Unexpected failure of Ixodes scapularis nymphs to transmit a North American Borrelia bissettiae strain

Abstract

Globally, the Borrelia burgdorferi (sensu lato) complex comprises more than 21 species of spirochetes. Although the USA is home to a diverse fauna of Lyme disease group Borrelia species, only two are considered responsible for human clinical disease: Borrelia burgdorferi (sensu stricto) and Borrelia mayonii. However, evidence has implicated additional B. burgdorferi (s.l.) species in human illness elsewhere. While much research has focused on the B. burgdorferi (s.s.)-tick interface, tick vectors for most of the other North American Lyme disease group Borrelia species remain experimentally unconfirmed. In this report we document the ability of Ixodes scapularis to acquire but not transmit a single strain of Borrelia bissettiae, a potential human pathogen, in a murine infection model. Pathogen-free I. scapularis larvae were allowed to feed on mice with disseminated B. burgdorferi (s.s.) or B. bissettiae infections. Molted infected nymphs were then allowed to feed on naïve mice to assess transmission to a susceptible host through spirochete culture and qPCR throughout in ticks collected at various developmental stages (fed larvae and nymphs, molted nymphs, and adults). In this study, similar proportions of I. scapularis larvae acquired B. bissettiae and B. burgdorferi (s.s.) but transstadial passage to the nymphal stage was less effective for B. bissettiae. Furthermore, B. bissettiae-infected nymphs did not transmit B. bissettiae infection to naïve susceptible mice as determined by tissue culture and serology. In the tick, B. bissettiae spirochete levels slightly increased from fed larvae to molted and then fed nymphs, yet the bacteria were absent in molted adults. Moreover, in contrast to B. burgdorferi (s.s.), B. bissettiae failed to exponentially increase in upon completion of feeding in our transmission experiment. In this specific model, I. scapularis was unable to support B. bissettiae throughout its life-cycle, and while live spirochetes were detected in B. bissettiae-infected ticks fed on naïve mice, there was no evidence of murine infection. These data question the vector competence of Ixodes scapularis for B. bissettiae. More importantly, this specific B. bissettiae-I. scapularis model may provide a tool for researchers to delineate details on mechanisms involved in Borrelia-tick compatibility.