Comparison of the ${\sigma}^B$-Dependent General Stress Response between Bacillus subtilis and Listeria monocytogenes

Bacillus subtilis와 Listeria monocytogenes의 일반 스트레스반응의 비교

  • Shin, Ji-Hyun (Department of Microbiology, Kyungpook National University School of Medicine)
  • 신지현 (경북대학교 의과대학 미생물학교실)
  • Published : 2009.03.31

Abstract

A diverse range of stresses such as heat, cold, salt, ethanol, oxygen starvation or nutrient starvation induces same stress-responsive proteins. This general stress response enhances bacterial survival significantly. In Bacillus subtilis and closely related Gram-positive bacteria Listeria monocytogenes, the general stress response is controlled by the alternative transcription factor ${\sigma}^B$. The activity of ${\sigma}^B$ is regulated post-translationally by a signal transduction network that has been extensively studied in B. subtilis, and serve as a model for L. monocytogenes. The proposed model of L. monocytogenes signal transduction network is similar to that of B. subtilis, but the energy stress pathway is missing. More than 150 general stress proteins belong to ${\sigma}^B$ regulon of B. subtilis and L. monocytogenes. In both bacteria, ${\sigma}^B$ function is primarily important for resistance to diverse stresses. In addition, ${\sigma}^B$ function contributes to the control of important virulence genes in food-borne pathogen L. monocytogenes. Therefore, understanding of the general stress response is important not only for bacterial physiology, but also for pathogenicity.

일부 그람양성세균들은 고온, 저온, 염, 에탄올, 산소와 영양분 고갈과 같은 다양한 스트레스 상태에 노출되면, 일반 스트레스반응(general stress response)에 의해서 일련의 스트레스 단백질군을 발현시켜 외부 스트레스를 극복하고 세균의 생존력을 증가시킨다. 비병원성균인 Bacillus subtilis의 일반 스트레스반응에 관해서는 많은 연구가 이루어져 있으므로 다른 균의 연구모델로 이용이 가능하다. 본 총설에서는 B. subtilis와 병원성균인 Listeria monocytogenes의 일반 스트레스반응의 유사성과 차이점을 B. subtilis를 모델로 하여 비교하였다. 두 균의 일반 스트레스반응은 대체 전사 인자인 ${\sigma}^B$ (alternative transcription factor sigma B)에 의해서 조절되고 신호전달 네트워크 또한 매우 유사하며, ${\sigma}^B$ 의존성 유전자들에 의해 150여 개의 스트레스 단백질들이 발현된다. 그러나 L. monocytogenes는 B. subtilis의 에너지 스트레스 신호 경로를 가지고 있지 않은 점과, 일반 스트레스반응에 의해 병독 유전자들(virulence genes)이 조절되는 것이 가장 큰 차이점이다. 그러므로 L. monocytogenes의 생리 및 병원성 규명을 위해서는 일반 스트레스반응에 관한 이해가 매우 중요하다.

Keywords

References

  1. Alper, S., L. Duncan, and R. Losick. 1994. An adenosine nucleotide switch controlling the activity of a cell type-specific transcription factor in B. subtilis. Cell 77, 195-205 https://doi.org/10.1016/0092-8674(94)90312-3
  2. Bagyan, I., L. Casillas-Martinez, and P. Setlow. 1998. The katX gene, which codes for the catalase in spores of Bacillus subtilis, is a forespore-specific gene controlled by $\sigma$$^F$, and KatX is essential for hydrogen peroxide resistance of the germinating spore. J. Bacteriol. 180, 2057-2062
  3. Bayles, D.O. and B.J. Wilkinson. 2000. Osmoprotectants and cryoprotectants for Listeria monocytogenes. Lett. Appl. Microbiol. 30, 23-27 https://doi.org/10.1046/j.1472-765x.2000.00646.x
  4. Begley, M., R.D. Sleator, C.G.M. Gahan, and C. Hill. 2005. Contribution of three bile-associated loci, bsh, pva, and btlB, to gastrointestinal persistence and bile tolerance of Listeria monocytogenes. Infect. Immun. 73, 894-904. https://doi.org/10.1128/IAI.73.2.894-904.2005
  5. Benson, A.K. and W.G. Haldenwang. 1992. Characterization of a regulatory network that control $\sigma$$^B$ expression in Bacillus subtilis. J. Bacteriol. 174, 749-757 https://doi.org/10.1128/jb.174.3.749-757.1992
