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Differential Gene Regulation in Yersinia pestis versus Yersinia pseudotuberculosis: Effects of Hypoxia and Potential Role of a Plasmid Regulator

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The Genus Yersinia

Part of the book series: Advances In Experimental Medicine And Biology ((AEMB,volume 603))

The molecular basis of the biological differences between Yersinia pestis and Yersinia pseudotuberculosis remains largely unknown, and relatively little is known about environmental regulation of gene expression in these bacteria. We used a proteomic approach to explore the regulatory response of each bacterium to carbon dioxide-supplemented hypoxic conditions. Both organisms responded similarly and the magnitude of their responses was similar to what was observed in low iron conditions. We also identified proteins that were expressed at different levels in Y. pestis and Y. pseudotuberculosis, and found that SodB is expressed more strongly at both the protein and RNA levels in Y. pseudotuberculosis than in Y. pestis. Enzyme activity did not directly correlate with levels of protein expression, and we propose that an amino acid change difference between these orthologous proteins has the potential to affect catalytic activity. In addition, the upstream regulatory regions of several chromosomal genes were found to exhibit specific binding with a putative transcription factor, CDS4, from the Y. pestis-specific pPCP1 plasmid. The potential role of this protein in modulating Y. pestis- specific gene regulation warrants further investigation.

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References

  • Achtman, M., Morelli, G., Zhu, P., Wirth, T., Diehl, I., Kusecek, B., Vogler, A.J., Wagner, D.M., Allender, C.J., Easterday, W.R., Chenal-Francisque, V., Worsham, P., Thomson, N.R., Parkhill, J., Lindler, L.E., Carniel, E. and Keim, P. (2004). Microevolution and his-tory of the plague bacillus, Yersinia pestis. PNAS. U S A 101, 17837-17842.

    Article  CAS  Google Scholar 

  • Ammendola, S., Ajello, M., Pasquali, P., Kroll, J.S., Langford, P.R., Rotilio, G., Valenti, P. and Battistoni, A. (2005). Differential contribution of sodC1 and sodC2 to intracellular survival and pathogenicity of Salmonella enterica serovar Choleraesuis. Microbes Infect. 7, 698-707.

    Article  CAS  PubMed  Google Scholar 

  • Bai, G., McCue, L.A. and McDonough, K.A. (2005). Characterization of Mycobacterium tuberculosis Rv3676 (CRPMt), a cyclic AMP receptor protein-like DNA binding protein. J. Bacteriol. 187, 7795-7804.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bakshi, C.S., Malik, M., Regan, K., Melendez, J.A., Metzger, D.W., Pavlov, V.M. and Sellati, T.J. (2006). Superoxide dismutase B gene (sodB)-deficient mutants of Francisella tularensis demonstrate hypersensitivity to oxidative stress and attenuated virulence. J. Bacteriol. 188, 6443-6448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barnes, A.M. (1982). Surveillance and control of bubonic plague in the United States. Symp. Zool. Soc. London 50, 237-270.

    Google Scholar 

  • Beauchamp, C. and Fridovich, I. (1971). Superoxide dismutase improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 44, 276-287.

    Article  CAS  PubMed  Google Scholar 

  • Bercovier, H., Mollaret, H.H., Alonso, J.M., Brault, J., Fanning, G.R., Steigerwalt, A.G. and Brenner, D.J. (1980). Intra- and interspecies relatedness of Yersinia pestis by DNA hybridization and its relationship to Yersinia pseudotuberculosis. Curr. Microbiol. 4, 225-229.

    Article  CAS  Google Scholar 

  • Bond, C.J., Huang, J., Hajduk, R., Flick, K.E., Heath, P.J. and Stoddard, B.L. (2000). Cloning, sequence and crystallographic structure of recombinant iron superoxide dismutase from Pseudomonas ovalis. Acta Crystallogr. D Biol. Crystallogr. 56, 1359-1366.

    Article  CAS  Google Scholar 

  • Brubaker, R.R., Beesley, E.D. and Surgalla, M.J. (1965). Pasteurella pestis: role of pesticin I and iron in experimental plague. Science 149, 422-424.

    Article  CAS  PubMed  Google Scholar 

  • Cash, P. (2003). Proteomics of bacterial pathogens. Adv. Biochem. Eng. Biotechnol. 83, 93-115.

