences in the expression of these genes when comparing the salivary glands and midguts of unfed O. turicata ticks. Our results indicate that the salivary glands of unfed O. turicata nymphs are highly oxidative environments where reactive oxygen species (ROS) predominate, whereas midgut tissues comprise a primarily nitrosative environment where nitric oxide synthase is highly expressed. Additionally, B. turicatae was found to be hyperresistant to ROS compared with the Lyme disease spirochete Borrelia burgdorferi , suggesting it is uniquely adapted to the highly oxidative environment of O. turicata salivary gland acini.

Differential Expression of Putative Ornithodoros turicata Defensins Mediated by Tick Feeding

“…O. turicata defensins were identified from our previously reported salivary gland transcriptome (Bourret et al, 2019). The transcriptome was analyzed to select transcripts that were annotated as defensins.…”

“…We evaluated the O. turicata salivary gland transcriptome (Bourret et al, 2019) with the goal of identifying defensin transcripts. Through this analysis we identified five candidates.…”

“…Ornithodoros species are also unique from other tick genera because they live for 10-20 years and can endure over 5 years of starvation and still remain competent vectors (Davis, 1943;Assous and Wilamowski, 2009). Recently, physiological differences were detected between the midgut and salivary glands of O. turicata, which revealed selective pressures that pathogens encounter in the argasid tick including reactive nitrogen and oxygen species (ROS and RNS) (Bourret et al, 2019). However, it remains vague what other immunological pressures exist in these two disparate environments.…”

“…In this study, we focused on identifying immunological pressures produced in the tick midgut and salivary glands. Since genomic and transcriptomic resources are limited for O. turicata, we utilized a salivary gland transcriptome to identify putative defensins (Bourret et al, 2019). These candidates had the characteristic six cysteine residues observed in known defensin molecules of insects and arthropods.…”

Humoral immune response of pigs, Sus scrofa domesticus, upon repeated exposure to blood-feeding by Ornithodoros turicata Duges (Ixodida: Argasidae)

“…Consequently, to improve surveillance efforts, it is important to develop an accurate molecular assay to differentiate exposure of feral swine to Ornithodoros species and ixodid ticks. With the availability of the O. turicata salivary gland transcriptome [42], future proteomic work will identify the tick salivary antigens recognized by the vertebrate immune response. This will be an important first step toward the development of a specific assay to evaluate the exposure of domestic and wild pigs to O. turicata salivary proteins.…”