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Title: Anaplasma marginale actively modulates vacuolar maturation during intracellular infection of its tick vector dermacentor andersoni

item MAGUNDA, FOREGIVEMORE - Washington State University
item THOMPSON WRIGHT, CHELSEA - Old Dominion University
item Schneider, David
item Noh, Susan

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/19/2016
Publication Date: 5/27/2016
Citation: Magunda, F., Thompson Wright, C., Schneider, D.A., Noh, S.M. 2016. Anaplasma marginale actively modulates vacuolar maturation during intracellular infection of its tick vector dermacentor andersoni. Applied and Environmental Microbiology. doi: 10.1128/AEM.01030-16.

Interpretive Summary: Ticks transmit a variety of intracellular bacterial pathogens that cause significant diseases in humans and animals. For successful transmission, these bacterial pathogens must first gain entry into the tick midgut digestive cells, avoid digestion and establish a replicative niche without harming the tick vector. Little is known about how this replicative niche is established and maintained. Using the ruminant pathogen A. marginale and its natural tick vector, D. andersoni, this study describes the features of the A. marginale niche in the tick midgut and demonstrates that A. marginale protein synthesis is required for maintenance of this niche. This work opens a new line of inquiry about the pathogen effectors and their targets within the tick that mediate tick-pathogen interactions and ultimately serve as the determinants of pathogen success.

Technical Abstract: Tick-borne transmission of bacterial pathogens in the Order Rickettsiales is responsible for a diversity of infectious diseases, many of them severe, in both humans and animals. Transmission dynamics differ among these pathogens and are reflected in the pathogen-vector interaction. Anaplasma marginale has been shown to establish and maintain infectivity within Dermacentor spp. for weeks to months while escaping the complex network of vacuolar peptidases responsible for digestion of the tick blood meal. How this prolonged maintenance of infectivity in a potentially hostile environment is effected has been unknown. Using the natural vector Dermacentor andersoni, we demonstrated that A. marginale-infected tick vacuoles (AmVs) concurrently recruit markers of the early (Rab5), recycling (Rab4 and Rab11) and late endosome (Rab7), are maintained near neutral pH, do not fuse with lysosomes, exclude the protease cathepsin L, and engage the endoplasmic reticulum and Golgi for up to 21d post infection. Maintenance of this safe vacuolar niche requires active A. marginale protein synthesis; in its absence the AmVs mature into acidic, protease-active phagolysosomes. Identification of this bacterial directed modeling of the tick midgut endosome provides a mechanistic basis for examination of differences in transmission efficiency observed among A. marginale strains and among vector populations.