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Infection and Immunity, March 2009, p. 1222-1229, Vol. 77, No. 3
0019-9567/09/$08.00+0     doi:10.1128/IAI.00950-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

The Yersinia pestis caf1M1A1 Fimbrial Capsule Operon Promotes Transmission by Flea Bite in a Mouse Model of Bubonic Plague{triangledown}

Florent Sebbane,1* Clayton Jarrett,2 Donald Gardner,3 Daniel Long,3 and B. Joseph Hinnebusch2

Laboratory of Zoonotic Pathogens,2 Veterinary Branch, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana,3 Institut National de la Santé et de la Recherche Médicale, U801, Institut Pasteur de Lille, Université de Lille 2, Lille, France1

Received 30 July 2008/ Returned for modification 4 September 2008/ Accepted 15 December 2008

Plague is a zoonosis transmitted by fleas and caused by the gram-negative bacterium Yersinia pestis. During infection, the plasmidic caf1M1A1 operon that encodes the Y. pestis F1 protein capsule is highly expressed, and anti-F1 antibodies are protective. Surprisingly, the capsule is not required for virulence after injection of cultured bacteria, even though it is an antiphagocytic factor and capsule-deficient Y. pestis strains are rarely isolated. We found that a caf-negative Y. pestis mutant was not impaired in either flea colonization or virulence in mice after intradermal inoculation of cultured bacteria. In contrast, absence of the caf operon decreased bubonic plague incidence after a flea bite. Successful development of plague in mice infected by flea bite with the caf-negative mutant required a higher number of infective bites per challenge. In addition, the mutant displayed a highly autoaggregative phenotype in infected liver and spleen. The results suggest that acquisition of the caf locus via horizontal transfer by an ancestral Y. pestis strain increased transmissibility and the potential for epidemic spread. In addition, our data support a model in which atypical caf-negative strains could emerge during climatic conditions that favor a high flea burden. Human infection with such strains would not be diagnosed by the standard clinical tests that detect F1 antibody or antigen, suggesting that more comprehensive surveillance for atypical Y. pestis strains in plague foci may be necessary. The results also highlight the importance of studying Y. pestis pathogenesis in the natural context of arthropod-borne transmission.

* Corresponding author. Mailing address: INSERM U801, Institut Pasteur de Lille, 1 rue du Professeur Calmette, 59021 Lille Cedex, France. Phone: (33) 320-87-11-93. Fax: (33) 320-87-11-83. E-mail: florent.sebbane{at}ibl.fr

{triangledown} Published ahead of print on 22 December 2008.

Editor: J. B. Bliska

Infection and Immunity, March 2009, p. 1222-1229, Vol. 77, No. 3
0019-9567/09/$08.00+0     doi:10.1128/IAI.00950-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Cornelius, C. A., Quenee, L. E., Elli, D., Ciletti, N. A., Schneewind, O. (2009). Yersinia pestis IS1541 Transposition Provides for Escape from Plague Immunity. Infect. Immun. 77: 1807-1816 [Abstract] [Full Text]  


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