Skip to main content
ARS Home » Pacific West Area » Pullman, Washington » Animal Disease Research » Research » Publications at this Location » Publication #330328
Title: Superinfection exclusion of the ruminant pathogen anaplasma marginale in the tick vector is dependent on time between exposures to the strains

Author
item Noh, Susan
item DARK, MICHAEL - Washington State University
item Reif, Kathryn
item Ueti, Massaro
item Kappmeyer, Lowell
item Scoles, Glen
item PALMER, GUY - Washington State University
item BRAYTON, KELLY - Washington State University

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/15/2016
Publication Date: 3/18/2016
Citation: Noh, S.M., Dark, M.J., Reif, K.E., Ueti, M.W., Kappmeyer, L.S., Scoles, G.A., Palmer, G.H., Brayton, K.A. 2016. Superinfection exclusion of the ruminant pathogen anaplasma marginale in the tick vector is dependent on time between exposures to the strains. Applied and Environmental Microbiology. 82(11):3217-3124.

Interpretive Summary: Anaplasma marginale, the causative agent of bovine anaplasmosis is the most prevalent tick borne pathogen of cattle worldwide. A. marginale is transmitted by ticks. Once within the bovine host, infects red blood cells and causes anemia, weight loss, reduced production, and in severe cases, death. A. marginale has a large amount of genetic diversity which allows it to establish persistent infection in the bovine host. Additionally this large amount of genetic diversity allows for infection of an individual host with multiple strains, which may occur through co-infection, the simultaneous transmission of more than one strain or by superinfection, sequential infection by distinct strains. However, it has been observed that sequential exposure of the vector to multiple strains frequently prevents establishment of the second strain, a phenomenon termed superinfection exclusion, and only the primary strain is transmitted. As a consequence, uniform exclusion has the potential to greatly limit genetic diversity in the host population, which is difficult to reconcile with the high degree of genetic diversity maintained among many vector-borne pathogens, including A. marginale. In this work, we tested the hypothesis that superinfection exclusion is not uniform but rather is temporally dependent and that longer time intervals between strain exposure allows successful acquisition and transmission of a second, superinfecting strain. To test this hypothesis, Dermacentor andersoni ticks were sequentially exposed to two readily tick transmissible strains of A. marginale. The tick feedings were either immediately sequential or 28 days apart. Ticks were allowed to transmission feed and were individually assessed to determine if they were infected with one or both strains. We found that the second strain was excluded from the tick when the exposure interval was brief, but not prolonged. Midguts and salivary glands of individual ticks were super-infected and transmission of both strains occurred only when the exposure interval was prolonged. These findings indicate that superinfection exclusion is temporally dependent and helps account for observation that animals in tropical regions, where ticks are active for long time periods tend to harbor multiple A. marginale strains, while animals in temperate regions, where ticks are active for short time periods, tend to harbor only a single strain of A. marginale.

Technical Abstract: The remarkable genetic diversity of vector-borne pathogens allows for the establishment of superinfection in the mammalian host. To have a long-term impact on population strain structure, the introduced strains must also be transmitted by a vector population that has been exposed to the existing primary strain. The sequential exposure of the vector to multiple strains frequently prevents establishment of the second strain, a phenomenon termed superinfection exclusion. As a consequence, uniform exclusion may greatly limit genetic diversity in the host population, which is difficult to reconcile with the high degree of genetic diversity maintained among vector-borne pathogens. Using Anaplasma marginale, a tick-borne bacterial pathogen of ruminants, we hypothesized that superinfection exclusion is temporally dependent and that longer time intervals between strain exposure allows successful acquisition and transmission of a superinfecting strain. To test this hypothesis, Dermacentor andersoni ticks were sequentially exposed to two readily tick transmissible strains of A. marginale. The tick feedings were either immediately sequential or 28 days apart. Ticks were allowed to transmission feed and were individually assessed to determine if they were infected with one or both strains. The second strain was excluded from the tick when the exposure interval was brief, but not prolonged. Midguts and salivary glands of individual ticks were super-infected and transmission of both strains occurred only when the exposure interval was prolonged. These findings indicate that superinfection exclusion is temporally dependent and helps account for the differences in pathogen strain structure in tropical as compared to temperate regions.