Yersinia-flea interactions and the evolution of the arthropod-borne transmission route of plague

Current Opinion in Microbiology

Volumn 15, Issue 3, 2012, Pages 239-246

  Chouikha, Iman ^a   Hinnebusch, B Joseph ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTHROPOD; BACTERIAL COLONIZATION; BIOFILM; DISEASE TRANSMISSION; ECOLOGY; FLEA; FOOD POISONING; GENETIC ASSOCIATION; NONHUMAN; ORGANISMAL INTERACTION; PLAGUE; REVIEW; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS; YERSINIA PSEUDOTUBERCULOSIS INFECTION;

ANIMALS; BIOLOGICAL EVOLUTION; HOST-PATHOGEN INTERACTIONS; INSECT VECTORS; PLAGUE; SIPHONAPTERA; YERSINIA PESTIS;

ARTHROPODA; HEXAPODA; NEGIBACTERIA; SIPHONAPTERA (FLEAS); YERSINIA; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

EID: 84864035046     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2012.02.003     Document Type: Review

References (46)

1. 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.
2. Achtman M., Morelli G., Zhu P., Wirth T., Diehl I., Kusecek B., Vogler A.J., Wagner D.M., Allender C.J., Easterday W.R., et al. Microevolution and history of the plague bacillus, Yersinia pestis. Proc Natl Acad Sci U S A 2004, 101:17837-17842.
3. Beard C.B., Butler J.F., Hall D.W. Prevalence and biology of endosymbionts of fleas (Siphonaptera: Pulicidae) from dogs and cats in Alachua County, Florida. J Med Entomol 1990, 27:1050-1061.
4. Pornwiroon W., Kearney M.T., Husseneder C., Foil L.D., Macaluso K.R. Comparative microbiota of Rickettsia felis-uninfected and -infected colonized cat fleas, Ctenocephalides felis. ISME J 2007, 1:394-402.
5. Jones R.T., McCormick K.F., Martin A.P. Bacterial communitites of Bartonella-positive fleas: diversity and community assembly patterns. Appl Environ Microbiol 2008, 74:1667-1670.
6. Erickson D.L., Anderson N.E., Cromar L.M., Jolley A. Bacterial communities associated with flea vectors of plague. J Med Entomol 2009, 46:1532-1536.
7. Bengoechea J.A., Lindner B., Seydel U., Diaz R., Moriyon I. Yersinia pseudotuberculosis and Yersinia pestis are more resistant to bactericidal cationic peptides than Yersinia enterocolitica. Microbiology 1998, 144(Pt 6):1509-1515.
8. Rebeil R., Ernst R.K., Gowen B.B., Miller S.I., Hinnebusch B.J. Variation in lipid A structure in the pathogenic yersiniae. Mol Microbiol 2004, 52:1363-1373.
9. Anisimov A.P., Dentovskaya S.V., Titareva G.M., Bakhteeva I.V., Shaikhutdinova R.Z., Balakhonov S.V., Lindner B., Kocharova N.A., Senchenkova S.N., Holst O., et al. Intraspecies and temperature-dependent variations in susceptibility of Yersinia pestis to the bactericidal action of serum and to polymyxin B. Infect Immun 2005, 73:7324-7331.
10. Engelthaler D.M., Hinnebusch B.J., Rittner C.M., Gage K.L. Quantitative competitive PCR as a technique for exploring flea-Yersina pestis dynamics. Am J Trop Med Hyg 2000, 62:552-560.
11. Lorange E.A., Race B.L., Sebbane F., Hinnebusch B.J. Poor vector competence of fleas and the evolution of hypervirulence in Yersinia pestis. J Infect Dis 2005, 191:1907-1912.
12. Hinnebusch B.J., Perry R.D., Schwan T.G. Role of the Yersinia pestis hemin storage (hms) locus in the transmission of plague by fleas. Science 1996, 273:367-370.
13. Hinnebusch B.J., Rudolph A.E., Cherepanov P., Dixon J.E., Schwan T.G., Forsberg Å. Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science 2002, 296:733-735.
14. Darby C., Hsu J.W., Ghori N., Falkow S. Caenorhabditis elegans: plague bacteria biofilm blocks food intake. Nature 2002, 417:243-244.
15. Jarrett C.O., Deak E., Isherwood K.E., Oyston P.C., Fischer E.R., Whitney A.R., Kobayashi S.D., DeLeo F.R., Hinnebusch B.J. Transmission of Yersinia pestis from an infectious biofilm in the flea vector. J Infect Dis 2004, 190:783-792.
16. Bacot A.W. Further notes on the mechanism of the transmission of plague by fleas. J Hygiene Plague 1915, 14(Suppl. 4):774-776.
17. 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.
18. 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.
19. 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.
20. Martin B., Collar J.L., Tjallingii W.F., Fereres A. Intracellular ingestion and salivation by aphids may cause the acquisition and inoculation of non-persistently transmitted plant viruses. J Gen Virol 1997, 78:2701-2705.
