Yersinia–flea interactions and the evolution of the arthropod-borne transmission route of plague

Yersinia pestis, the causative agent of plague, is unique among the enteric group of Gram-negative bacteria in relying on a blood-feeding insect for transmission. The Yersinia–flea interactions that enable plague transmission cycles have had profound historical consequences as manifested by human plague pandemics. The arthropod-borne transmission route was a radical ecologic change from the food-borne and water-borne transmission route of Yersinia pseudotuberculosis, from which Y. pestis diverged only within the last 20 000 years. Thus, the interactions of Y. pestis with its flea vector that lead to colonization and successful transmission are the result of a recent evolutionary adaptation that required relatively few genetic changes. These changes from the Y. pseudotuberculosis progenitor included loss of insecticidal activity, increased resistance to antibacterial factors in the flea midgut, and extending Yersinia biofilm-forming ability to the flea host environment.

► Flea-borne transmission of Yersinia pestis is a recent evolutionary phenomenon. ► Y. pestis biofilm formation in the flea gut is important for transmission. ► Y. pestis biofilm requires hms genes and enzymes controlling c-di-GMP levels. ► Y. pestis regulates its gene expression to specifically adapt to the flea vector. ► Gene gain and gene loss contributed to the evolution of flea-borne transmission.