Vector Competence of Geographical Populations of Ornithodoros turicata for the Tick-Borne Relapsing Fever Spirochete Borrelia turicatae

Abstract

Vector competence refers to the ability of an arthropod to acquire, maintain, and successfully transmit a microbial pathogen. Tick-borne relapsing fever (TBRF) spirochetes are globally distributed pathogens, and most species are transmitted by argasid ticks of the genus Ornithodoros. A defining characteristic in vector competence is an apparent specificity of a species of TBRF spirochete to a given tick species. In arid regions of the southern United States, Borrelia turicatae is the primary cause of TBRF. Interestingly, there are two populations of the tick vector distributed throughout this region. Ornithodoros turicata is a western population that ranges from California to Texas. There is a gap through Louisiana, Mississippi, and Alabama where the tick has not been identified. An isolated eastern population exists in Florida and was designated a subspecies, O. turicata americanus. A knowledge gap that exists is the poor understanding of vector competence between western and eastern populations of ticks for B. turicatae. In this study, we generated uninfected colonies of O. turicata that originated in Texas and Kansas and of O. turicataamericanus. B. turicatae acquisition, maintenance through the molt, and subsequent transmission were evaluated. Our findings revealed significant differences in murine infection after feeding infected O. turicata and O. turicataamericanus ticks on the animals. Interestingly, the salivary glands of both tick populations were colonized with B. turicatae to similar densities. Our results suggest that the salivary glands of the tick colonies assessed in this study impact vector competence of the evaluated B. turicatae isolates.IMPORTANCE Several knowledge gaps exist in the vector competence of various geographical populations of O. turicata that transmit B. turicatae A western population of this tick is distributed from California to Texas, and an eastern population exists in Florida. Utilizing western and eastern populations of the vector, we studied acquisition and transmission of two B. turicatae isolates. Regardless of the isolate used, infection frequencies were poor in mice after the eastern population feeding on them. Since salivary gland colonization is essential for B. turicatae transmission, these tissues were further evaluated. Interestingly, the salivary glands from the two populations were similarly colonized with B. turicatae. These findings suggest the role of tick saliva in the establishment of infection and that the salivary glands may be a bottleneck for successful transmission.

Keywords: Borrelia turicatae; Ornithodoros turicata; relapsing fever; vector competence; vector competency.

FIG 1

Assessment of serological responses to B. turicatae (Bt) protein lysates from mice fed upon by infected O. turicata and O. turicata americanus ticks. Immunoblots from two mice are representative of the remaining animals in each treatment group. Serum samples were used from mice that were fed upon by the following O. turicata (Ot) or O. turicata americanus (Ota)::B. turicatae isolate combinations: Ot-TX::Bt-TX (A), Ot-TX::Bt-FL (B), Ot-KS::Bt-TX (C), Ot-KS::Bt-FL (D), Ota::Bt-TX (E), and Ota::Bt-FL (F). A preinfection (Pre) serum sample is shown (G) and represents the remaining animals. Molecular masses are shown on the left of the immunoblots in kilodaltons.

FIG 2

Demonstration of O. turicata americanus salivary gland colonization by B. turicatae-gfp. (A) Intact salivary glands were excised from O. turicata americanus ticks that were infected with B. turicatae-gfp. A dark-field image shows the structural outline of the acinus (B), and an image of fluorescing B. turicatae-gfp localizes the spirochetes to the acinus lumen (C). (D) Dark-field and fluorescent images were also overlaid. (B to D) A scale bar is shown in the bottom right.

FIG 3

Quantification of Bt-TX and Bt-FL in the salivary glands of O. turicata and O. turicata americanus ticks. Each gDNA sample consisted of salivary glands from five ticks, and two to four samples were evaluated per group. gDNA from salivary gland samples of O. turicata-B. turicatae or O. turicata americanus-B. turicatae isolate groups are as follows: Ot-TX::Bt-TX, Ot-TX::Bt-FL, Ot-KS::Bt-FL, Ota::Bt-TX, and Ota::Bt-FL.