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ARS Home » Pacific West Area » Pullman, Washington » Animal Disease Research » Research » Publications at this Location » Publication #369066
Research Project: Identification of Tick Colonization Mechanisms and Vaccine Development for Anaplasmosis

Location: Animal Disease Research

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

Author
item CHÁVEZ, OLIVA ADELA - Texas A&M University
item WANG, XIAOWEI - University Of Maryland
item ARCHER, NATHAN - Johns Hopkins University
item HAMMOND, HOLLY - University Of Maryland
item MCCLURE, ERIN - University Of Maryland
item SHAW, DANA - Washington State University
item BUSKIRK, AMANDA - University Of Maryland
item FORD, SHELBY - Centers For Disease Control And Prevention (CDC) - United States
item MOROZOVA, KATERYNA - Albert Einstein College Of Medicine
item CLEMENT, CRISTINA - Albert Einstein College Of Medicine
item LAWRES, LAUREN - Yale University
item O'NEAL, ANYA - University Of Maryland
item MAMOUN, CHOUKRI BEN - Yale University
item Mason, Kathleen
item HOBBS, BRANDI - University Of Maryland
item Scoles, Glen
item BARRY, EILEEN - University Of Maryland
item SONENSHINE, DANIEL - Old Dominion University
item PAL, UTPAL - University Of Maryland
item VALENZUELA, JESUS - Nih, National Institutes Of Allergy And Infectious Diseases
item SZTEIN, MARCELO - University Of Maryland
item PASETTI, MARCELA - University Of Maryland
item LEVIN, MICHAEL - Centers For Disease Control And Prevention (CDC) - United States
item KOTSYFAKIS, MICHAIL - Czech Academy Of Sciences
item JAY, STEVEN - University Of Maryland
item MILLER, LLOYD - Johns Hopkins University
item SANTAMBROGIO, LAURA - Centers For Disease Control And Prevention (CDC) - United States
item PEDRA, JOAO - University Of Maryland

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/24/2021
Publication Date: 6/17/2021
Publication URL: https://handle.nal.usda.gov/10113/7709337
Citation: Chávez, O.S., Wang, X., Archer, N., Hammond, H.L., McClure, E.E., Shaw, D.K., Buskirk, A.D., Ford, S.L., Morozova, K., Clement, C.C., Lawres, L., O'Neal, A.J., Mamoun, C., Mason, K.L., Hobbs, B.E., Scoles, G.A., Barry, E.M., Sonenshine, D.E., Pal, U., Valenzuela, J.G., Sztein, M.B., Pasetti, M.F., Levin, M.L., Kotsyfakis, M., Jay, S.M., Miller, L., Santambrogio, L., Pedra, J.H. 2021. Tick extracellular vesicles enable arthropod feeding and promote distinct outcomes of bacterial infection. Nature Communications. 12. Article 3696. https://doi.org/10.1038/s41467-021-23900-8.
DOI: https://doi.org/10.1038/s41467-021-23900-8

Interpretive Summary: Microbes undergo distinct selection pressures to survive in both arthropods and mammals. We show that nanovesicles from blood-feeding arthropods tailor microbial virulence during transmission. Nanovesicles from the tick Dermacentor andersoni reduced spreading of the deadly pathogen Francisella tularensis to mammals. This strategy benefits the arthropod because it allows unabated feeding on a healthier host. Conversely, nanovesicles from the deer tick Ixodes scapularis enabled transmission of the mildly virulent rickettsial agent Anaplasma phagocytophilum. This evolutionary approach promotes pathogen dissemination because there is mostly a neutral relationship between the microbe and the mammalian host. As the arthropod directs microbial virulence during blood-feeding, we suggest that the biology of the vector must be taken into consideration when developing strategies to control these illnesses.

Technical Abstract: 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