    CAS  PubMed  Google Scholar 

  • 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., Brubaker, R.R., Fowler, J., Hinnebusch, J., Marceau, M., Medigue, C., Simonet, M., Chenal-Francisque, V., Souza, B., Dacheux, D., Elliott, J.M., Derbise, A., Hauser, L.J. and Garcia, E. (2004). Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudo-tuberculosis. PNAS 101, 13826-13831.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chain, P.S.G., Hu, P., Malfatti, S.A., Radnedge, L., Larimer, F., Vergez, L.M., Worsham, P., “Chu, M.C. and Andersen, G.L. (2006). Complete genome sequence of Yersinia pestis strains Antiqua and Nepal516: evidence of gene reduction in an emerging pathogen. J. Bacteriol. 188, 4453-4463.

    Article  PubMed  PubMed Central  Google Scholar 

  • Deng, W., Burland, V., Plunkett, G., III, Boutin, A., Mayhew, G.F., Liss, P., Perna, N.T., Rose, D.J., Mau, B., Zhou, S., Schwartz, D.C., Fetherston, J.D., Lindler, L.E., Brubaker, R.R., Plano, G.V., Straley, S.C., McDonough, K.A., Nilles, M.L., Matson, J.S., Blattner, F.R. and Perry, R.D. (2002). Genome Sequence of Yersinia pestis KIM. J. Bacteriol. 184, 4601-4611.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erickson, D.L., Jarrett, C.O., Wren, B.W. and Hinnebusch, B.J. (2006). Serotype differences and lack of biofilm formation characterize Yersinia pseudotuberculosis infection of the Xenopsylla cheopis flea vector of Yersinia pestis. J. Bacteriol. 188, 1113-1119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eswar, N., John, B., Mirkovic, N., Fiser, A., Ilyin, V.A., Pieper, U., Stuart, A.C., Marti-Renom, M.A., Madhusudhan, M.S., Yerkovich, B. and Sali, A. (2003). Tools for com-parative protein structure modeling and analysis. Nucleic Acids Res. 31, 3375-3380.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferber, D.M. and Brubaker, R.R. (1981) Plasmids in Yersinia pestis. Infect. Immun. 31, 839-841.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ferber, D.M., Fowler, J.M. and Brubaker, R.R. (1981). Mutations to tolerance and resistance to pesticin and colicins in Escherichia coli. J. Bacteriol. 146, 506-511.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Florczyk, M.A., McCue, L.A., Purkayastha, A., Currenti, E., Wolin, M.J. and McDonough, K.A. (2003). A family of acr-coregulated Mycobacterium tuberculosis genes shares a common DNA motif and requires Rv3133c (dosR or devR) for expression. Infect. Immun. 71, 5332-5343.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Florczyk, M.A., McCue, L.A., Stack, R.F., Hauer, C.R. and McDonough, K.A. (2001). Identi-fication and characterization of mycobacterial proteins differentially expressed under standing and shaking culture conditions, including Rv2623 from a novel class of putative ATP-binding proteins. Infect. Immun. 69, 5777-5785.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gazdik, M. A. and McDonough, K.A. (2005). Identification of cyclic AMP-regulated genes in Mycobacterium tuberculosis complex bacteria under low-oxygen conditions. J. Bacteriol. 187, 2681-2692.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gee, J.M., Valderas, M.W., Kovach, M.E., Grippe, V.K., Robertson, G.T., Ng, W.L., Richardson, J.M., Winkler, M.E. and Roop, R.M. 2nd. (2005). The Brucella abortus Cu, Zn superoxide dismutase is required for optimal resistance to oxidative killing by murine macrophages and wild-type virulence in experimentally infected mice. Infect. Immun. 73, 2873-2880.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gronberg, A. and Kihlstrom, E. (1989). Structural variations and growth potential of Yersinia enterocolitica under different culture conditions. Apmis 97, 227-235.

    Article  CAS  PubMed  Google Scholar 

  • Guyton, A.C., Ed. (1991). Textbook of medical physiology, 8th ed. Philadelphia, PA, W.B. Saunders Company.

