Advertisement

Coping with High Temperature: A Unique Regulation in A. tumefaciens

  • Dvora Biran
  • Or Rotem
  • Ran Rosen
  • Eliora Z. RonEmail author
Chapter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 418)

Abstract

Elevation of temperature is a frequent and considerable stress for mesophilic bacteria. Therefore, several molecular mechanisms have evolved to cope with high temperature. We have been studying the response of Agrobacterium tumefaciens to temperature stress, focusing on two aspects: the heat-shock response and the temperature-dependent regulation of methionine biosynthesis. The results indicate that the molecular mechanisms involved in A. tumefaciens control of growth at high temperature are unique and we are still missing important information essential for understanding how these bacteria cope with temperature stress.

References

  1. Arsene F, Tomoyasu T, Bukau B (2000) The heat shock response of Escherichia coli. Int J Food Microbiol 55:3–9CrossRefGoogle Scholar
  2. Biran D, Brot N, Weissbach H, Ron EZ (1995) Heat shock-dependent transcriptional activation of the metA gene of Escherichia coli. J Bacteriol 177:1374–1379CrossRefGoogle Scholar
  3. Biran D, Gur E, Gollan L, Ron EZ (2000) Control of methionine biosynthesis in Escherichia coli by proteolysis. Mol Microbiol 37:1436–1443CrossRefGoogle Scholar
  4. Boshoff A, Stephens LL, Blatch GL (2008) The Agrobacterium tumefaciens DnaK: ATPase cycle, oligomeric state and chaperone properties. Int J Biochem Cell B 40:804–812CrossRefGoogle Scholar
  5. Chilton MD, Currier TC, Farrand SK, Bendich AJ, Gordon MP, Nester EW (1974) Agrobacterium-tumefaciens DNA and Ps8 bacteriophage DNA not detected in crown gall tumors. Proc Natl Acad Sci USA 71:3672–3676CrossRefGoogle Scholar
  6. Christians ES, Yan LJ, Benjamin IJ (2002) Heat shock factor 1 and heat shock proteins: critical partners in protection against acute cell injury. Crit Care Med 30:S43–S50CrossRefGoogle Scholar
  7. Craig EA (1985) The heat shock response. CRC Crit Rev Biochem 18:239–280CrossRefGoogle Scholar
  8. Erickson JW, Vaughn V, Walter WA, Neidhardt FC, Gross CA (1987) Regulation of the promoters and transcripts of rpoH, the Escherichia coli heat shock regulatory gene. Genes Develop 1:419–432CrossRefGoogle Scholar
  9. Ghazaei C (2017) Role and mechanism of the Hsp70 molecular chaperone machines in bacterial pathogens. J Med Microbiol 66:259–265CrossRefGoogle Scholar
  10. Grossman AD, Erickson JW, Gross CA (1984) The htpR gene product of E. coli is a sigma factor for heat-shock promoters. Cell 38:383–390CrossRefGoogle Scholar
  11. Guan N, Li J, Shin HD, Du G, Chen J, Liu L (2017) Microbial response to environmental stresses: from fundamental mechanisms to practical applications. Appl Microbiol Biotechnol 101:3991–4008CrossRefGoogle Scholar
  12. Guisbert E, Herman C, Lu CZ, Gross CA (2004) A chaperone network controls the heat shock response in E. coli. Genes Develop 18:2812–2821CrossRefGoogle Scholar
  13. Gur E, Biran D, Gazit E, Ron EZ (2002) In vivo aggregation of a single enzyme limits growth of Escherichia coli at elevated temperatures. Mol Microbiol 46:1391–1397CrossRefGoogle Scholar
  14. Gur E, Biran D, Ron EZ (2011) Regulated proteolysis in Gram-negative bacteria–how and when? Nature Rev Microbiol 9:839–848CrossRefGoogle Scholar
  15. Hecker M, Schumann W, Volker U (1996) Heat-shock and general stress response in Bacillus subtilis. Mol Microbiol 19:417–428CrossRefGoogle Scholar
  16. Herman C, Thevenet D, D’Ari R, Bouloc P (1995) Degradation of sigma 32, the heat shock regulator in Escherichia coli, is governed by HflB. Proc Natl Acad Sci USA 92:3516–3520CrossRefGoogle Scholar
  17. Hwang HH, Liu YT, Huang SC, Tung CY, Huang FC, Tsai YL, Cheng TF, Lai EM (2015) Overexpression of the HspL promotes Agrobacterium tumefaciens virulence in Arabidopsis under heat shock conditions. Phytopathol 105:160–168CrossRefGoogle Scholar
