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Infect. Immun. doi:10.1128/IAI.00284-07
Copyright (c) 2007, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.

Identification of midgut and salivary glands as specific and distinct barriers to efficient tick-borne transmission of Anaplasma marginale

Massaro W. Ueti*, James O. Reagan Jr., Donald P. Knowles Jr., Glen A. Scoles, Varda Shkap, and Guy H. Palmer

Program in Vector-borne Diseases, Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, Washington, Animal Diseases Research Unit, U.S. Department of Agriculture-Agricultural Research Service, Pullman, Washington, Division of Parasitology, Kimron Veterinary Institute, Bet Dagan, Israel

* To whom correspondence should be addressed. Email: massaro{at}vetmed.wsu.edu.


   Abstract

Understanding the determinants of efficient tick-borne microbial transmission is needed to better predict the emergence of highly transmissible pathogen strains and disease outbreaks. Although the basic developmental cycle of Anaplasma and Ehrlichia spp. within the tick has been delineated, there are marked differences in the ability of specific strains to be efficiently tick transmitted. Using the highly transmissible St. Maries strain of A. marginale in Dermacentor andersoni as a positive control and two unrelated non-transmissible strains, we identified distinct barriers to efficient transmission within the tick. The Mississippi strain was unable to establish infection at the level of midgut epithelium despite successful ingestion of infected blood following acquisition feeding on a bacteremic animal host. This inability to colonize the midgut epithelium prevented subsequent development within the salivary glands and transmission. In contrast, A. marginale ss. centrale colonized the midgut and then the salivary glands, replicating to a titer indistinguishable from that of the highly transmissible St. Maries strain and at least 100x greater than that previously associated with successful transmission. Nonetheless, A. marginale ss. centrale was not transmitted, even using a large number of infected ticks for transmission feeding. These results establish that there are at least two specific barriers, the midgut and salivary glands, to efficient tick-borne transmission, and highlight the complexity of the pathogen-tick interaction.




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