Interaction and transmission of two Borrelia burgdorferi sensu stricto strains in a tick-rodent maintenance system

Abstract

In the northeastern United States, the Lyme disease agent, Borrelia burgdorferi sensu stricto, is maintained by enzoonotic transmission, cycling between white-footed mice (Peromyscus leucopus) and black-legged ticks (Ixodes scapularis). B. burgdorferi sensu stricto is genetically variable and has been divided into three major genotypes based on 16S-23S ribosomal DNA spacer (RST) analysis. To better understand how genetic differences in B. burgdorferi sensu stricto may influence transmission dynamics in nature, we investigated the interaction between an RST1 and an RST3 strain in a laboratory system with P. leucopus mice and I. scapularis ticks. Two groups of mice were infected with either BL206 (RST1) or B348 (RST3). Two weeks later, experimental mice were challenged with the opposite strain, while control mice were challenged with the same strain as that used for the primary infection. The transmission of BL206 and B348 from infected mice was then determined by xenodiagnosis with uninfected larval ticks at weekly intervals for 42 days. Mice in both experimental groups were permissive for infection with the second strain and were able to transmit both strains to the xenodiagnostic ticks. However, the overall transmission efficiencies of BL206 and B348 were significantly different. BL206 was more efficiently transmitted than B348 to xenodiagnostic ticks. Significantly fewer double infections than expected were detected in xenodiagnostic ticks. The results suggest that some B. burgdorferi sensu stricto strains, such as BL206, may be preferentially maintained in transmission cycles between ticks and white-footed mice. Other strains, such as B348, may be more effectively maintained in different tick-vertebrate transmission cycles.

FIG. 1.

Experimental design. Mice were divided into four groups as follows: group E1, infected with BL206-infected nymphs (day 0) and challenged with B348-infected nymphs (day 14); group C1, infected and challenged with BL206-infected nymphs (days 0 and 14); group E3, infected with B348-infected nymphs (day 0) and challenged with BL206-infected nymphs (day 14); group C3, infected and challenged with B348-infected nymphs (days 0 and 14). The infection of mice was determined by xenodiagnosis with 100 uninfected larvae per mouse on days 10, 21, 28, and 42.

FIG. 2.

Progress of infection of xenodiagnostic ticks with BL206 (blue), B348 (red), and a mixture of B348 and BL206 (green). Percentages of B. burgdorferi sensu stricto strains in four groups of mice were determined after 10, 21, 28, and 42 days. E1, infected with BL206 and challenged with B348; E3, infected with B348 and challenged with BL206; C1, infected and challenged with BL206; C3, infected and challenged with B348.