21. Hinnebusch BJ: Biofilm-dependent and biofilm-independent mechanisms of transmission of Yersinia pestis by fleas. Adv Exp Med Biol 2012. In press.
22. Beloin C., Da Re S., Ghigo J.-M. Colonization of abiotic surfaces. EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology 2005, vol. 2005. ASM Press, Washington, DC.
23. Perry R.D., Fetherston J.D. Yersinia pestis-etiologic agent of plague. Clin Microbiol Rev 1997, 10:35-66.
24. Vadyvaloo V., Jarrett C., Sturdevant D.E., Sebbane F., Hinnebusch B.J. Transit through the flea vector induces a pretransmission innate immunity resistance phenotype in Yersinia pestis. PLoS Pathog 2010, 6:e10000783.
25. Hinnebusch B.J., Sebbane F., Vadyvaloo V. Transcriptional profiling of the Yersinia pestis life cycle. Yersinia: Systems Biology and Control 2012, Horizon Scientific Press. E. Carniel, B.J. Hinnebusch (Eds.).
26. Beloin C., Ghigo J.M. Finding gene-expression patterns in bacterial biofilms. Trends Microbiol 2005, 13:16-19.
27. Hennge R. Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 2009, 7:263-273.
28. 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.
29. Sun Y.-C., Koumoutsi A., Jarrett C., Lawrence K., Gherardini F.C., Darby C., Hinnebusch B.J. Differential control of Yersinia pestis biofilm formation in vitro and in the flea vector by two c-di-GMP diguanylate cyclases. PLoS One 2011, 6:e19267.
30. Perry R.D., Bobrov A.G., Kirillina O., Jones H.A., Pedersen L., Abney J., Fetherston J.D. Temperature regulation of the hemin storage (Hms+) phenotype of Yersinia pestis is posttranscriptional. J Bacteriol 2004, 186:1638-1647.
31. 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.
32. Kawahara K., Tsukano H., Watanabe H., Lindner B., Matsuura M. Modification of the structure and activity of lipid A in Yersinia pestis lipopolysaccharide by growth temperature. Infect Immun 2002, 70:4092-4098.
33. Rebeil R., Ernst R.K., Jarrett C.O., Adams K.N., Miller S.I., Hinnebusch B.J. Characterization of late acyltransferase genes of Yersinia pestis and their role in temperature-dependent lipid A variation. J Bacteriol 2006, 188:1381-1388.
34. Erickson D.L., Waterfield N.R., Vadyvaloo V., Long D., Fischer E.R., Ffrench-Constant R.H., Hinnebusch B.J. Acute oral toxicity of Yersinia pseudotuberculosis to fleas: implications for the evolution of vector-borne transmission of plague. Cell Microbiol 2007, 9:2658-2666.
35. Fuchs T.M., Bresolin G., Marcinowski L., Schachtner J., Scherer S. Insecticidal genes of Yersinia spp.: taxonomical distribution, contribution to toxicity towards Manduca sexta and Galleria mellonella, and evolution. BMC Microbiol 2008, 8:214.
36. Pinheiro V.B., Ellar D.J. Expression and insecticidal activity of Yersinia pseudotuberculosis and Photorhabdus luminescens toxin complex proteins. Cell Microbiol 2007, 9:2372-2380.
37. Hurst M.R., Jones S.A., Binglin T., Harper L.A., Jackson T.A., Glare T.R. The main virulence determinant of Yersinia entomophaga MH96 is a broad-host-range toxin complex active against insects. J Bacteriol 2011, 193:1966-1980.
38. 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.
39. Hinnebusch B.J., Fischer E.R., Schwan T.G. 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 1998, 178:1406-1415.
40. Sebbane F., Jarrett C.O., Gardner D., Long D., Hinnebusch B.J. Role of the Yersinia pestis plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea-borne plague. Proc Natl Acad Sci U S A 2006, 103:5526-5530.
41. Lähteenmäki K., Edelman S., Korhonen T.K. Bacterial metastasis: the host plasminogen system in bacterial invasion. Trends Microbiol 2005, 13:79-85.
42. Parkhill J., Wren B.W., Thomson N.R., Titball R.W., Holden M.T.G., Prentice M.B., Sebhaihia 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.
43. Chain P.S.G., 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.
44. 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.
45. Qi M., Sun F.-J., Caetano-Anollés G., Zhao Y. Comparative genomic and phylogenetic analyses reveal the evolution of the core two-component signal transduction systems in Enterobacteria. J Mol Evol 2010, 70:167-180.
46. Williams K.P., Gillespie J.J., Sobral B.W.S., Nordberg E.K., Snyder E.E., Shallom J.M., Dickerman A.W. Phylogeny of gammaproteobacteria. J Bacteriol 2010, 192:2305-2314.