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Low temperature effects on the transcriptome of Yersinia pestis and its transmissibility by Oropsylla montana fleas




Williams, Shanna K., author
Borlee, Brad, advisor
Bearden, Scott, advisor
Gage, Ken, committee member
Stenglein, Mark, committee member
Archibeque, Shawn, committee member

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Yersinia pestis, the causative agent of plague, is primarily a rodent-associated, flea-borne zoonosis. Transmission to humans is mediated most commonly by the flea vector, Oropsylla montana, and occurs predominantly in the Southwestern United States. In these studies, we hypothesized that Y. pestis-infected O. montana fleas held at temperatures as low as 6ºC could serve as reservoirs of the plague bacillus during the winter months in temperate regions with endemic plague foci. With few exceptions, previous studies showed O. montana to be an inefficient vector at transmitting Y. pestis at 22-23°C particularly when such fleas were fed on susceptible hosts more than a few days after ingesting an infectious blood meal. We examined whether holding fleas at sub-ambient temperatures (for purposes of these studies, ambient temperature is defined as 23°C) affected the transmissibility of Y. pestis by this vector. Colony-reared O. montana fleas were given an infectious blood meal containing a virulent Y. pestis strain (CO96-3188), and potentially infected fleas were maintained at different temperatures (6ºC, 10°C, 15°C, or 23ºC). Transmission efficiencies were tested by allowing groups of ~15 infectious fleas to feed on each of seven naïve CD-1 mice on days 1-4, 7, 10, 14, 17, and 21, 28, 35, and 42 post infection (p.i.). Fleas held at 6ºC, 10°C and 15°C were able to effectively transmit at every time point p.i. The percentage of transmission to naïve mice by fleas maintained at low temperatures was higher than for fleas maintained at 23ºC and indicates that O. montana fleas efficiently transmit Y. pestis at low temperatures. Moreover, bacterial loads of flea cohorts maintained at temperatures of 6ºC, 10ºC and 15ºC were statistically higher than fleas maintained at 23ºC. In addition, whole transcriptomes of Y. pestis bacteria grown at 6ºC, 10°C, 15°C and 23ºC were analyzed to assess differential gene expression at each temperature to identify genes which may contribute to an increase in virulence or survivability of the plague pathogen at the lower temperatures when compared to ambient temperature. This is the first comprehensive study to demonstrate efficient transmission of Y. pestis by O. montana fleas maintained at temperatures as low as 6ºC. Our findings further contribute to the understanding of plague ecology in temperate climates by providing support for the hypothesis that Y. pestis is able to overwinter within the flea gut and potentially cause infection during the following transmission season. The findings also might hold implications for explaining the focality of plague in tropical regions where plague occurs in cooler environments, primarily located at higher elevations.


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