  6. Bernhardt, J., U. V$\ddot{o}$lker, A. V $\ddot{o}$lker, H. Antelmann, R. Schmid, H. Mach, and M. Hecker. 1997. Specific and general stress proteins in Bacillus subtilis-a two-dimensional protein electrophoresis study. Microbiology 143, 999-1017 https://doi.org/10.1099/00221287-143-3-999
  7. Boylan, S.A., A.R. Redfield, M.S. Brody, and C.W. Price. 1993. Stress-induced activation of the $\sigma$$^B$ transcription factor of Bacillus subtilis. J. Bacteriol. 175, 7931-7937 https://doi.org/10.1128/jb.175.24.7931-7937.1993
  8. Braden, C.R. 2003. Listeriosis. Pediatr. Infect. Dis. J. 22, 745-746 https://doi.org/10.1097/01.inf.0000079439.30496.57
  9. Brigulla, M., T. Hoffmann, A. Krisp, A. V$\ddot{o}$lker, E. Bremer, and U. V$\ddot{o}$lker. 2003. Chill induction of the SigB-dependent general stress response in Bacillus subtilis and its contribution to low-temperature adaptation. J. Bacteriol. 185, 4305-4314 https://doi.org/10.1128/JB.185.15.4305-4314.2003
  10. Chakraborty, T., M. Leimeister-Wchter, E. Domann, M. Hartl, W. Goebel, T. Nichterlein, and S. Notermans. 1992. Coordinate regulation of virulence genes in Listeria monocytogenes requires the product of the prfA gene. J. Bacteriol. 174, 568-574 https://doi.org/10.1128/jb.174.2.568-574.1992
  11. Chan, Y.C., K.J. Boor, and M. Wiedmann. 2007. $\sigma$$^B$-dependent and $\sigma$$^B$-independent mechanisms contribute to transcription of Listeria monocytogenes cold stress genes during cold shock and cold growth. Appl. Environ. Microbiol. 73, 6019-6029 https://doi.org/10.1128/AEM.00714-07
  12. Chaturongakul, S. and K.J. Boor. 2004. RsbT and RsbV contribute to $\sigma$$^B$-dependent survival under environmental, energy, and intracellular stress conditions in Listeria monocytogenes. Appl. Environ. Microbiol. 70, 5349-5356 https://doi.org/10.1128/AEM.70.9.5349-5356.2004
  13. Cole, M.B., M.V. Jones, and C. Holyoak. 1990. The effect of pH, salt concentration and temperature on the survival and growth of Listeria monocytogenes. J. Appl. Bacteriol. 69, 63-72 https://doi.org/10.1111/j.1365-2672.1990.tb02912.x
  14. Cotter, P.D., C.G.M. Gahan, and C. Hill. 2001. A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Mol. Microbiol. 40, 2465-2475 https://doi.org/10.1046/j.1365-2958.2001.02398.x
  15. Davis, M.J., P.J. Coote, and C.P. O'Byrne. 1996. Acid tolerance in Listeria monocytogenes: the adaptive acid tolerance response (ATR) and growth phase-dependent acid resistance. Microbiology 142, 2975-2982 https://doi.org/10.1099/13500872-142-10-2975
  16. Dufour, A. and W.G. Haldenwang. 1994. Interactions between a Bacillus subtilis anti-sigma factor (RsbW) and its antagonist (RsbV). J. Bacteriol. 176, 1813-1820 https://doi.org/10.1128/jb.176.7.1813-1820.1994
  17. Engelmann, S., C. Lindner, and M. Hecker. 1995. Cloning, nucleotide sequence, and regulation of katE encoding a $\sigma$$^B$-dependent catalase in Bacillus subtilis. J. Bacteriol. 177, 5598-5605 https://doi.org/10.1128/jb.177.19.5598-5605.1995
  18. Ferreira, A., C.P. O’ Byrne, and K.J. Boor. 2001. Role of $\sigma$$^B$ in heat, ethanol, acid, and oxidative stress resistance and during carbon starvation in Listeria monocytogenes. Appl. Environ. Microbiol. 67, 4454-4457 https://doi.org/10.1128/AEM.67.10.4454-4457.2001
  19. Fraser, K.R., D. Sue, M. Wiedmann, K. Boor, and C.P. O'Byrne. 2003. Role of $\sigma$$^B$ in regulating the compatible solute uptake systems of Listeria monocytogenes: osmotic induction of opuC is $\sigma$$^B$ dependent. Appl. Environ. Microbiol. 69, 2015-2022 https://doi.org/10.1128/AEM.69.4.2015-2022.2003
