Comparative Ability of Oropsylla montana and Xenopsylla cheopis Fleas to Transmit Yersinia pestis by Two Different Mechanisms

The ability of the agent of plague, Yersinia pestis , to form a biofilm blocking the gut of the flea has been considered to be a key evolutionary step in maintaining flea‐borne transmission. However, blockage decreases dramatically the life expectancy of fleas, challenging the adaptive nature of blockage. Here, we develop an epidemiological model of plague that accounts for its different transmission routes, as well as the within‐host competition taking place between bacteria within the flea vector. We use this theoretical framework to identify the environmental conditions promoting the evolution of blockage. We also show that blockage is favored at the onset of an epidemic, and that the frequencies of bacterial strains exhibiting different strategies of blockage can fluctuate in seasonal environments. This analysis quantifies the contribution of different transmission routes in plague and makes testable predictions on the adaptive nature of blockage.

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“…; Hinnebusch et al. ). Besides, the infectious blood source is also known to affect the development of Y. pestis in the fleas (Bland et al.…”

Section: Discussionmentioning

confidence: 97%

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

2019

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“…5). The best yet characterized is the oriental rat flea, Xenopsylla cheopis, although others are also known to play important roles in Y. pestis transmission 142,144,146 . Notably, recent modelling infer ences suggest important roles for ectoparasites such as body lice and human fleas in its propagation during human epidemics 147 .…”

Section: Not a Human Pathogen: Plague Ecologymentioning

confidence: 99%

Ancient pathogen genomics as an emerging tool for infectious disease research

et al. 2019

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| Over the past decade, a genomics revolution, made possible through the development of high-throughput sequencing, has triggered considerable progress in the study of ancient DNA , enabling complete genomes of past organisms to be reconstructed. A newly established branch of this field, ancient pathogen genomics, affords an in-depth view of microbial evolution by providing a molecular fossil record for a number of human-associated pathogens. Recent accomplishments include the confident identification of causative agents from past pandemics, the discovery of microbial lineages that are now extinct, the extrapolation of past emergence events on a chronological scale and the characterization of long-term evolutionary history of microorganisms that remain relevant to public health today. In this Review , we discuss methodological advancements, persistent challenges and novel revelations gained through the study of ancient pathogen genomes.

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“…At that time point, the bacteria have begun to multiply and form multicellular aggregates in the midgut and proventriculus, but mature biofilm has not yet developed (4). By 14 days, the blockage is at its peak incidence (5,13,21 (Fig. S2).…”

Section: Resultsmentioning

confidence: 99%

Differential Gene Expression Patterns of Yersinia pestis and Yersinia pseudotuberculosis during Infection and Biofilm Formation in the Flea Digestive Tract

et al. 2019

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Yersinia pestis, the etiologic agent of plague, emerged as a fleaborne pathogen only within the last 6,000 years. Just five simple genetic changes in the Yersinia pseudotuberculosis progenitor, which served to eliminate toxicity to fleas and to enhance survival and biofilm formation in the flea digestive tract, were key to the transition to the arthropodborne transmission route. To gain a deeper understanding of the genetic basis for the development of a transmissible biofilm infection in the flea foregut, we evaluated additional gene differences and performed in vivo transcriptional profiling of Y. pestis, a Y. pseudotuberculosis wild-type strain (unable to form biofilm in the flea foregut), and a Y. pseudotuberculosis mutant strain (able to produce foregut-blocking biofilm in fleas) recovered from fleas 1 day and 14 days after an infectious blood meal. Surprisingly, the Y. pseudotuberculosis mutations that increased c-di-GMP levels and enabled biofilm development in the flea did not change the expression levels of the hms genes responsible for the synthesis and export of the extracellular polysaccharide matrix required for mature biofilm formation. The Y. pseudotuberculosis mutant uniquely expressed much higher levels of Yersinia type VI secretion system 4 (T6SS-4) in the flea, and this locus was required for flea blockage by Y. pseudotuberculosis but not for blockage by Y. pestis. Significant differences between the two species in expression of several metabolism genes, the Psa fimbrial genes, quorum sensing-related genes, transcription regulation genes, and stress response genes were evident during flea infection. IMPORTANCE Y. pestis emerged as a highly virulent, arthropod-transmitted pathogen on the basis of relatively few and discrete genetic changes from Y. pseudotuberculosis. Parallel comparisons of the in vitro and in vivo transcriptomes of Y. pestis and two Y. pseudotuberculosis variants that produce a nontransmissible infection and a transmissible infection of the flea vector, respectively, provided insights into how Y. pestis has adapted to life in its flea vector and point to evolutionary changes in the regulation of metabolic and biofilm development pathways in these two closely related species.

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Comparative Ability of Oropsylla montana and Xenopsylla cheopis Fleas to Transmit Yersinia pestis by Two Different Mechanisms

Cited by 36 publications

References 38 publications

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

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

Ancient pathogen genomics as an emerging tool for infectious disease research

Differential Gene Expression Patterns of Yersinia pestis and Yersinia pseudotuberculosis during Infection and Biofilm Formation in the Flea Digestive Tract

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