Contrasts in tick innate immune responses to Borrelia burgdorferi challenge: Immunotolerance in Ixodes scapularis versus immunocompetence in Dermacentor variabilis (Acari : Ixodidae)

The blacklegged tick, Ixodes scapularis Say, transmits the Lyme disease spi rochete Borrelia burgdorferi, whereas the American dog tick, Dermacentor va riabilis (Say), is unable to transmit the bacterium. We compared the innate immune response of these ticks against spirochetes directly inoculated int o the hemocoel cavity of ticks. In I. scapularis, some Borrelia were found associated with hemocytes, while numerous other spiral-shaped, intact bacte ria remained free in the hemolymph. In contrast, in D. variabilis only remn ants of the bacteria were evident in the hemolymph, indicating lysis; intac t spirochetes were rare. Spirochetes were observed bound to or within the o rgans of both tick species, although many more spirochetes were found assoc iated with the I. scapularis organs. The few spirochetes observed with the D. variabilis organs appeared to be dead because D. variabilis tissues rare ly contained culturable bacteria, unlike I. scapularis tissues. When spiroc hetes were incubated with I. scapularis hemolymph plasma in vitro, bacteria l survival and motility were not reduced. In contrast, incubation of spiroc hetes with D. variabilis hemolymph plasma resulted in >50% of the spirochet es becoming nonmotile by 45 min. The differences in the responses of the tw o different tick species indicate that I. scapularis is immunotolerant when challenged with B. burgdorferi and dependent on a slow phagocytic response to clear Borrelia from the hemolymph. In contrast, D. variabilis is highly immunocompetent (i.e., innate immunity), using plasma borreliacidal factor s and a rapid increase in phagocytic cells to clear the infection and limit tissue invasion.