Environmental and Host Blood Interactions Shape Yersinia pestis Dynamics in the Rat Flea, Xenopsylla cheopis

Yersinia pestis is the causative agent of bubonic plague, a zoonotic disease that is primarily transmitted by infectious fleas. Plague is endemic in regions around the world, including the United States, where optimal climate conditions support a stable, enzootic sylvatic transmission cycle. Epizootic outbreaks periodically occur with rapid spread of disease that increases the risk of human exposure. As fleas are ectotherms that are responsive to environmental conditions, it is likely that transmission efficiency varies under different ecological conditions, with optimal conditions capable of supporting rapid spread of disease while sub-optimal conditions may promote lower levels of transmission. To test this, we experimentally infected Xenopsylla cheopis with Y. pestis using a membrane feeder in order to define the impact of varying temperature, humidity and mammalian blood sources on infection and transmission. We show that environmental factors and host blood source are key factors influencing colonization, bacterial aggregation, and transmission rates, with variation in the responses seen depending on the experimental conditions. The combined data illustrate the impact of ecological factors on Y. pestis flea infection and suggests that optimal conditions involving the vector–host–pathogen interface are needed for enhanced transmission rates and the rapid spread of infection that occurs during epizootic outbreaks.