Abstract
Vector-borne pathogens establish systemic infections in host tissues to maximize transmission to arthropod vectors. Co-feeding transmission occurs when the pathogen is transferred between infected and naive vectors that feed in close spatiotemporal proximity on a host that has not yet developed a systemic infection. Borrelia afzelii is a tick-borne spirochete bacterium that causes Lyme borreliosis (LB) and is capable of co-feeding transmission. Whether ticks that acquire LB pathogens via co-feeding are actually infectious to vertebrate hosts has never been tested. We created nymphs that had been experimentally infected as larvae with B. afzelii via co-feeding or systemic transmission, and compared their performance over one complete LB life cycle. Co-feeding nymphs had a spirochete load that was 26 times lower than systemic nymphs but both nymphs were highly infectious to mice (i.e., probability of nymph-to-host transmission of B. afzelii was ~100%). The mode of transmission had no effect on the other infection phenotypes of the LB life cycle. Ticks that acquire B. afzelii via co-feeding transmission are highly infectious to rodents, and the resulting rodent infection is highly infectious to larval ticks. This is the first study to show that B. afzelii can use co-feeding transmission to complete its life cycle.
Highlights
In vector-borne infections, there are two major pathways by which naive vectors acquire vector-borne pathogens: systemic transmission and co-feeding transmission[1–3]
At 2 and 30 days post nymphal infestation (PNI), the mice were infested with I. ricinus larval ticks, and the resulting engorged larval ticks were allowed to moult into nymphs
The larval ticks at 2 days PNI overlapped with the nymphs and acquired B. afzelii via co-feeding transmission, whereas the larval ticks at 30 days PNI acquired B. afzelii via systemic transmission
Summary
In vector-borne infections, there are two major pathways by which naive vectors acquire vector-borne pathogens: systemic transmission and co-feeding transmission[1–3]. L. is a genospecies complex of spirochete bacteria that contains the etiological agents of human Lyme disease[9–13] These tick-borne pathogens are transmitted among vertebrate hosts by hard ticks belonging to the genus Ixodes. We compared the spirochete load of B. afzelii between I. ricinus nymphs that acquired this pathogen as larval ticks via co-feeding transmission or systemic transmission[29, 30]. The size of the spirochete population in the nymphal tick influences the probability that a particular Borrelia strain is transmitted to the rodent host[31, 32] Taken together, these studies suggest that co-feeding nymphs may be less infectious to vertebrate reservoir hosts than systemic nymphs. A recent review pointed out that the critical remaining question is whether nymphs that acquired Lyme disease pathogens as larval ticks via co-feeding transmission are infectious to naive vertebrate hosts[1]. We tested whether the mode of transmission by which the nymphs had acquired the infection influenced the infection phenotype in the mice and in the generation of ticks
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