  18. Inbar O, Ron EZ (1993) Induction of cadmium tolerance in Escherichia coli K-12. FEMS Microbiol Lett 113:197–200CrossRefGoogle Scholar
  19. Katz C, Rasouly A, Gur E, Shenhar Y, Biran D, Ron EZ (2009) Temperature-dependent proteolysis as a control element in Escherichia coli metabolism. Res Microbiol 160:684–686CrossRefGoogle Scholar
  20. Li Z, Menoret A, Srivastava P (2002) Roles of heat-shock proteins in antigen presentation and cross-presentation. Curr Opin Immunol 14:45–51CrossRefGoogle Scholar
  21. Lindquist S (1986) The heat-shock response. Ann Rev. Biochem 55:1151–1191CrossRefGoogle Scholar
  22. Mathew A, Morimoto RI (1998) Role of the heat-shock response in the life and death of proteins. Ann NY Acad Sci 851:99–111CrossRefGoogle Scholar
  23. Mathew A, Shi Y, Jolly C, Morimoto RI (2000) Analysis of the mammalian heat-shock response. Inducible gene expression and heat-shock factor activity. Meth Mol Biol 99:217–255Google Scholar
  24. Michaud S, Marin R, Tanguay RM (1997) Regulation of heat shock gene induction and expression during Drosophila development. Cell Mol Life Sci 53:104–113CrossRefGoogle Scholar
  25. Mujacic M, Baneyx F (2006) Regulation of Escherichia coli hchA, a stress-inducible gene encoding molecular chaperone Hsp31. Mol Microbiol 60:1576–1589CrossRefGoogle Scholar
  26. Nakahigashi K, Yanagi H, Yura T (1995) Isolation and sequence analysis of rpoH genes encoding sigma 32 homologs from gram negative bacteria: conserved mRNA and protein segments for heat shock regulation. Nucl Acids Res 23:4383–4390PubMedGoogle Scholar
  27. Nakahigashi K, Yanagi H, Yura T (1998) Regulatory conservation and divergence of sigma32 homologs from Gram-negative bacteria: Serratia marcescens, Proteus mirabilis, Pseudomonas aeruginosa, and Agrobacterium tumefaciens. J Bacteriol 180:2402–2408PubMedPubMedCentralGoogle Scholar
  28. Nakahigashi K, Ron EZ, Yanagi H, Yura T (1999) Differential and independent roles of a sigma(32) homolog (RpoH) and an HrcA repressor in the heat shock response of Agrobacterium tumefaciens. J Bacteriol 181:7509–7515PubMedPubMedCentralGoogle Scholar
  29. Nakahigashi K, Yanagi H, Yura T (2001) DnaK chaperone-mediated control of activity of a sigma(32) homolog (RpoH) plays a major role in the heat shock response of Agrobacterium tumefaciens. J Bacteriol 183:5302–5310CrossRefGoogle Scholar
  30. Neidhardt FC, Phillips TA, VanBogelen RA, Smith MW, Georgalis Y, Subramanian AR (1981) Identity of the B56.5 protein, the A-protein, and the groE gene product of Escherichia coli. J Bacteriol 145:513–520PubMedPubMedCentralGoogle Scholar
  31. O’Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021PubMedPubMedCentralGoogle Scholar
  32. Ramsay N (1988) A mutant in a major heat shock protein of Escherichia coli continues to show inducible thermotolerance. Mol Gen Genet 211:332–334CrossRefGoogle Scholar
  33. Rasouly A, Shenhar Y, Ron EZ (2007) Thermoregulation of Escherichia coli hchA transcript stability. J Bacteriol 189:5779–5781CrossRefGoogle Scholar
  34. Ron EZ (1975) Growth rate of Enterobacteriaceae at elevated temperatures: limitation by methionine. J Bacteriol 124:243–246PubMedPubMedCentralGoogle Scholar
  35. Ron EZ (2009) An update on the bacterial stress response. Res Microbiol 160:243–244CrossRefGoogle Scholar
  36. Ron EZ, Davis BD (1971) Growth rate of Escherichia coli at elevated temperatures: limitation by methionine. J Bacteriol 107:391–396PubMedPubMedCentralGoogle Scholar
  37. Ron EZ, Shani M (1971) Growth rate of Escherichia coli at elevated temperatures: reversible inhibition of homoserine trans-succinylase. J Bacteriol 107:397–400PubMedPubMedCentralGoogle Scholar
  38. Ron EZ, Alajem S, Biran D, Grossman N (1990) Adaptation of Escherichia coli to elevated temperatures: the metA gene product is a heat shock protein. Antonie Van Leeuwenhoek 58:169–174CrossRefGoogle Scholar
  39. Rose JK, Rankin CH (2001) Analyses of habituation in Caenorhabditis elegans. Learn Mem 8:63–69CrossRefGoogle Scholar
