Single-Nucleotide Polymorphisms Reveal Spatial Diversity Among Clones ofYersinia pestisDuring Plague Outbreaks in Colorado and the Western United States

Abstract

Background: In western North America, plague epizootics caused by Yersinia pestis appear to sweep across landscapes, primarily infecting and killing rodents, especially ground squirrels and prairie dogs. During these epizootics, the risk of Y. pestis transmission to humans is highest. While empirical models that include climatic conditions and densities of rodent hosts and fleas can predict when epizootics are triggered, bacterial transmission patterns across landscapes, and the scale at which Y. pestis is maintained in nature during interepizootic periods, are poorly defined. Elucidating the spatial extent of Y. pestis clones during epizootics can determine whether bacteria are propagated across landscapes or arise independently from local inter-epizootic maintenance reservoirs. Material and Methods: We used DNA microarray technology to identify single-nucleotide polymorphisms (SNPs) in 34 Y. pestis isolates collected in the western United States from 1980 to 2006, 21 of which were collected during plague epizootics in Colorado. Phylogenetic comparisons were used to elucidate the hypothesized spread of Y. pestis between the mountainous Front Range and the eastern plains of northern Colorado during epizootics. Isolates collected from across the western United States were included for regional comparisons. Results: By identifying SNPs that mark individual clones, our results strongly suggest that Y. pestis is maintained locally and that widespread epizootic activity is caused by multiple clones arising independently at small geographic scales. This is in contrast to propagation of individual clones being transported widely across landscapes. Regionally, our data are consistent with the notion that Y. pestis diversifies at relatively local scales following long-range translocation events. We recommend that surveillance and prediction by public health and wildlife management professionals focus more on models of local or regional weather patterns and ecological factors that may increase risk of widespread epizootics, rather than predicting or attempting to explain epizootics on the basis of movement of host species that may transport plague.

Investigation of and Response to 2 Plague Cases, Yosemite National Park, California, USA, 2015

“…Previous findings indicate that Y. pestis whole-genome MLST alleles are not rapidly changing and that most detected changes are caused by the more slowly evolving SNPs than by more rapidly changing variable number tandem repeats ( 24 ). Our results are consistent with those of a previous SNP-based study, which indicated that widespread plague epizootics are caused by multiple Y. pestis clones arising independently in small geographic areas ( 31 ). …”

Factors that affect parasitism of black‐tailed prairie dogs by fleas

“…, Lowell et al. , Mize ) and causes relatively low, chronic rates of mortality within colonies during enzootic periods (Biggins et al. ) and occasional sudden, far‐reaching die‐offs during epizootic outbreaks (Eads and Biggins ).…”

Spores and soil from six sides: interdisciplinarity and the environmental biology of anthrax (Bacillus anthracis)

“…For example, recent work has confirmed that Mycoplasma bovis , a bacterial pathogen associated with mastitis in cattle and bison ( Bison bison ), can persist for long periods and possibly replicate, most likely through the formation of biofilms associated with gram‐negative bacteria, in sandy soil used as cattle bedding under certain moisture conditions (Justice‐Allen et al ., ). Similarly, plague ( Yersinia pestis ), conventionally studied as a vector‐borne disease, recently has been shown to persist in the soil for weeks – although the importance of this to the ecology and epidemiology of plague is still controversial (Lowell et al ., ).…”

“…Environmental maintenance has a substantial effect on epidemiological dynamics even when only a small part of a pathogen life cycle; for instance, Lowell et al . () demonstrated that widespread plague epizootics are driven by local persistence in the soil for up to weeks at a time, a finding that can inform anticipatory surveillance of local factors (e.g. climate) known to increase plague outbreak risk.…”

“…From an eco-epidemiological angle, the role of environmental transmission in pathogen dynamics remains understudied and rarely modelled, especially in the case of diseases for which environmental transmission is not the primary mode of transmission (Saad-Roy, van den Driessche for generalist bacterial pathogens like anthrax (Almberg et al, 2011;Ivanek & Lahodny, 2015). Environmental maintenance has a substantial effect on epidemiological dynamics even when only a small part of a pathogen life cycle; for instance, Lowell et al (2015) demonstrated that widespread plague epizootics are driven by local persistence in the soil for up to weeks at a time, a finding that can inform anticipatory surveillance of local factors (e.g. climate) known to increase plague outbreak risk.…”