Borrelia hermsii Acquisition Order in Superinfected Ticks Determines Transmission Efficiency

Abstract

Multilocus sequence typing of Borrelia hermsii isolates reveals its divergence into two major genomic groups (GG), but no differences in transmission efficiency or host pathogenicity are associated with these genotypes. To compare GGI and GGII in the tick-host infection cycle, we first determined if spirochetes from the two groups could superinfect the tick vector Ornithodoros hermsi. We infected mice with isolates from each group and fed ticks sequentially on these mice. We then fed the infected ticks on naive mice and measured GGI and GGII spirochete densities in vector and host, using quantitative PCR of genotype-specific chromosomal DNA sequences. Sequential feedings resulted in dual tick infections, showing that GGI or GGII primary acquisition did not block superinfection by a secondary agent. On transmission to naive mice at short intervals after acquisition, ticks with primary GGI and secondary GGII spirochete infections caused mixed GGI and GGII infections in mice. However, ticks with primary GGII and secondary GGI spirochete infections caused only GGII infections with all isolate pairs examined. At longer intervals after acquisition, the exclusion of GGI by GGII spirochetes declined and cotransmission predominated. We then examined GGI and GGII spirochetemia in mice following single inoculation and coinoculation by needle and found that GGI spirochete densities were reduced on multiple days when coinoculated with GGII. These findings indicate that dual GGI-GGII spirochete infections can persist in ticks and that transmission to a vertebrate host is dependent on the order of tick acquisition and the interval between acquisition and transmission events. Borrelia hermsii is the primary agent of tick-borne relapsing fever in western North America, where it persists in enzootic cycles involving the argasid (soft tick) vector Ornithodoros hermsi and diverse vertebrate hosts (1). Argasid ticks are predominately nest dwelling and feed at each immature stage and multiple times as adults, with the potential for acquisition and transmission of multiple spirochete genotypes (2). As rapid feeders, their occasional infestation of humans is rarely discovered, and spirochete isolation from ticks involved in transmission is virtually unreported. Spirochete DNA analysis from clinical samples, rodent hosts, and ticks indicates divergence into two major B. hermsii genomic groups (GGI and GGII), based on the 16S-23S rRNA gene intergenic spacer (2, 3) and multilocus sequence typing (4). The latter study demonstrated that GGI and GGII isolates are distributed throughout the range of the vector. Clinical isolates from a western Montana site showed sympatry of GGI and GGII spirochetes within a microenvironment where the disease is endemic (4, 5), suggesting that ticks may be exposed to spirochetes of both genotypes during their life cycle. Tick vectors and mammalian hosts can show significant heterogeneity in pathogen populations, as shown by studies on B. burgdorferi sensu lato and sensu stricto isolates (6-8) and Anaplasma ma...

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

“…Applied and Environmental Microbiology transmission-fed ticks (16). In the assessment of O. turicata americanus salivary glands, utilization of B. turicatae producing GFP indicated that the pathogens were also localized in the lumen of type II acini.…”

Transmission Dynamics of Borrelia turicatae from the Arthropod Vector

“…hermsi model of relapsing fever spirochetes indicate that transmission and dissemination of the bacteria within the tick and mammal is unique [30]. For example, B. burgdorferi , the causative agent of Lyme borreliosis, initially colonizes the midgut of Ixodes spp.…”

Broad diversity of host responses of the white-footed mouse Peromyscus leucopus to Borrelia infection and antigens

“…The subjects differed from animals captured in the field in being detectably free of other infectious diseases and parasites, in the predictability and adequateness of their nutrition (Martin et al, 2007a), and their habitat’s controlled, unvarying conditions (Martin et al, 2008). The animals were infected by needle inoculation and not by tick bite, although this may not be an important distinction for experimental B. hermsii infections (Policastro et al, 2013). Though more than a hundred animals were studied in total, these were divided for the experiments in groups of 30 or less.…”