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. 2021 Apr 15;58(4):1926–1930. doi: 10.1093/jme/tjab060

Vector Specificity of the Relapsing Fever Spirochete Borrelia hermsii (Spirochaetales: Borreliaceae) for the Tick Ornithodoros hermsi (Acari: Argasidae) Involves Persistent Infection of the Salivary Glands

Tom G Schwan 1,✉
Editor: Kevin Macaluso
PMCID: PMC8285016  PMID: 33855354

Abstract

The relapsing fever spirochetes Borrelia hermsii and Borrelia turicatae are each maintained and transmitted in nature by their specific tick vectors, Ornithodoros hermsi Wheeler (Acari: Argasidae) and Ornithodoros turicata (Duges), respectively. The basis for this spirochete and vector specificity is not known, but persistent colonization of spirochetes in the tick’s salivary glands is presumed to be essential for transmission by these long-lived ticks that feed in only minutes on their warm-blooded hosts. To examine this hypothesis further, cohorts of O. hermsi and O. turicata were infected with B. hermsii and examined 7–260 d later for infection in their midgut, salivary glands, and synganglion. While the midgut from all ticks of both species at all time points examined were infected with spirochetes, the salivary glands of only O. hermsi remained persistently infected. The salivary glands of O. turicata were susceptible to an early transient infection. However, no spirochetes were observed in these tissues beyond the first 32 d after acquisition. Ticks of both species were fed on mice 112 d after they acquired spirochetes and only those mice fed upon by O. hermsi became infected. Thus, the vector competency for B. hermsii displayed by O. hermsi but not O. turicata lies, in part, in the persistent infection of the salivary glands of the former but not the latter species of tick. The genetic and biochemical mechanisms supporting this spirochete and vector specificity remain to be identified.

Keywords: borreliosis, zoonosis, vector competency

Vector specificity of the three primary species of soft tick-associated relapsing fever spirochetes in the United States, Borrelia hermsii (Davis) (Spirochaetales: Borreliaceae), Borrelia turicatae (Brumpt) (Spirochaetales: Borreliacae), and Borrelia parkeri (Davis) (Spirochaetales: Borreliacae), for the three species of ticks that transmit them each in nature was demonstrated many years ago (Brumpt 1933, Davis 1942, 1956). Gordon E. Davis and coworkers at the Rocky Mountain Laboratory performed most of the seminal work that defined this specificity. For these experiments, mice were first infected when fed upon by one species of tick and fed upon again later while spirochetemic by three species of uninfected ticks, which were subsequently tested for their ability to transmit when feeding on uninfected mice (Fig. 1). Davis (1942) summarized these efforts as follows: “Approximately 1600 ticks have been tested in this manner. In no instance has one of the three species of ticks transmitted spirochetes recovered from either of the other two.” Yet, the mechanisms underlying this restriction of biological transmission by just one species of tick remain largely unknown. Ornithodoros hermsi Wheeler (Acari: Argasidae), Ornithodoros turicata (Duges) (Acari: Argasidae), and Ornithodoros parkeri Cooley (Arcari: Argasidae), the respective tick vectors of the three species of spirochetes listed above, are rapid feeders—usually less than 60 min—in all active stages of their life cycle. Thus, for efficient transmission by tick bite, the assumption was early on that spirochetes must reside in the tick’s salivary glands at the time of feeding (Wheeler 1942). Given the speed that transmission may occur so soon after ticks attach (Davis 1941, Boyle et al. 2014), and the attention directed at the salivary glands of Old World species of Ornithodoros and other relapsing fever spirochetes (Burgdorfer 1951), this hypothesis was reasonable.

Fig. 1.

Fig. 1.

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Gordon E. Davis (right) feeding North American species of Ornithodoros ticks on white mice to examine transmission and vector specificity of B. hermsii, B. turicatae and B. parkeri (circa 1940; photo provided by Rocky Mountain Laboratories, NIAID, NIH).

The first and only hint underlying the specificity for these spirochetes for just one tick species came from work with B. turicatae, B. parkeri and their respective tick vectors (Davis and Burgdorfer 1955). While O. turicata was able to acquire B. turicatae and B. parkeri when fed on infected mice, only B. turicatae persisted in the salivary glands—out to 322 d after the infectious bloodmeal. When O. turicata ingested B. parkeri with the bloodmeal, the salivary glands became transiently infected only during the first 35 d after acquisition, which resulted in no transmission during the later test feedings. Therefore, in this specific combination of tick and spirochete infection, vector specificity may be partially due to one species of spirochete persisting in the salivary glands of only one species of tick. Therefore, to address this persistence further with another relapsing fever spirochete, B. hermsii infection was examined in its known vector O. hermsi and compared to infection in O. turicata.

