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. 2011 Mar 5;2(3):173–179. doi: 10.1007/s13238-011-1024-3

Formation and regulation of Yersinia biofilms

Dongsheng Zhou 1,✉, Ruifu Yang 1,✉
PMCID: PMC4875308  PMID: 21380640

Abstract

Flea-borne transmission is a recent evolutionary adaptation that distinguishes the deadly Yersinia pestis from its progenitor Y. Pseudotuberculosis, a mild pathogen transmitted via the food-borne route. Y. Pestis synthesizes biofilms in the flea gut, which is important for fleaborne transmission. Yersinia biofilms are bacterial colonies surrounded by extracellular matrix primarily containing a homopolymer of N-acetyl-D-glucosamine that are synthesized by a set of specific enzymes. Yersinia biofilm production is tightly regulated at both transcriptional and post-transcriptional levels. All the known structural genes responsible for biofilm production are harbored in both Y. Pseudotuberculosis and Y. Pestis, but Y. Pestis has evolved changes in the regulation of biofilm development, thereby acquiring efficient arthropod-borne transmission.

Keywords: Yersinia pestis, Y. Pseudotuberculosis, biofilm, flea-borne transmission

Contributor Information

Dongsheng Zhou, Email: dongshengzhou1977@gmail.com.

Ruifu Yang, Email: ruifuyang@gmail.com.