    Google Scholar 

  • Han, Y.W. and Miller, V.L. (1997). Reevaluation of the virulence phenotype of the inv yadA double mutants of Yersinia pseudotuberculosis. Infect. Immun. 65, 327-330.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hare, J. M. and McDonough, K.A. (1999). High-frequency RecA-dependent and -independent mechanisms of congo red binding mutations in Yersinia pestis. J. Bacteriol. 181, 4896-4904.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hinchliffe, S.J., Isherwood, K.E., Stabler, R.A., Prentice, M.B., Rakin, A., Nichols, R.A., Oyston, P.C.F., Hinds, J., Titball, R.W. and Wren, B.W. (2003) Application of DNA microarrays to study the evolutionary genomics of Yersinia pestis and Yersinia pseudotu-berculosis. Genome Res. 13, 2018-2029.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hinnebusch, B.J. (2003). Transmission factors: Yersinia pestis genes required to infect the flea vector of plague. Adv. Exp. Med. Biol. 529, 55-62.

    Article  PubMed  Google Scholar 

  • Hinnebusch, B.J., Perry, R.D. and Schwan, T.G. (1996). Role of the Yersinia pestis hemin storage (hms) locus in the transmission of plague by fleas. Science 273, 367-370.

    Article  CAS  PubMed  Google Scholar 

  • Hinnebusch, B.J., Rudolph, A.E., Cherepanov, P., Dixon, J.E., Schwan, T.G. and Forsberg, A. (2002). Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science 296, 733-735.

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim, A., Goebel, B.M., Liesack, W., Griffiths, M. and Stackebrandt, E. (1993). The phy-logeny of the genus Yersinia based on 16S rDNA sequences. FEMS Microb. Letters 114, 173-178.

    CAS  Google Scholar 

  • Jungblut, P.R., Muller, E.C., Mattow, J. and Kaufmann, S.H. (2001). Proteomics reveals open reading frames in Mycobacterium tuberculosis H37Rv not predicted by genomics. Infect. Immun. 69, 5905-5907.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jydegaard-Axelsen, A.M., Hoiby, P.E., Holmstrom, K., Russell, N. and Knochel, S. (2004). CO 2 - and anaerobiosis-induced changes in physiology and gene expression of different Listeria monocytogenes strains. Appl. Environ. Microbiol. 70, 4111-4117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lathem, W.W., Crosby, S.D., Miller, V.L. and Goldman, W.E. (2005). Progression of primary pneumonic plague: A mouse model of infection, pathology, and bacterial transcriptional activity. PNAS 102, 17786-17791.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lide, D.R., Ed. (1997). CRC handbook of chemistry and physics. Cleveland Ohio, CRC Press.

    Google Scholar 

  • Masse, E. and Gottesman, S. (2002). A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. PNAS U S A 99, 4620-4625.

    Article  CAS  Google Scholar 

  • McDonough, K. A. and Falkow, S. (1989). A Yersinia pestis-specific DNA fragment encodes temperature-dependent coagulase and fibrinolysin-associated phenotypes. Mol. Microbiol. 3, 767-775.

    Article  CAS  PubMed  Google Scholar 

  • McDonough, K.A., Florczyk, M.A. and Kress, Y. (2000). Intracellular passage within macro-phages affects the trafficking of virulent tubercle bacilli upon reinfection of other macro-phages in a serum-dependent manner. Tuber Lung Dis. 80, 259-271.

    Article  CAS  PubMed  Google Scholar 

  • Mollaret, H. H. (1965). Sur la nomenclature et la taxonomic du bacille de malassez et vignal. Int. Bull. Bacteriol. Nomencl. Taxon. 15, 97-106.

    Google Scholar 

  • Motin, V.L., Georgescu, A.M., Fitch, J.P., Gu, P.P., Nelson, D.O., Mabery, S.L., Garnham, J.B., Sokhansanj, B.A., Ott, L.L., Coleman, M.A., Elliott, J.M., Kegelmeyer, L.M., Wyrobek, A.J., Slezak, T.R., Brubaker, R.R. and Garcia, E. (2004) Temporal global chan-ges in gene expression during temperature transition in Yersinia pestis. J. Bacteriol. 186, 6298-6305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Najdenski, H.M., Golkocheva, E.N., Vesselinova, A.M. and Russmann, H. (2004). Compari-son of the course of infection of virulent Yersinia enterocolitica serotype O:8 with an isogenic sodA mutant in the peroral rabbit model. Int. J. Med. Microbiol. 294, 383-393.