Materials and Methods

Bacterial Strain and Cultivation

Borrelia hermsii originated from a clinical diagnostic specimen from a human patient (isolate designated DAH) infected in eastern Washington (Schwan et al. 2007). A clone (2E7) was acquired by growth in BSK-II medium (Barbour 1984) and limiting dilution in 96-well microtiter plates (Schwan et al. 1992) and used for the experiments described herein.

Spirochete Infection of Ticks

Ornithodoros hermsi and O. turicata were from established uninfected tick colonies at the Rocky Mountain Laboratories (RML). Two adult laboratory mice (Mus musculus) strain RML—a closed colony established at RML in 1937 that originated from outbred Swiss Webster mice—were anesthetized by inhalation of isoflurane (Fluriso; Vet ONE, MWI Veterinary Supply, Boise, ID), needle inoculated intraperitoneally with 200 µl BSK-II of the same culture of spirochetes, and followed daily for infection by microscopic examination of blood from the tail vein. When spirochetemias achieved cell densities of approximately 107 spirochetes per ml of blood, the two mice were anesthetized with pentobarbital sodium (0.5 mg/10 g body weight) (Abbott Laboratories, North Chicago, IL), the abdominal hair was sheared, and ticks were placed on the abdomen to feed. Approximately 150 2nd-stage nymphs of the two species of ticks were fed on separate mice and then placed in ventilated plastic tubes in glass jars with 85% relative humidity and kept at room temperature with ambient light. Immediately after tick feeding, blood samples from the mice were prepared on glass microscope slides for quantification of spirochetes as described (McCoy et al. 2010). Three ticks of both species were also examined immediately after feeding by dispersing their engorged midgut in phosphate-buffered saline (PBS) on microscope slides and viewing at 400× with a Nikon Eclipse E600 dark-field microscope (Nikon Instruments, Melville, NY). Spirochetes were numerous in all six samples, showing that both cohorts of ticks acquired B. hermsii when feeding.

At seven time points after tick feeding (days 7, 22, 32, 69, 118, 139, and 260), 3 or 5 ticks of both species were examined for spirochete infection. The midgut, synganglion, and salivary glands were dissected separately in PBS and fixed for immunofluorescence staining on glass microscope slides and cover slips as described (Schwan and Hinnebusch 1998). The fine-tipped dissection forceps were wiped with disposable tissue and flame-sterilized with an alcohol lamp after removing each tissue to prevent spirochete contamination between the samples. Salivary glands and synganglia were first rinsed in clean PBS on a microscope slide and then placed in fresh PBS on another slide for final preparation. Fixed tissues were incubated in a 1:50 dilution of rabbit anti-B. hermsii DAH polyclonal antiserum #2779 produced at RML, rinsed in PBS, incubated with goat anti-rabbit IgG (H & L chain) antibody conjugated with fluorescein isothiocyanate (Kirkegaard & Perry, Gaithersburg, MD) diluted 1:100, rinsed in PBS and distilled water, air dried, and mounted with glycerol. The entire tissues were examined for spirochetes at 600× with a Nikon Eclipse E800 epifluorescence microscope (Nikon Instruments) using a 60× oil immersion objective lens.

Tick Transmission and Infectivity Experiments

Ticks of both species were fed on three mice each at 112 d after their previous infectious bloodmeal when all of the previously engorged nymphs had molted. The midgut from four additional ticks of both species were also dissected in PBS on the same day, suspended in 100 µl of PBS, and inoculated intraperitoneally into mice. The salivary glands were not tested for infectivity because the O. turicata salivary glands were negative by immunofluorescent antibody staining by day 69 post-acquisition. Mice were examined daily for 9 d for spirochetemia by collecting a drop of blood from the tail vein while anesthetized with isoflurane and viewing wet preparations on glass microscope slides with coverslips at 400× with a Nikon Eclipse E600 dark-field microscope.

Ethics Statement

The RML, NIAID, NIH, Animal Care and Use Committee approved study protocols (2009–32, 2009–87) for the feeding of ticks on mice, spirochete infection in mice, and sampling mouse blood for spirochetemia. All work was done in adherence to the institution’s guidelines for animal husbandry and followed the guidelines and basic principals in the Public Health Service Policy on Humane Care and Use of Laboratory Animals, and the Guide for the Care and Use of Laboratory Animals, United States Institute of Laboratory Animal Resources, National Research Council.