  20. Glaser, P., L. Frangeul, C. Buchrieser, C. Rusniok, A. Amend, F. Baquero, P. Berche, H. Bloecker, P. Brandt, T. Chakraborty, A. Charbit, F. Chetouani, E. Couv, A. de Daruvar, P. Dehoux, E. Domann, G. Domnguez-Bernal, E. Duchaud, L. Durant, O. Dussurget, K.D. Entian, H. Fsihi, F. Garca-del Portillo, P. Garrido, L, Gautier, W. Goebel, N. Gmez-Lpez, T. Hain, J. Hauf, D. Jackson, L.M. Jones, U. Kaerst, J. Kreft, M. Kuhn, F. Kunst, G. Kurapkat, E. Madueno, A. Maitournam, J.M. Vicente, E. Ng, H. Nedjari, G. Nordsiek, S. Novella, B. de Pablos, J.C. Prez-Diaz, R. Purcell, B. Remmel, M. Rose, T. Schlueter, N. Simoes, A. Tierrez, J.A. Vzquez-Boland, H. Voss, J. Wehland, and P. Cossart. 2001. Comparative genomics of Listeria species. Science 294, 849-852 https://doi.org/10.1126/science.1063447
  21. Haldenwang, W.G. 1995. The sigma factors of Bacllus subtilis. Microbiol. Rev. 59, 1-30
  22. Haldenwang, W.G. and R. Losick. 1979. A modified RNA polymerase transcribes a cloned gene under sporulation control in Bacillus subtilis. Nature 282, 256-260 https://doi.org/10.1038/282256a0
  23. Haldenwang, W.G. and R. Losick. 1980. Novel RNA polymerase $\sigma$ factor from Bacillus subtilis. Proc. Natl. Acad. Sci. USA 77, 7000-7004 https://doi.org/10.1073/pnas.77.12.7000
  24. Hardy, J., J.J. Margolis, and C.H. Contag. 2006. Induced biliary excretion of Listeria monocytogenes. Infect. Immun. 74, 1819-1827 https://doi.org/10.1128/IAI.74.3.1819-1827.2006
  25. Hecker, M. and U. V$\ddot{o}$lker. 2001. General stress response of Bacillus Bacillus subtilis and other bacteria. Adv. Microb. Physiol. 44, 35-91 https://doi.org/10.1016/S0065-2911(01)44011-2
  26. Hennge-Aronis, R. 2000. The general stress response in Escherichia coli, pp. 161-178. In G. Storz and R. Hennge-Aronis (eds.), Bacterial Stress Responses. American Society for Microbiology, Washington, D.C., USA
  27. Kalman, S., M.L. Duncan, S.M. Thomas, and C.W. Price. 1990. Similar organization of the sigB and spoIIA operons encoding alternate sigma factors of Bacillus subtilis RNA polymerase. J. Bacteriol. 172, 5575-5585 https://doi.org/10.1128/jb.172.10.5575-5585.1990
  28. Kang, C.M., M.S. Brody, S. Akbar, X. Yang, and C.W. Price. 1996. Homologous pairs of regulatory proteins control activity of Bacillus subtilis transcription factor $\sigma$$^B$ in response to environmental stress. J. Bacteriol. 178, 3846-3853 https://doi.org/10.1128/jb.178.13.3846-3853.1996
  29. Karzai, A.W., E.D. Roche, and R.T. Sauer. 2000. The SsrA-SmpB system for protein tagging, directed degradation and ribosome rescue. Nat. Struct. Biol. 7, 449-455 https://doi.org/10.1038/75843
  30. Karzai, A.W. and R.T. Sauer. 2001. Protein factors associated with the SsrA-SmpB tagging and ribosome rescue complex. Proc. Natl. Acad. Sci. USA 98, 3040-3044 https://doi.org/10.1073/pnas.051628298
  31. Kazmierczak, M.J., W. Wiedmann, and K.J. Boor. 2005. Alternative sigma factor and their roles in bacterial virulence. Microbiol. Mol. Biol. Rev. 69, 527-543 https://doi.org/10.1128/MMBR.69.4.527-543.2005
  32. Kazmierczak, M.J., S.C. Mithoe, K.J. Boor, and M. Wiedmann. 2003. Listeria monocytogenes $\sigma$$^B$ regulates stress response and virulence functions. J. Bacteriol. 185, 5722-5734 https://doi.org/10.1128/JB.185.19.5722-5734.2003
  33. Kim, H., H. Marquis, and K.J. Boor. 2005. $\sigma$$^B$ contributes to Listeria monocytogenes invasion by controlling expression of inlA and inlB. Microbiology 151, 3215-3222 https://doi.org/10.1099/mic.0.28070-0
  34. Kim, Y.I., R.E. Burton, B.M. Burton, R.T. Sauer, and T.A. Baker. 2000. Dynamics of substrate denaturation and translocation by the ClpXP degradation machine. Mol. Cell. 5, 639-648 https://doi.org/10.1016/S1097-2765(00)80243-9
