1887

Abstract

Plague, caused by , is characterized by quiescent periods punctuated by rapidly spreading epizootics. The classical ‘blocked flea’ paradigm, by which a blockage forms in the flea’s proventriculus on average 1–2 weeks post-infection (p.i.), forces starving fleas to take multiple blood meals, thus increasing opportunities for transmission. Recently, the importance of early-phase transmission (EPT), which occurs prior to blockage formation, has been emphasized during epizootics. Whilst the physiological and molecular mechanisms of blocked flea transmission are well characterized, the pathogen–vector interactions have not been elucidated for EPT. Within the blocked flea model, murine toxin (Ymt) has been shown to be important for facilitating colonization of the midgut within the flea. One proposed mechanism of EPT is the regurgitation of infectious material from the flea midgut during feeding. Such a mechanism would require bacteria to colonize and survive for at least brief periods in the midgut, a process that is mediated by Ymt. Two key bridging vectors of to humans, (Siphonaptera: Ceratophyllidae) or (Siphonaptera: Pulicidae), were used in our study to test this hypothesis. Fleas were infected with a mutant strain of containing a non-functional that was shown previously to be incapable of colonizing the midgut and were then allowed to feed on SKH-1 mice 3 days p.i. Our results show that Ymt was not required for EPT by either flea species.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.082123-0
2014-11-01
2021-02-27
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/11/2517.html?itemId=/content/journal/micro/10.1099/mic.0.082123-0&mimeType=html&fmt=ahah

References

  1. Ajl S. J., Reedal J. S., Durrum E. L., Warren J. ( 1955). Studies on plague. I. Purification and properties of the toxin of Pasteurella pestis . J Bacteriol 70:158–169[PubMed]
    [Google Scholar]
  2. Bacot A. W., Martin C. J. ( 1914). LXVII. Observations on the mechanism of the transmission of plague by fleas. J Hyg (Lond) 13:Suppl423–439[PubMed]
    [Google Scholar]
  3. Barnes A. M. ( 1982). Surveillance and control of bubonic plague in the United States. Symp Zool Soc Lond 50:237–270[PubMed]
    [Google Scholar]
  4. Biggerstaff B. J. ( 2009). PooledInfRate, Version 4.0: A Microsoft® Office Excel© Add-In to Compute Prevalence Estimates from Pooled Samples Fort Collins, CO: CDC;
    [Google Scholar]
  5. Burroughs A. L. ( 1947). Sylvatic plague studies. The vector efficiency of nine species of fleas compared to Xenopsylla cheopsis . J. Hyg (Lond) 45:371–396[PubMed] [CrossRef]
    [Google Scholar]
  6. Chu M. C. ( 2000). Laboratory Manual of Plague Diagnostics Geneva: CDC/WHO;
    [Google Scholar]
  7. Drancourt M., Houhamdi L., Raoult D. ( 2006). Yersinia pestis as a telluric, human ectoparasite-borne organism. Lancet Infect Dis 6:234–241 [CrossRef][PubMed]
    [Google Scholar]
  8. Eisen R. J., Gage K. L. ( 2009). Adaptive strategies of Yersinia pestis to persist during inter-epizootic and epizootic periods. Vet Res 40:01 [CrossRef][PubMed]
    [Google Scholar]
  9. Eisen R. J., Bearden S. W., Wilder A. P., Montenieri J. A., Antolin M. F., Gage K. L. ( 2006). Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics. Proc Natl Acad Sci U S A 103:15380–15385 [CrossRef][PubMed]
    [Google Scholar]
  10. Eisen R. J., Lowell J. L., Montenieri J. A., Bearden S. W., Gage K. L. ( 2007a). Temporal dynamics of early-phase transmission of Yersinia pestis by unblocked fleas: secondary infectious feeds prolong efficient transmission by Oropsylla montana (Siphonaptera: Ceratophyllidae). J Med Entomol 44:672–677 [CrossRef][PubMed]