Results

Spirochete Infection in Ticks

The midgut, salivary glands, and synganglion from three to five ticks of both species were examined for infection at seven time points 7–260 d after feeding on infected mice (Table 1). The midgut samples from all ticks examined at all time points were infected. Most salivary glands of O. hermsi were infected (29/31, 93.5%) out to 260 d with spirochetes often very numerous (Fig. 2). In contrast, while the salivary glands of O. turicata were susceptible to infection during the first month after feeding, after day 32 spirochetes were no longer observed. The difference in the number of O. hermsi and O. turicata with infected salivary glands was highly significant (χ 2 = 29.5589; P = <0.00001). The prevalence of infection in the synganglion was similar to the salivary glands of the two species of ticks. However, the synganglion of two O. turicata were still infected at 139 d after feeding (Table 1; Fig. 2).

Table 1.

Tissue colonization of B. hermsii in O. hermsi and O. turicata following acquisition by feeding on infected mice

Ornithodoros hermsi Ornithodoros turicata
Daysa Stageb MGc SG SYN Stage MG SG SYN
7 2N, 2♂, 1♀ 5/5d 3/5 0/5 5N 5/5 3/5 3/5
22 4N, 1♀ 5/5 5/5 5/5 5N 5/5 4/5 3/5
32 3N, 1♂, 1♀ 5/5 5/5 5/5 5N 5/5 1/5 1/5
69 2♂, 3♀ 5/5 5/5 5/5 5N 5/5 0/5 0/5
118 3N, 1♂, 1♀ 5/5 5/5 4/5 5N 5/5 0/5 0/4
139 2N, 1♀ 3/3 3/3 2/3 3N 3/3 0/3 2/3
260 3N 3/3 3/3 2/3 3N 3/3 0/3 0/3
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a Days = number of days after spirochete acquisition.

b N = nymph, ♂ = male, ♀ = female.

c MG = midgut, SG = salivary glands, SYN = synganglion.

d Number of tick tissues positive/number of tick tissues examined.

Fig. 2.

Fig. 2.

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Ornithodoros hermsi salivary gland infected with B. hermsii, day 32 postinfection, scale bar = 60 µm (A); O. turicata synganglion infected with B. hermsii., day 32 postinfection, scale bar = 40 µm (B).

Tick Transmission and Infectivity

At 112 d post infection, ticks of both species were fed on mice (Table 2). All mice fed upon by O. hermsi became spirochetemic while none of the mice fed upon by O. turicata became infected. Additionally, all mice needle-inoculated with one midgut from O. hermsi became infected, while the midgut from only one O. turicata produced a detectable spirochetemia (Table 2).

Table 2.

Tick feeding and needle inoculation of mice with O. hermsi and O. turicata infected with B. hermsiia

Ornithodoros hermsi b Ornithodoros turicata c
Mouse Ticks Infection Mouse Ticks Infection
1 4/5d + e 1 5/5 -
2 3/5 + 2 5/5 -
3 3/5 + 3 1/3 -
4 1 MGf + 4 1 MG +
5 1 MG + 5 1 MG -
6 1 MG + 6 1 MG -
7 1 MG + 7 1 MG -
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a Performed 112 d after tick infection.

b All ticks used were nymphs except 1 female included on mouse 1.

c All ticks used were nymphs.

d Number of ticks fed/number of ticks placed on mouse.

e + = mouse infected; - = mouse not infected.

f 1 MG = 1 midgut inoculated intraperitoneally.

Discussion

Two exemplary studies of Old World ticks and spirochetes demonstrated the persistent colonization of the salivary glands of Ornithodoros moubata (Murray) (Acari: Argasidae) and Ornithodoros erraticus (Lucas) (Acari: Argasidae) infected with Borrelia duttonii (Novy and Knapp) (Spirochaetales: Borreliaceae) and Borrelia crocidurae (Leger) (Spirochaetales: Borreliaceae), respectively (Burgdorfer 1951, Gaber et al. 1984). However, the first early attempt to demonstrate B. hermsii in the salivary glands of O. hermsi failed (Wheeler 1942), possibly due to the relatively insensitive techniques used—silver staining of fixed tissue sections. More recent studies utilizing immunofluorescent antibody staining of spirochetes in whole, squashed, salivary glands including results presented herein clearly demonstrated high prevalence and persistence of B. hermsii in salivary glands of O. hermsi out to at least 448 d after their acquisition by tick feeding (Policastro et al. 2013, Raffel et al. 2014, Schwan and Hinnebusch 1998, Schwan et al. 2020). Yet, B. hermsii did not persist in the salivary glands of O. turicata after a transient infection lasting about a month after ticks ingested spirochetes (Table 1), which is similar to what was observed for B. parkeri when infecting O. turicata (Davis and Burgdorfer 1955).

In the present study, ticks were not abundant enough in colonies to perform the reverse experiment, which was to infect O. hermsi and O. turicata with B. turicatae. Such experiments remain to be done but the prediction is that B. turicatae will persist in the salivary glands of O. turicata but not in O. hermsi. The first half of this prediction is based on work by others. Borrelia turicatae remained infectious to mammals while residing in O. turicata ticks that had not fed for 5 yr (Francis 1938). Given the rapidity of transmission, the assumption was that these spirochetes persisted in the salivary glands of O. turicata, which has subsequently been demonstrated by several investigators (Davis and Burgdorfer 1955, Varma 1956, Varma 1962, Boyle et al. 2014, Krishnavajhala et al. 2017).