  35. Krger, E., E. Witt, S. Ohlmeier, R. Hanschke, and M. Hecker. 2000. The clp proteases of Bacillus subtilis are directly involved in degradation of misfolded proteins. J. Bacteriol. 182, 3259-3265 https://doi.org/10.1128/JB.182.11.3259-3265.2000
  36. Lange, R. and R. Hengge-Aronis. 1991. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol. Microbiol. 5, 49-59 https://doi.org/10.1111/j.1365-2958.1991.tb01825.x
  37. McLauchlin, J., R.T. Mitchell, W.J. Smerdon, and K. Jewell. 2004. Listeria monocytogenes and listeriosis: a review of hazard characterisation for use in microbiological risk assessment of foods. Int. J. Food Microbiol. 92, 15-33 https://doi.org/10.1016/S0168-1605(03)00326-X
  38. Muto, A., A. Fujihara, K.I. Ito, J. Matsuno, C. Ushida, and H. Himeno. 2000. Requirement of transfer-messenger RNA for the growth of Bacillus subtilis under stresses. Genes Cells 5, 627-635 https://doi.org/10.1046/j.1365-2443.2000.00356.x
  39. Nadon, C., B.M. Bowen, M. Wiedmann, and K.J. Boor. 2002. $\sigma$$^B$ contributes to PrfA-mediated virulence in Listeria monocytogenes. Infect. Immun. 70, 3948-3952 https://doi.org/10.1128/IAI.70.7.3948-3952.2002
  40. Nair, S., E. Milohanic, and P. Berche. 2000. ClpC ATPase is required for cell adhesion and invasion of Listeria monocytogenes. Infect. Immun. 68, 7061-7068 https://doi.org/10.1128/IAI.68.12.7061-7068.2000
  41. O'Byrne, C.P. and K.A.G. Karatzas. 2008. The role of sigma B ($\sigma$$^B$) in the stress adaptations of Listeria monocytogenes: overlaps between stress adaptation and virulence. Adv. Appl. Microbiol. 65, 115-140 https://doi.org/10.1016/S0065-2164(08)00605-9
  42. Petersohn, A., H. Antelmann, U. Gerth, and M. Hecker. 1999. Identification and transcriptional analysis of new members of the $\sigma$$^B$ regulon in Bacillus subtilis. Microbiology 145, 869-880 https://doi.org/10.1099/13500872-145-4-869
  43. Price, C.W. 2000. Protective function and regulation of the general stress response in Bacillus subtilis and related gram-positive bacteria, pp. 179-197. In G. Storz and R. Hengge-Aronis (eds.), Bacterial Stress Responses. American Society for Microbiology, Washington, D.C., USA
  44. Price, C.W. 2002. General stress response, pp. 369-384. In A.L. Sonenshein, R. Losick, and J.A. Hoch (eds.), In Bacillus subtilis and its closest relatives: from genes to cells. American Society for Microbiology, Washington, D.C., USA
  45. Price, C.W., P. Fawcett, H. Crmonie, N. Su, C.K. Murphy, and P. Youngman. 2001. Genome-wide analysis of the general stress response in Bacillus subtilis. Mol. Microbiol. 41, 757-774 https://doi.org/10.1046/j.1365-2958.2001.02534.x
  46. Raengpradub, S., M. Wiedmann, and K.J. Boor. 2008. Comparative analysis of the $\sigma$$^B$-dependent stress responses in Listeria monocytogenes and Listeria innocua strains exposed to selected stress conditions. Appl. Environ. Microbiol. 74, 158-171 https://doi.org/10.1128/AEM.00951-07
  47. Shin, J.H., M.S. Brody, and C.W. Price. Unpublished results
  48. Spiegelhalter, F. and E. Bremer. 1998. Osmoregulation of the opuE proline transport gene from Bacillus subtilis: contributions of the $\sigma$$^A$-and $\sigma$$^B$-dependent stress-responsive promoters. Mol. Microbiol. 29, 285-296 https://doi.org/10.1046/j.1365-2958.1998.00929.x
  49. Sue, D., D. Fink, M. Wiedmann, and K.J. Boor. 2004. $\sigma$$^B$-dependent gene induction and expression in Listeria monocytogenes during osmotic and acid stress conditions simulating the intestinal environment. Microbiology 150, 3843-3855 https://doi.org/10.1099/mic.0.27257-0
