The role of autophagy in tick-endosymbiont interactions: insights from Ixodes scapularis and Rickettsia buchneri

Approximately 80 identified tick species are recognized as vectors and impact global public health by transmitting a wide range of pathogens; however, little is known about the interactions of ticks with the microbiome that they harbor, let alone their bacterial symbionts. In this study, we used the black-legged tick, Ixodes scapularis Say (Acari: Ixodidae), a vector of seven human pathogens in the United States, and utilized Rickettsia buchneri sensu stricto ISO7^T (Rickettsiales: Rickettsiaceae), a spotted fever group (SFG) rickettsia that is an endosymbiont of I. scapularis, to investigate the role of autophagy in symbiont and tick interactions. We found that the expression profile of most autophagy family member proteins (ATGs) is down-regulated after R. buchneri infection in tick cell cultures. The autophagic process was observed by assessment of autophagosome formation and maturation in vitro (tick cell culture) and in vivo (tick ovary) in the presence of R. buchneri, whereas apoptosis was not induced. We further showed that R. buchneri infection triggered the accumulation of plasma membranes within cells. Suppressing autophagy via Atg8 siRNA interference inhibited intracellular rickettsial replication. This research indicates that autophagy regulation is important for the maintenance of R. buchneri in its I. scapularis tick host and provides more clues to solve the tick-symbiont interaction puzzle.