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Title: Quantitative Differences in Salivary Pathogen Load during Tick Transmission Underlie Strain-Specific Variation in Transmission Efficiency of Anaplasma marginale

item Knowles Jr, Donald
item Scoles, Glen

Submitted to: Infection and Immunity
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/20/2008
Publication Date: 1/2/2009
Citation: Ueti, M.W., Knowles Jr, 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. Infection and Immunity. 77(1):70-75.

Interpretive Summary: Strains of the tick-borne cattle pathogen Anaplasma marginale differ in the efficiency with which they are transmitted by their vector ticks. Some strains are transmitted very efficiently, while others may be transmitted poorly, or not at all. This is referred to as the "transmission efficiency phenotype" of a strain. The transmission efficiency phenotypes of the Anaplasma strains circulating in a population can affect the proportion of the cattle that is infected with each particular strain, the "pathogen strain structure" of the population. We have worked with two strains of A. marginale that have very different transmission efficiency phenotypes, the St. Maries strain, which is transmitted very efficiently, and the Israel vaccine strain which has a low transmission efficiency. The primary difference between these two strains is in how they infect the tick salivary glands. We have suggested two different possible explanations for the differences in transmission efficiency between the St. Maries and Israel vaccine strains: 1) Both are secrete equally in the saliva but one is intrinsically more infectious to cattle than the other, or 2) St. Maries is secreted at a significantly higher level than Israel vaccine and so each tick bite delivers a higher dose of St. Maries. Our data shows that organisms from the salivary glands of each tick are equally infectious for cattle. However, St Maries infects a significantly greater number of ticks and in these ticks it replicates to a significantly higher level compared to the Israel vaccine strain. The vaccine strain could be transmitted to cattle by increasing the dose delivered, either by dissecting tick salivary glands and injecting organisms isolated from them, or by feeding a larger number if vaccine strain infected ticks on the host. Microscopic examination showed that there were differences in the way that the two different strains infected the tick salivary glands and we suggest that these differences may be responsible for the strain specific differences in the transmission efficiency phenotypes.

Technical Abstract: The relative fitness of arthropod-borne pathogens within the vector can be a major determinant of pathogen prevalence within the mammalian host population. Strains of the tick-borne rickettsia Anaplasma marginale differ markedly in transmission efficiency with consequent impact on pathogen strain structure. We have identified two A. marginale strains with significant differences in transmission phenotype that are effected following infection of the salivary gland. We have proposed competing hypotheses to explain the phenotypes: i) both strains are secreted equally but there is an intrinsic difference in infectivity for the mammalian host; or ii) one strain is secreted at a significantly higher level and thus represents delivery of a greater pathogen dose. Quantitative analysis of pathogen replication and secretion revealed that the high efficiency St. Maries strain replicated to a 10-fold higher titer and a significantly greater percentage of infected ticks secreted A. marginale into the saliva and at a significantly higher level as compared to the low efficiency Israel vaccine strain. Furthermore the transmission phenotype of the vaccine strain could be restored to that of the St. Maries strain simply by increasing the delivered pathogen dose, either by direct inoculation of salivary gland organisms or by increasing the number of ticks during transmission feeding. We identified morphologic differences in the colonization of each strain within the salivary glands and propose that these reflect strain-specific differences in replication and secretion pathways linked to the vector-pathogen interaction.