References

  1. Abu Khweek A., Fetherston J.D., Perry R.D. Analysis of HmsH and its role in plague biofilm formation. Microbiology. 2010;156:1424–1438. doi: 10.1099/mic.0.036640-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Achtman M., Zurth K., Morelli G., Torrea G., Guiyoule A., Carniel E. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A. 1999;96:14043–14048. doi: 10.1073/pnas.96.24.14043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bobrov A.G., Kirillina O., Forman S., Mack D., Perry R.D. Insights into Yersinia pestis biofilm development: topology and co-interaction of Hms inner membrane proteins involved in exopolysaccharide production. Environ Microbiol. 2008;10:1419–1432. doi: 10.1111/j.1462-2920.2007.01554.x. [DOI] [PubMed] [Google Scholar]
  4. Bobrov A.G., Kirillina O., Perry R.D. The phosphodiesterase activity of the HmsP EAL domain is required for negative regulation of biofilm formation in Yersinia pestis. FEMS Microbiol Lett. 2005;247:123–130. doi: 10.1016/j.femsle.2005.04.036. [DOI] [PubMed] [Google Scholar]
  5. Bobrov A.G., Kirillina O., Ryjenkov D.A., Waters C.M., Price P.A., Fetherston J.D., Mack D., Goldman W.E., Gomelsky M., Perry R.D. Systematic analysis of cyclic di-GMP signalling enzymes and their role in biofilm formation and virulence in Yersinia pestis. Mol Microbiol. 2011;79:533–551. doi: 10.1111/j.1365-2958.2010.07470.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chain P.S., Carniel E., Larimer F.W., Lamerdin J., Stoutland P.O., Regala W.M., Georgescu A.M., Vergez L.M., Land M.L., Motin V.L., et al. Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A. 2004;101:13826–13831. doi: 10.1073/pnas.0404012101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Darby C. Uniquely insidious: Yersinia pestis biofilms. Trends Microbiol. 2008;16:158–164. doi: 10.1016/j.tim.2008.01.005. [DOI] [PubMed] [Google Scholar]
  8. Darby C., Ananth S.L., Tan L., Hinnebusch B.J. Identification of gmhA, a Yersinia pestis gene required for flea blockage, by using a Caenorhabditis elegans biofilm system. Infect Immun. 2005;73:7236–7242. doi: 10.1128/IAI.73.11.7236-7242.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Darby C., Hsu J.W., Ghori N., Falkow S. Caenorhabditis elegans: plague bacteria biofilm blocks food intake. Nature. 2002;417:243–244. doi: 10.1038/417243a. [DOI] [PubMed] [Google Scholar]
  10. Davies D. Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov. 2003;2:114–122. doi: 10.1038/nrd1008. [DOI] [PubMed] [Google Scholar]
  11. Donlan R.M., Costerton J.W. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002;15:167–193. doi: 10.1128/CMR.15.2.167-193.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Drace K., Darby C. The hmsHFRS operon of Xenorhabdus nematophila is required for biofilm attachment to Caenorhabditis elegans. Appl Environ Microbiol. 2008;74:4509–4515. doi: 10.1128/AEM.00336-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Eisen R.J., Bearden S.W., Wilder A.P., Montenieri J.A., Antolin M. F., Gage K.L. Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics. Proc Natl Acad Sci U S A. 2006;103:15380–15385. doi: 10.1073/pnas.0606831103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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., Vetter S.M., et al. 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. 2008;78:949–956. [PubMed] [Google Scholar]
  15. Eisen R.J., Gage K.L. Adaptive strategies of Yersinia pestis to persist during inter-epizootic and epizootic periods. Vet Res. 2009;40:1. doi: 10.1051/vetres:2008039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Erickson D.L., Jarrett C.O., Callison J.A., Fischer E.R., Hinnebusch B.J. Loss of a biofilm-inhibiting glycosyl hydrolase during the emergence of Yersinia pestis. J Bacteriol. 2008;190:8163–8170. doi: 10.1128/JB.01181-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Erickson D.L., Jarrett C.O., Wren B.W., Hinnebusch B.J. Serotype differences and lack of biofilm formation characterize Yersinia pseudotuberculosis infection of the Xenopsylla cheopis flea vector of Yersinia pestis. J Bacteriol. 2006;188:1113–1119. doi: 10.1128/JB.188.3.1113-1119.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Erickson D.L., Jarrett C.O., Wren B.W., Hinnebusch B.J. Serotype differences and lack of biofilm formation characterize Yersinia pseudotuberculosis infection of the Xenopsylla cheopis flea vector of Yersinia pestis. J Bacteriol. 2006;188:1113–1119. doi: 10.1128/JB.188.3.1113-1119.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Flemming H.C., Wingender J. The biofilm matrix. Nat Rev Microbiol. 2010;8:623–633. doi: 10.1038/nrmicro2415. [DOI] [PubMed] [Google Scholar]
  20. Forman S., Bobrov A.G., Kirillina O., Craig S.K., Abney J., Fetherston J.D., Perry R.D. Identification of critical amino acid residues in the plague biofilm Hms proteins. Microbiology. 2006;152:3399–3410. doi: 10.1099/mic.0.29224-0. [DOI] [PubMed] [Google Scholar]
  21. Fux C.A., Costerton J.W., Stewart P.S., Stoodley P. Survival strategies of infectious biofilms. Trends Microbiol. 2005;13:34–40. doi: 10.1016/j.tim.2004.11.010. [DOI] [PubMed] [Google Scholar]
  22. Grabenstein J.P., Fukuto H.S., Palmer L.E., Bliska J.B. Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect Immun. 2006;74:3727–3741. doi: 10.1128/IAI.00255-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hall-Stoodley L., Costerton J.W., Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol. 2004;2:95–108. doi: 10.1038/nrmicro821. [DOI] [PubMed] [Google Scholar]