    [Google Scholar]
  11. Eisen R. J., Wilder A. P., Bearden S. W., Montenieri J. A., Gage K. L. ( 2007b). Early-phase transmission of Yersinia pestis by unblocked Xenopsylla cheopis (Siphonaptera: Pulicidae) is as efficient as transmission by blocked fleas. J Med Entomol 44:678–682 [CrossRef][PubMed]
    [Google Scholar]
  12. Eisen R. J., Borchert J. N., Holmes J. L., Amatre G., Van Wyk K., Enscore R. E., Babi N., Atiku L. A., Wilder A. P. & other authors ( 2008a). Early-phase transmission of Yersinia pestis by cat fleas (Ctenocephalides felis) and their potential role as vectors in a plague-endemic region of Uganda. Am J Trop Med Hyg 78:949–956[PubMed]
    [Google Scholar]
  13. Eisen R. J., Holmes J. L., Schotthoefer A. M., Vetter S. M., Montenieri J. A., Gage K. L. ( 2008b). Demonstration of early-phase transmission of Yersinia pestis by the mouse flea, Aetheca wagneri (Siphonaptera: Ceratophylidae), and implications for the role of deer mice as enzootic reservoirs. J Med Entomol 45:1160–1164 [CrossRef][PubMed]
    [Google Scholar]
  14. Eisen R. J., Eisen L., Gage K. L. ( 2009). Studies of vector competency and efficiency of North American fleas for Yersinia pestis: state of the field and future research needs. J Med Entomol 46:737–744 [CrossRef][PubMed]
    [Google Scholar]
  15. Engelthaler D. M., Hinnebusch B. J., Rittner C. M., Gage K. L. ( 2000). Quantitative competitive PCR as a technique for exploring flea–Yersinia pestis dynamics. Am J Trop Med Hyg 62:552–560[PubMed]
    [Google Scholar]
  16. Eskey C. R. ( 1938). Fleas as vectors of plague. Am J Public Health Nations Health 28:1305–1310 [CrossRef][PubMed]
    [Google Scholar]
  17. Fetherston J. D., Schuetze P., Perry R. D. ( 1992). Loss of the pigmentation phenotype in Yersinia pestis is due to the spontaneous deletion of 102 kb of chromosomal DNA which is flanked by a repetitive element. Mol Microbiol 6:2693–2704 [CrossRef][PubMed]
    [Google Scholar]
  18. Furman D. P., Catts E. P. ( 1982). Manual of Medical Entomology New York: Cambridge University Press.;
    [Google Scholar]
  19. Gage K. L., Kosoy M. Y. ( 2005). Natural history of plague: perspectives from more than a century of research. Annu Rev Entomol 50:505–528 [CrossRef][PubMed]
    [Google Scholar]
  20. Gong S., Bearden S. W., Geoffroy V. A., Fetherston J. D., Perry R. D. ( 2001). Characterization of the Yersinia pestis Yfu ABC inorganic iron transport system. Infect Immun 69:2829–2837 [CrossRef][PubMed]
    [Google Scholar]
  21. Graham C. B., Woods M. E., Vetter S. M., Peterson J. M., Montenieri J. A., Holmes J. L., Maes S. E., Bearden S. W., Gage K. L., Eisen R. J. ( 2014). Evaluation of the effect of host immune status on short-term Yersinia pestis infection in flea with implications for the enzootic host model for maintenance of Y. pestis during interepizootic periods. J Med Entomol 51:1079–1086 [CrossRef]
    [Google Scholar]
  22. Hinnebusch B. J. ( 2012). Biofilm-dependent and biofilm-independent mechanisms of transmission of Yersinia pestis by fleas. Adv Exp Med Biol 954:237–243 [CrossRef][PubMed]
    [Google Scholar]
  23. Hinnebusch B. J., Perry R. D., Schwan T. G. ( 1996). Role of the Yersinia pestis hemin storage (hms) locus in the transmission of plague by fleas. Science 273:367–370 [CrossRef][PubMed]
    [Google Scholar]
  24. Hinnebusch B. J., Fischer E. R., Schwan T. G. ( 1998). Evaluation of the role of the Yersinia pestis plasminogen activator and other plasmid-encoded factors in temperature-dependent blockage of the flea. J Infect Dis 178:1406–1415 [CrossRef][PubMed]