Thus, one striking attribute emerging for the species specificity and vector competency of these relapsing fever spirochetes and their respective tick vectors lies in their persistent colonization of the salivary glands in only one species of tick. How B. hermsii persists in the salivary glands of O. hermsi but not O. turicata is the primary question at the basis of this vector specificity. If these spirochetes evolved first as symbionts of ticks as proposed by Hoogstraal (1979), then the species specificity may have developed prior to any involvement of the tick salivary glands. However, these spirochetes can remain in other organs of the non-vector tick. For example, the midgut of all O. turicata examined herein contained B. hermsii (Table 1), although their infectivity was demonstrated for only one sample (Table 2). B. hermsii persisted in the synganglion of O. hermsii but was also found in the synganglion of two O. turicata at 139 d after infection, which is similar to previous observations in our laboratory with B. hermsii in this organ in O. turicata and O. parkeri (Schwan 1996).

The expansion of these spirochetes to become parasites of warm-blooded vertebrates as well as ticks required their adaption to infect the salivary glands for horizontal transmission during blood feeding. The salivary glands of argasid ticks are composed of granular and agranular acini (Sonenshine 1991). The localization of B. hermsii and B. turicatae to specific acini and compartments within them in their specific vectors is not well understood, but preliminary observations suggest that B. hermsii may be restricted to the granular acini in O. hermsi (Fischer and Schwan 1999, Policastro et al. 2013). In contrast, B. turicatae was found in agranular acini in O. turicata although it is unclear if granular acini were also examined for infection (Krishnavajhala et al. 2017). Both species of spirochetes reside, in part, in the lumen and luminal duct of the salivary gland acini of their respective vectors (Fischer and Schwan 1999, Boyle et al. 2014, Krishnavajhala et al. 2017), which explains the rapid transmission via saliva immediately after ticks attach to their host. Where these spirochetes localize in the salivary glands of their vector compared to other non-vector competent tick species during transient infection is worthy of further investigation.

Transmission by ticks feeding on mice was tested only at 112 d after spirochete acquisition. Earlier times were not attempted as the majority of O. turicata nymphs had not yet molted, and these ticks routinely feed only once during each inter-molt stage (Balashov 1972). Yet, the question arises as to whether or not the O. turicata nymphs infected with B. hermsi could have transmitted spirochetes if allowed to attach to mice during their first month of infection when some salivary glands were likely infected. Davis (1942) provided no information regarding how long the three species of Ornithodoros had been infected before they were fed again to test for transmission and vector specificity. However, years later Davis and Burgdorfer (1955) described what they called an aberrant strain of B. parkeri that originated from O. parkeri collected in Oregon. For the first time, spirochete specificity broke down as O. turicata transmitted this spirochete, including ticks that had been infected for only 7 and 19 d. The time of these transmissions corresponded to early infections when the salivary glands might be infected. Additional experiments are warranted to examine the possibility that O. turicata, if forced or allowed to attach to mice soon after their acquisition feedings, are capable of transmitting B. hermsii when the salivary glands are transiently infected.

The mechanisms controlling the ability of only one species of relapsing fever spirochete to persist and remain viable in the salivary glands of its vector but not in other closely related ticks of the same genus will hopefully be investigated. If localization to specific salivary gland acini is a requirement for survival and subsequent transmission as discussed above, how might the environments in different acini and cellular compartments within them vary that affect spirochete survival? Might the required nutrients or other conditions available for spirochetes differ between granular and agranular acini? How might gene expression of these spirochetes vary when infecting the salivary glands of their vector compared to an incompetent tick species? Might the expression of salivary gland proteins vary among different ticks when infected with different spirochetes to include the upregulation of selective borreliacidal agents that eliminate all but one species? And finally, how might the microbiota of different tick species (Bonnet et al. 2017) and specifically in the salivary glands influence which spirochetes may persist in these tissues and become transmissible? With the availability of genomic data for numerous species in the genus Borrelia (Barbour and Schwan 2018), genetic manipulation techniques (Drecktrah and Samuels 2018), expression arrays and RNAseq approaches (Wu et al. 2015), expanding tick sialome information (Francischetti et al. 2008), and classic microscopy, the stage is set to gain an understanding of the basis of spirochete and vector specificity described by Davis 80 yr ago (Davis 1942).

Acknowledgments

I thank Philip Stewart and Sandra Stewart for providing constructive reviews of the manuscript. This work was supported by the Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health.

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