    Article  PubMed  Google Scholar 

  • Narasipura, S.D., Ault, J.G., Behr, M.J., Chaturvedi, V. and Chaturvedi, S. (2003). Characteri-zation of Cu, Zn superoxide dismutase (SOD1) gene knock-out mutant of Cryptococcus neoformans var. gattii: role in biology and virulence. Mol. Microbiol. 47, 1681-1694.

    Article  CAS  PubMed  Google Scholar 

  • 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., Baker, S., Basham, D., Bentley, S.D., Brooks, K., Cerdeno-Tarraga, A.M., Chillingworth, T., Cronin, A., Davies, R.M., Davis, P., Dougan, G., Feltwell, T., Hamlin, N., Holroyd, S., Jagels, K., Karlyshev, A.V., Leather, S., Moule, S., Oyston, P.C., Quail, M., Rutherford, K., Simmonds, M., Skelton, J., Stevens, K., Whitehead, S. and Barrell, B.G. (2001). Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413, 523-527.

    Article  CAS  PubMed  Google Scholar 

  • Perry, R.D. (1993) Acquisition and storage of inorganic iron and hemin by the yersiniae. Trends Microbiol. 1, 142-147.

    Article  CAS  PubMed  Google Scholar 

  • Perry, R.D. and Fetherston, J.D. (1997). Yersinia pestis - etiologic agent of plague. Clin. Microbiol. Rev. 10, 35-66.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Poland, J.D. and Barnes, A.M. (1979). Plague. in J.F. Steele (ed.), CRC Handbook Series in Zoonoses, Vol. 1, Section A. Bacterial, rickettsial and mycotic diseases-1979. CRC Press, Inc., Boca Raton, Fla., pp. 515-516.

    Google Scholar 

  • Portnoy, D.A. and Falkow, S. (1981). Virulence-associated plasmids from Yersinia enterocoli-tica and Yersinia pestis. J. Bacteriol. 148, 877-883.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Protsenko, O.A., Anisimov, P.I., Mosharov, O.T., Konnov, N.P., Popov, Y.A. and Kokushkin, A.M. (1983) Detection and characterization of Yersinia pestis plasmids determining pes-ticin I, fraction I antigen, and “mouse” toxin synthesis. Soviet Genet. 19, 838-846.

    Google Scholar 

  • Purkayastha, A., McCue, L.A. and McDonough, K.A., et al. (2002). Identification of a Myco-bacterium tuberculosis putative classical nitroreductase gene whose expression is coregu-lated with that of the acr aene within macrophages, in standing versus shaking cultures, and under low oxygen conditions. Infect. Immun. 70, 1518-1529.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quan, T. J., Barnes, A.M. and Polland, J.D. (1981). Yersinioses, p. 723-745. In A. Balows and W. J. Hausler, (ed.). Diagnostic procedures for bacterial, mycotic and parasitic infections, 6th edition. American Public Health Association, Washington, D. C.

    Google Scholar 

  • Roggenkamp, A., Bittner, T., Leitritz, L., Sing, A. and Heesemann, J. (1997). Contribution of the Mn-cofactored superoxide dismutase (SodA) to the virulence of Yersinia enterocoli-tica serotype O8. Infect. Immun. 65, 4705-4710.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rosqvist, R., Skurnik, M. and Wolf-Watz, H. (1988). Increased virulence of Yersinia pseudo-tuberculosis by two independent mutations. Nature 334, 522-525.

    Article  CAS  PubMed  Google Scholar 

  • Ross, P.L., Huang, Y.N., Marchese, J.N., Williamson, B., Parker, K., Hattan, S., Khainovski, N., Pillai, S., Dey, S., Daniels, S., Purkayastha, S., Juhasz, P., Martin, S., Bartlet-Jones, M., He, F., Jacobson, A. and Pappin, D.J. (2004). Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell. Proteomics 3, 1154-1169.