  50. Sue, D., K.J. Boor, and M. Wiedmann. 2003. $\sigma$$^B$-dependent expression patterns of compatible solute transporter genes opuCA and lmo1421 and the conjugated bile salt hydrolase gene bsh in Listeria monocytogenes. Microbiology 149, 3247-3256 https://doi.org/10.1099/mic.0.26526-0
  51. Vijay, K., M.S. Brody, E. Fredlund, and C.W. Price. 2000. A PP2C phophatase containing a PAS domain is required to convey signals of energy stress to the $\sigma$$^B$ transcription factor of Bacillus subtilis. Mol. Microbiol. 35, 180-188 https://doi.org/10.1046/j.1365-2958.2000.01697.x
  52. Voelker, U., A. Voelker, B. Maul, M. Hecker, A. Dufour, and W.G. Haldenwang. 1995. Separate mechanism activate $\sigma$$^B$ of Bacillus subtilis in response to environmental and metabolic stresses. J. Bacteriol. 177, 3771-3780 https://doi.org/10.1128/jb.177.13.3771-3780.1995
  53. V$\ddot{o}$lker, U., B. Maul, and M. Hecker. 1999. Expression of the $\sigma$$^B$-dependent general stress regulon confers multiple stress resistance in Bacillus subtilis. J. Bacteriol. 181, 3942-3948
  54. Von Blohn, C., B. Kempf, R.M. Kappes, and E. Bremer. 1997. Osmostress response in Bacillus subtilis: characterization of a proline uptake system (OpuE) regulated by high osmolarity and the alternative transcription factor $\sigma$$^B$. Mol. Microbiol. 25, 175-187 https://doi.org/10.1046/j.1365-2958.1997.4441809.x
  55. Walker, S.J., P. Archer, and J.G. Banks. 1990. Growth of Listeria monocytogenes at refrigeration temperatures. J. Appl. Bacteriol. 68, 157-162 https://doi.org/10.1111/j.1365-2672.1990.tb02561.x
  56. Wemekamp-Kamphuis, H.H., R.D. Sleator, J.A. Wouters, C. Hill, and T. Abee. 2004. Molecular and physiological analysis of the role of osmolyte transporters BetL, Gbu, and OpuC in growth of Listeria monocytogenes at low temperatures. Appl. Environ. Microbiol. 70, 2912-2918 https://doi.org/10.1128/AEM.70.5.2912-2918.2004
  57. Wemekamp-Kamphuis, H.H., J.A. Wouters, P.P.L.A. de Leeuw, T. Hain, T. Chakraborty, and T. Abee. 2004. Identification of sigma factor $\sigma$$^B$-controlled genes and their impact on acid stress, high hydrostatic pressure, and freeze survival in Listeria monocytogenes EGD-e. Appl. Environ. Microbiol. 70, 3457-3466 https://doi.org/10.1128/AEM.70.6.3457-3466.2004
  58. Wiedmann, M., T.J. Arvik, R.J. Hurley, and K.J. Boor. 1998. General stress transcription factor $\sigma$$^B$ and its role in acid tolerance and virulence of Listeria monocytogenes. J. Bacteriol. 180, 3650-3656
  59. Wise, A.A. and C.W. Price. 1995. Four additional genes in the sigB operon of Bacillus subtilis that control activity of the general stress factor $\sigma$$^B$ in response to environmental signals. J. Bacteriol. 177, 123-133 https://doi.org/10.1002/path.1711770204
  60. Zheleznova, E.E., P.N. Markham, A.A. Neyfakh, and R.G. Brennan. 1997. Preliminary structural studies on the multi-ligand-binding domain of the transcription activator, BmrR, from Bacillus subtilis. Protein Sci. 6, 2465-2468 https://doi.org/10.1002/pro.5560061122
  61. Zheng, W. and S. Kathariou. 1995. Differentiation of epidemicassociated strains of Listeria monocytogenes by restriction fragment length polymorphism in a gene region essential for growth at low temperatures (4$^{\circ}C$). Appl. Environ. Microbiol. 61, 4310-4314
  62. Yang, X., C.M. Kang, M.S. Brody, and C.W. Price. 1996. Opposing pairs of serine protein kinases and phosphatases transmit signals of environmental stress to activate a bacterial transcription factor. Genes Dev. 10, 2265-2275 https://doi.org/10.1101/gad.10.18.2265