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Infection and Immunity, June 2007, p. 2959-2964, Vol. 75, No. 6
0019-9567/07/$08.00+0     doi:10.1128/IAI.00284-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Identification of Midgut and Salivary Glands as Specific and Distinct Barriers to Efficient Tick-Borne Transmission of Anaplasma marginale{triangledown}

Massaro W. Ueti,1* James O. Reagan Jr.,1,2 Donald P. Knowles Jr.,1,2 Glen A. Scoles,2 Varda Shkap,3 and Guy H. Palmer1

Program in Vector-borne Diseases, Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, Washington,1 Animal Diseases Research Unit, U.S. Department of Agriculture, Agricultural Research Service, Pullman, Washington,2 Division of Parasitology, Kimron Veterinary Institute, Bet Dagan, Israel3

Received 20 February 2007/ Returned for modification 27 March 2007/ Accepted 30 March 2007

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 Anaplasma marginale in Dermacentor andersoni as a positive control and two unrelated nontransmissible strains, we identified distinct barriers to efficient transmission within the tick. The Mississippi strain was unable to establish infection at the level of the 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 subsp. 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 100 times greater than that previously associated with successful transmission. Nonetheless, A. marginale subsp. centrale was not transmitted, even when a large number of infected ticks was used for transmission feeding. These results establish that there are at least two specific barriers to efficient tick-borne transmission, the midgut and salivary glands, and highlight the complexity of the pathogen-tick interaction.

* Corresponding author. Mailing address: Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, WA 99164-7040. Phone: (509) 335-6325. Fax: (509) 335-8529. E-mail: massaro{at}vetmed.wsu.edu

{triangledown} Published ahead of print on 9 April 2007.

Editor: R. P. Morrison

Infection and Immunity, June 2007, p. 2959-2964, Vol. 75, No. 6
0019-9567/07/$08.00+0     doi:10.1128/IAI.00284-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Galletti, M. F. B. M., Ueti, M. W., Knowles, D. P. Jr., Brayton, K. A., Palmer, G. H. (2009). Independence of Anaplasma marginale Strains with High and Low Transmission Efficiencies in the Tick Vector following Simultaneous Acquisition by Feeding on a Superinfected Mammalian Reservoir Host. Infect. Immun. 77: 1459-1464 [Abstract] [Full Text]  
  • Ueti, M. W., Knowles, D. P., Davitt, C. M., Scoles, G. A., Baszler, T. V., Palmer, G. H. (2009). Quantitative Differences in Salivary Pathogen Load during Tick Transmission Underlie Strain-Specific Variation in Transmission Efficiency of Anaplasma marginale. Infect. Immun. 77: 70-75 [Abstract] [Full Text]  
  • Leverich, C. K., Palmer, G. H., Knowles, D. P. Jr., Brayton, K. A. (2008). Tick-Borne Transmission of Two Genetically Distinct Anaplasma marginale Strains following Superinfection of the Mammalian Reservoir Host. Infect. Immun. 76: 4066-4070 [Abstract] [Full Text]  


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