    Article  CAS  PubMed  Google Scholar 

  • Sebbane, F., Lemaîre, N., Sturdevant, D.E., Rebeil, R., Virtaneva, K., Porcella, S.F. and Hinnebusch, B.J. (2006). Adaptive response of Yersinia pestis to extracellular effectors of innate immunity during bubonic plague. PNAS 103, 11766-11771.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seoh, H.K. and Tai, P.C. (1999). Catabolic repression of secB expression is positively con-trolled by cyclic AMP (cAMP) receptor protein-cAMP complexes at the transcriptional level. J. Bacteriol. 181, 1892-1899.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Simonet, M., Riot, B., Fortineau, M. and Berche, P. (1996). Invasin production by Yersinia pestis is abolished by insertion of an IS200-like element within the inv gene. Infect. Immun. 64, 375-379.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sodeinde, O.A. and Goguen, J.D. (1988). Genetic analysis of the 9.5-kilobase virulence plas-mid of Yersinia pestis. Infect. Immun. 56, 2743-2748.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sodeinde, O.A., Sample, A.K., Brubaker, R.R. and Goguen, J.D. (1988). Plasminogen activa-tor/coagulase gene of Yersinia pestis is responsible for degradation of plasmid-encoded outer membrane proteins. Infect. Immun. 56, 2749-2752.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stabler, R.A., Hinds, J., Witney, A.A., Isherwood, K., Oyston, P., Titball, R., Wren, B., Hinchliffe, S., Prentice, M., Mangan, J.A. and Butcher, P.D. (2003). Construction of a Yersinia pestis microarray. Adv. Exp. Med. Biol. 529, 47-49.

    Article  PubMed  Google Scholar 

  • Straley, S.C. and Perry, R.D. (1995). Environmental modulation of gene expression and patho-genesis in Yersinia. Trends Microbiol. 3, 310-317.

    Article  CAS  PubMed  Google Scholar 

  • Stretton, S. and Goodman, A.E. (1998). Carbon dioxide as a regulator of gene expression in microorganisms. Antonie Van Leeuwenhoek 73, 79-85.

    Article  CAS  PubMed  Google Scholar 

  • Sun, L., Fukamachi, T., Saito, H. and Kobayashi, H. (2005). Carbon dioxide increases acid resistance in Escherichia coli. Lett. Appl. Microbiol. 40, 397-400.

    Article  CAS  PubMed  Google Scholar 

  • Timm, J., Post, F.A., Bekker, L.G., Walther, G.B., Wainwright, H.C., Manganelli, R., Chan, W.T., Tsenova, L., Gold, B., Smith, I., Kaplan, G. and McKinney, J.D. (2003). Differen-tial expression of iron-, carbon-, and oxygen-responsive mycobacterial genes in the lungs of chronically infected mice and tuberculosis patients. PNAS U S A 100, 14321-14326.

    Article  CAS  Google Scholar 

  • Touati, D. (1997). Superoxide dismutases in bacteria and pathogen protists. Oxidative stress and the molecular biology of antioxidant defenses. J.G. Scandlios. New York, Cold Spring Harbor Laboratory Press: 447-493.

    Google Scholar 

  • Une, T. (1977). Studies on the pathogenicity of Yersinia enterocolitica. III. Comparative studies between Y. enterocolitica and Y. pseudotuberculosis. Microbiol. Immunol. 21, 505-516.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, D., Han, Y., Song, Y., Tong, Z., Wang, J., Guo, Z., Pei, D., Pang, X., Zhai, J., Li, M., Cui, B., Qi, Z., Jin, L., Dai, R., Du, Z., Bao, J., Zhang, X., Yu, J., Wang, J., Huang, P. and Yang, R. (2004). DNA microarray analysis of genome dynamics in Yersinia pestis: Insights into bacterial genome microevolution and niche adaptation. J. Bacteriol. 186, 5138-5146.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, D., Qin, L., Han, Y., Qiu, J., Chen, Z., Li, B., Song, Y., Wang, J., Guo, Z., Zhai, J., Du, Z., Wang, X. and Yang, R. (2006). Global analysis of iron assimilation and fur regulation in Yersinia pestis. FEMS Microbiol. Lett. 258, 9-17.

    Article  CAS  PubMed  Google Scholar 

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Bai, G., Pata, J., McDonough, K.A., Golubov, A., Smith, E. (2007). Differential Gene Regulation in Yersinia pestis versus Yersinia pseudotuberculosis: Effects of Hypoxia and Potential Role of a Plasmid Regulator. In: Perry, R.D., Fetherston, J.D. (eds) The Genus Yersinia. Advances In Experimental Medicine And Biology, vol 603. Springer, New York, NY. https://doi.org/10.1007/978-0-387-72124-8_11

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