    [Google Scholar]
  25. Hinnebusch J., Cherepanov P., Du Y., Rudolph A., Dixon J. D., Schwan T., Forsberg A. ( 2000). Murine toxin of Yersinia pestis shows phospholipase D activity but is not required for virulence in mice. Int J Med Microbiol 290:483–487 [CrossRef][PubMed]
    [Google Scholar]
  26. Hinnebusch B. J., Rudolph A. E., Cherepanov P., Dixon J. E., Schwan T. G., Forsberg A. ( 2002). Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science 296:733–735 [CrossRef][PubMed]
    [Google Scholar]
  27. Jones H. A., Lillard J. W. Jr, Perry R. D. ( 1999). HmsT, a protein essential for expression of the haemin storage (Hms+) phenotype of Yersinia pestis . Microbiology 145:2117–2128 [CrossRef][PubMed]
    [Google Scholar]
  28. Kado C. I., Liu S. T. ( 1981). Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol 145:1365–1373[PubMed]
    [Google Scholar]
  29. Kirillina O., Fetherston J. D., Bobrov A. G., Abney J., Perry R. D. ( 2004). HmsP, a putative phosphodiesterase, and HmsT, a putative diguanylate cyclase, control Hms-dependent biofilm formation in Yersinia pestis . Mol Microbiol 54:75–88 [CrossRef][PubMed]
    [Google Scholar]
  30. Lorange E. A., Race B. L., Sebbane F., Hinnebusch B. J. ( 2005). Poor vector competence of fleas and the evolution of hypervirulence in Yersinia pestis . J Infect Dis 191:1907–1912 [CrossRef][PubMed]
    [Google Scholar]
  31. Perry R. D., Pendrak M. L., Schuetze P. ( 1990). Identification and cloning of a hemin storage locus involved in the pigmentation phenotype of Yersinia pestis . J Bacteriol 172:5929–5937[PubMed]
    [Google Scholar]
  32. Plague Commission ( 1907). XV. Further observations on the transmission of plague by fleas, with special reference to the fate of the plague bacillus in the body of the rat flea (P. cheopis). J Hyg (Lond) 7:395–420 [CrossRef][PubMed]
    [Google Scholar]
  33. Politzer R. ( 1954). Plague Geneva: World Health Organization;
    [Google Scholar]
  34. Rudolph A. E., Stuckey J. A., Zhao Y., Matthews H. R., Patton W. A., Moss J., Dixon J. E. ( 1999). Expression, characterization, and mutagenesis of the Yersinia pestis murine toxin, a phospholipase D superfamily member. J Biol Chem 274:11824–11831 [CrossRef][PubMed]
    [Google Scholar]
  35. Vetter S. M., Eisen R. J., Schotthoefer A. M., Montenieri J. A., Holmes J. L., Bobrov A. G., Bearden S. W., Perry R. D., Gage K. L. ( 2010). Biofilm formation is not required for early-phase transmission of Yersinia pestis . Microbiology 156:2216–2225 [CrossRef][PubMed]
    [Google Scholar]
  36. Webb C. T., Brooks C. P., Gage K. L., Antolin M. F. ( 2006). Classic flea-borne transmission does not drive plague epizootics in prairie dogs. Proc Natl Acad Sci U S A 103:6236–6241 [CrossRef][PubMed]
    [Google Scholar]
  37. Wilder A. P., Eisen R. J., Bearden S. W., Montenieri J. A., Gage K. L., Antolin M. F. ( 2008a). Oropsylla hirsuta (Siphonaptera: Ceratophyllidae) can support plague epizootics in black-tailed prairie dogs (Cynomys ludovicianus) by early-phase transmission of Yersinia pestis . Vector Borne Zoonotic Dis 8:359–368 [CrossRef][PubMed]
    [Google Scholar]
  38. Wilder A. P., Eisen R. J., Bearden S. W., Montenieri J. A., Tripp D. W., Brinkerhoff R. J., Gage K. L., Antolin M. F. ( 2008b). Transmission efficiency of two flea species (Oropsylla tuberculata cynomuris and Oropsylla hirsuta) involved in plague epizootics among prairie dogs. EcoHealth 5:205–212 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.082123-0
Loading
/content/journal/micro/10.1099/mic.0.082123-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error