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Tick extracellular vesicles enable arthropod feeding and promote distinct outcomes of bacterial infection

Chávez Oliva Adela S., Xiaowei Wang, Liron Marnin, Nathan K. Archer, Holly L. Hammond, Erin E. McClure Carroll, Dana K. Shaw, Brenden G. Tully, Amanda D. Buskirk, Shelby L. Ford, L. Rainer Butler, Preeti Shahi, Kateryna Morozova, Christina C. Clement, Lauren Lawres, Anya J. O'Neal, Choukri Ben Mamoun, Kathleen L. Mason, Brandi E. Hobbs, Glen A. Scoles, Eileen M. Barry, Daniel E. Sonenshine, Utpal Pal, Jesus G. Valenzuela, Marcelo B. Sztein, Marcela F. Pasetti, Michael L. Levin, Michail Kotsyfakis, Steven M. Jay, Jason F. Huntley, Lloyd S. Miller, Laura Santambrogio, Joao H. F. Pedra
Nature communications 2021 v.12 no.1 pp. -
Anaplasma phagocytophilum, Dermacentor andersoni, Francisella tularensis, Ixodes scapularis, bacterial infections, ecosystems, exosomes, hematophagy, homeostasis, immunity, inflammation, mammals, morbidity, mortality, pathogens, ticks, virulence
Pathogens cycle between an arthropod and a mammal to cause vector-borne diseases. Thus, blood-feeding arthropods dictate mutualistic and parasitic relationships. For instance, arthropod salivary effectors are advantageous to pathogens because they may facilitate microbial dissemination. Conversely, arthropod salivary molecules are harmful to mammals because they alter immune homeostasis. We hypothesized that tick nanovesicles, also known as extracellular vesicles or exosomes, affect mammalian morbidity and mortality based on the degree of microbial virulence. Here, we show that tick nanovesicles drive these synergistic and antagonistic interactions based on the pathogenic potential of a microbe. Nanovesicles released by the tick Ixodes scapularis regulate skin immunity via SNARE proteins and 'd T cells, enabling transmission of the mildly virulent rickettsial agent Anaplasma phagocytophilum to the mammalian host. Paradoxically, nanovesicles from the tick Dermacentor andersoni reduce inflammation and mitigate spreading of the lethal pathogen Francisella tularensis. Altogether, we reveal a plastic trans-kingdom ecosystem where tick nanovesicles drive host morbidity and mortality based on the capability of a microbe to cause disease