  24. Hengge R. Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol. 2009;7:263–273. doi: 10.1038/nrmicro2109. [DOI] [PubMed] [Google Scholar]
  25. Hinnebusch B.J., Erickson D.L. Yersinia pestis biofilm in the flea vector and its role in the transmission of plague. Curr Top Microbiol Immunol. 2008;322:229–248. doi: 10.1007/978-3-540-75418-3_11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hinnebusch B.J., Rudolph A.E., Cherepanov P., Dixon J.E., Schwan T.G., Forsberg A. Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science. 2002;296:733–735. doi: 10.1126/science.1069972. [DOI] [PubMed] [Google Scholar]
  27. Joshua G.W., Karlyshev A.V., Smith M.P., Isherwood K.E., Titball R.W., Wren B.W. A Caenorhabditis elegans model of Yersinia infection: biofilm formation on a biotic surface. Microbiology. 2003;149:3221–3229. doi: 10.1099/mic.0.26475-0. [DOI] [PubMed] [Google Scholar]
  28. Kirillina O., Fetherston J.D., Bobrov A.G., Abney J., Perry R. D. HmsP, a putative phosphodiesterase, and HmsT, a putative diguanylate cyclase, control Hms-dependent biofilm formation in Yersinia pestis. Mol Microbiol. 2004;54:75–88. doi: 10.1111/j.1365-2958.2004.04253.x. [DOI] [PubMed] [Google Scholar]
  29. Li Y.L., Gao H., Qin L., Li B., Han Y.P., Guo Z.B., Song Y.J., Zhai J.H., Du Z.M., Wang X.Y., et al. Identification and characterization of PhoP regulon members in Yersinia pestis biovar Microtus. BMC Genomics. 2008;9:143. doi: 10.1186/1471-2164-9-143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lorange E.A., Race B.L., Sebbane F., Joseph Hinnebusch B. Poor vector competence of fleas and the evolution of hypervirulence in Yersinia pestis. J Infect Dis. 2005;191:1907–1912. doi: 10.1086/429931. [DOI] [PubMed] [Google Scholar]
  31. Lukaszewski R.A., Kenny D.J., Taylor R., Rees D.G., Hartley M. G., Oyston P.C. Pathogenesis of Yersinia pestis infection in BALB/c mice: effects on host macrophages and neutrophils. Infect Immun. 2005;73:7142–7150. doi: 10.1128/IAI.73.11.7142-7150.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Majdalani N., Gottesman S. The Rcs phosphorelay: a complex signal transduction system. Annu Rev Microbiol. 2005;59:379–405. doi: 10.1146/annurev.micro.59.050405.101230. [DOI] [PubMed] [Google Scholar]
  33. Matthysse A.G., Stretton S., Dandie C., McClure N.C., Goodman A.E. Construction of GFP vectors for use in gram-negative bacteria other than Escherichia coli. FEMS Microbiol Lett. 1996;145:87–94. doi: 10.1111/j.1574-6968.1996.tb08561.x. [DOI] [PubMed] [Google Scholar]
  34. Parkhill J., Wren B.W., Thomson N.R., Titball R.W., Holden M.T., Prentice M.B., Sebaihia M., James K.D., Churcher C., Mungall K.L., et al. Genome sequence of Yersinia pestis, the causative agent of plague. Nature. 2001;413:523–527. doi: 10.1038/35097083. [DOI] [PubMed] [Google Scholar]
  35. Patel C.N., Wortham B.W., Lines J.L., Fetherston J.D., Perry R. D., Oliveira M.A. Polyamines are essential for the formation of plague biofilm. J Bacteriol. 2006;188:2355–2363. doi: 10.1128/JB.188.7.2355-2363.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Perry R.D., Fetherston J.D. Yersinia pestis—etiologic agent of plague. Clin Microbiol Rev. 1997;10:35–66. doi: 10.1128/cmr.10.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schirmer T., Jenal U. Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol. 2009;7:724–735. doi: 10.1038/nrmicro2203. [DOI] [PubMed] [Google Scholar]
  38. Simm R., Fetherston J.D., Kader A., Römling U., Perry R.D. Phenotypic convergence mediated by GGDEF-domaincontaining proteins. J Bacteriol. 2005;187:6816–6823. doi: 10.1128/JB.187.19.6816-6823.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sun Y.C., Hinnebusch B.J., Darby C. Experimental evidence for negative selection in the evolution of a Yersinia pestis pseudogene. Proc Natl Acad Sci U S A. 2008;105:8097–8101. doi: 10.1073/pnas.0803525105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sun Y.C., Koumoutsi A., Darby C. The response regulator PhoP negatively regulates Yersinia pseudotuberculosis and Yersinia pestis biofilms. FEMS Microbiol Lett. 2009;290:85–90. doi: 10.1111/j.1574-6968.2008.01409.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Tan L., Darby C. A movable surface: formation of Yersinia sp. biofilms on motile Caenorhabditis elegans. J Bacteriol. 2004;186:5087–5092. doi: 10.1128/JB.186.15.5087-5092.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Tan L., Darby C. Yersinia pestis is viable with endotoxin composed of only lipid A. J Bacteriol. 2005;187:6599–6600. doi: 10.1128/JB.187.18.6599-6600.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Tan L., Darby C. Yersinia pestis YrbH is a multifunctional protein required for both 3-deoxy-D-manno-oct-2-ulosonic acid biosynthesis and biofilm formation. Mol Microbiol. 2006;61:861–870. doi: 10.1111/j.1365-2958.2006.05265.x. [DOI] [PubMed] [Google Scholar]
  44. 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. Biofilm formation is not required for early-phase transmission of Yersinia pestis. Microbiology. 2010;156:2216–2225. doi: 10.1099/mic.0.037952-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wortham B.W., Oliveira M.A., Fetherston J.D., Perry R.D. Polyamines are required for the expression of key Hms proteins important for Yersinia pestis biofilm formation. Environ Microbiol. 2010;12:2034–2047. doi: 10.1111/j.1462-2920.2010.02219.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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