TrackingBorrelia afzeliifrom infectedIxodes ricinusnymphs to mice suggests a direct ‘gut-to-mouth’ route of Lyme disease transmission
AbstractQuantitative tracking ofBorrelia afzeliihas shown that its transmission cycle differs from the salivary route ofB. burgdorferitransmission byIxodes scapularis.Borrelia afzeliiare abundant in the guts of unfedIxodes ricinusnymphs and their numbers continuously decrease during feeding. In contrast, spirochetes are not present in the salivary glands.Borrelia afzeliitransmission starts during the early stages of feeding, spirochetes could be detected in murine skin within 1 day of tick attachment. Tick saliva is not essential forB. afzeliiinfectivity, the main requirement for successful host colonization being a change in outer surface protein expression that occurs in the tick gut during feeding. Spirochetes in vertebrate mode are able to survive within the host even if the tick is not present. On the basis of our data we propose that a direct ‘gut-to-mouth’ route of infection appears to be the main route ofB. afzeliitransmission.ImportanceLyme borreliosis is the most common vector-borne disease in the USA and Europe. The disease is caused by theBorreliaspirochetes and is transmitted throughIxodesticks. A better understanding of howBorreliaspirochetes are transmitted is crucial for development of efficient vaccines for preventing Lyme borreliosis. Here we present that the transmission of EuropeanB. afzeliispirochetes byI. ricinusticks significantly differs from the model transmission cycle described for AmericanB. burgdorferi/I. scapularis. We suggest thatB. afzeliiis not transmitted via salivary glands but most likely through the ‘midgut to mouthpart’ route. We further demonstrate that tick saliva is not important forB. afzeliitransmission and infectivity. Therefore, we support early studies by Willy Burgdorfer, who proposed thatBorreliatransmission occurs by regurgitation of infected gut contents. Our findings collectively point to theBorrelia-tick midgut interface as the correct target in our endeavours to combat Lyme borreliosis.