Infectious blood source alters early foregut infection and regurgitative transmission of Yersinia pestis by rodent fleas

Abstract

Fleas can transmit Yersinia pestis by two mechanisms, early-phase transmission (EPT) and biofilm-dependent transmission (BDT). Transmission efficiency varies among flea species and the results from different studies have not always been consistent. One complicating variable is the species of rodent blood used for the infectious blood meal. To gain insight into the mechanism of EPT and the effect that host blood has on it, fleas were fed bacteremic mouse, rat, guinea pig, or gerbil blood; and the location and characteristics of the infection in the digestive tract and transmissibility of Y. pestis were assessed 1 to 3 days after infection. Surprisingly, 10–28% of two rodent flea species fed bacteremic rat or guinea pig blood refluxed a portion of the infected blood meal into the esophagus within 24 h of feeding. We term this phenomenon post-infection esophageal reflux (PIER). In contrast, PIER was rarely observed in rodent fleas fed bacteremic mouse or gerbil blood. PIER correlated with the accumulation of a dense mixed aggregate of Y. pestis, red blood cell stroma, and oxyhemoglobin crystals that filled the proventriculus. At their next feeding, fleas with PIER were 3–25 times more likely to appear partially blocked, with fresh blood retained within the esophagus, than were fleas without PIER. Three days after feeding on bacteremic rat blood, groups of Oropsylla montana transmitted significantly more CFU than did groups infected using mouse blood, and this enhanced transmission was biofilm-dependent. Our data support a model in which EPT results from regurgitation of Y. pestis from a partially obstructed flea foregut and that EPT and BDT can sometimes temporally overlap. The relative insolubility of the hemoglobin of rats and Sciurids and the slower digestion of their blood appears to promote regurgitative transmission, which may be one reason why these rodents are particularly prominent in plague ecology.

To block or not to block: The adaptive manipulation of plague transmission

“…Besides, the infectious blood source is also known to affect the development of Y. pestis in the fleas (Bland et al. ). A full understanding of the ecology and evolution of the plague thus requires a more comprehensive description of the network of host and vector species involved in its transmission.…”

“…Yet, the competence of fleas, their propensity to develop blockage, and their mortality rates (after blockage) are known to differ widely (Bland and Hinnebusch 2016;. Besides, the infectious blood source is also known to affect the development of Y. pestis in the fleas (Bland et al 2018). A full understanding of the ecology and evolution of the plague thus requires a more comprehensive description of the network of host and vector species involved in its transmission.…”

Ancient pathogen genomics as an emerging tool for infectious disease research

“…Nevertheless, an alternative mode of flea transmis sion, termed the early phase transmission, which occurs during the initial phases of infection and was suggested to be biofilm independent 161 , should also be considered as a possible way of Y. pestis propagation during its early evolution 34 . Although this transmission mechanism is currently not well understood, its comparative mode and efficiency in different rodent species have recently started to be assessed 162 evidence showing the full capacity for flea colonization similar to modern and historic strains was identified in two 3,800year old skeletons from the Samara region of modern day Russia 37 . Although this strain was shown to occupy a phylogenetic position among modern Y. pestis lineages (Fig.…”

Evolutionary selection of biofilm-mediated extended phenotypes in Yersinia pestis in response to a fluctuating environment

“…For mice, normal levels of biofilm formation, or even the complete absence of biofilm formation do not seem to negatively impact early-phase transmission 4 , while they do negatively impact blockage-induced transmission. In rats and guinea pigs, low or absent levels of biofilm formation also negatively impact early-phase transmission, as some degree of biofilm formation appears to be involved in an interaction between host blood and Y. pestis that drastically boosts the efficiency of early-phase transmission 7 . In addition, at reduced levels of biofilm production, more fleas will be at a stage of partial, rather than complete blockage of the proventriculus.…”