  40. Rosen R, Ron EZ (2002) Proteome analysis in the study of the bacterial heat-shock response. Mass Spectrom Rev 21:244–265CrossRefGoogle Scholar
  41. Rosen R, Ron EZ (2011) Proteomics of a plant pathogen: Agrobacterium tumefaciens. Proteomics 11:3134–3142CrossRefGoogle Scholar
  42. Rosen R, Buttner K, Schmid R, Hecker M, Ron EZ (2001) Stress-induced proteins of Agrobacterium tumefaciens. FEMS Microbiol Ecol 35:277–285CrossRefGoogle Scholar
  43. Rosen R, Buttner K, Becher D, Nakahigashi K, Yura T, Hecker M, Ron EZ (2002) Heat shock proteome of Agrobacterium tumefaciens: evidence for new control systems. J Bacteriol 184:1772–1778CrossRefGoogle Scholar
  44. Rotem O, Biran D, Ron EZ (2013) Methionine biosynthesis in Agrobacterium tumefaciens: study of the first enzyme. Res Microbiol 164:12–16CrossRefGoogle Scholar
  45. Schumann W (2003) The Bacillus subtilis heat shock stimulon. Cell Stress Chaperones 8:207–217CrossRefGoogle Scholar
  46. Schumann W (2016) Regulation of bacterial heat shock stimulons. Cell Stress Chaperones 21:959–968CrossRefGoogle Scholar
  47. Segal G, Ron EZ (1993) Heat shock transcription of the groESL operon of Agrobacterium tumefaciens may involve a hairpin-loop structure. J Bacteriol 175:3083–3088CrossRefGoogle Scholar
  48. Segal G, Ron EZ (1995a) The dnaKJ operon of Agrobacterium tumefaciens: transcriptional analysis and evidence for a new heat shock promoter. J Bacteriol 177:5952–5958CrossRefGoogle Scholar
  49. Segal G, Ron EZ (1995b) The groESL operon of Agrobacterium tumefaciens: evidence for heat shock-dependent mRNA cleavage. J Bacteriol 177:750–757CrossRefGoogle Scholar
  50. Segal G, Ron EZ (1996a) Heat shock activation of the groESL operon of Agrobacterium tumefaciens and the regulatory roles of the inverted repeat. J Bacteriol 178:3634–3640CrossRefGoogle Scholar
  51. Segal G, Ron EZ (1996b) Regulation and organization of the groE and dnaK operons in Eubacteria. FEMS Microbiol Lett 138:1–10CrossRefGoogle Scholar
  52. Segal G, Ron EZ (1998) Regulation of heat-shock response in bacteria. Ann NY Acad Sci 851:147–151CrossRefGoogle Scholar
  53. Shenhar Y, Rasouly A, Biran D, Ron EZ (2009) Adaptation of Escherichia coli to elevated temperatures involves a change in stability of heat shock gene transcripts. Environ Microbiol 11:2989–2997CrossRefGoogle Scholar
  54. Srivastava P (2002) Roles of heat-shock proteins in innate and adaptive immunity. Nature Rev Immunol 2:185–194CrossRefGoogle Scholar
  55. Straus D, Walter W, Gross CA (1990) DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock gene expression by controlling the synthesis and stability of sigma 32. Genes Developt 4:2202–2209CrossRefGoogle Scholar
  56. Su SC, Stephens BB, Alexandre G, Farrand SK (2006) Lon protease of the alpha-proteobacterium Agrobacterium tumefaciens is required for normal growth, cellular morphology and full virulence. Microbiol-Sgm 152:1197–1207CrossRefGoogle Scholar
  57. Taylor WE, Straus DB, Grossman AD, Burton ZF, Gross CA, Burgess RR (1984) Transcription from a heat-inducible promoter causes heat shock regulation of the sigma subunit of E. coli RNA polymerase. Cell 38:371–381CrossRefGoogle Scholar
  58. Tomoyasu T, Gamer J, Bukau B, Kanemori M, Mori H, Rutman AJ, Oppenheim AB, Yura T, Yamanaka K, Niki H et al (1995) Escherichia coli FtsH is a membrane-bound, ATP-dependent protease which degrades the heat-shock transcription factor sigma 32. EMBO J 14:2551–2560CrossRefGoogle Scholar
  59. Tomoyasu T, Ogura T, Tatsuta T, Bukau B (1998) Levels of DnaK and DnaJ provide tight control of heat shock gene expression and protein repair in Escherichia coli. Mol Microbiol 30:567–581CrossRefGoogle Scholar
  60. Tsai YL, Wang MH, Gao C, Kluesener S, Baron C, Narberhaus F, Lai EM (2009) Small heat-shock protein HspL is induced by VirB protein(s) and promotes VirB/D4-mediated DNA transfer in Agrobacterium tumefaciens. Microbiol-Sgm 155:3270–3280CrossRefGoogle Scholar
  61. Tsai YL, Chiang YR, Narberhaus F, Baron C, Lai EM (2010) The Small heat-shock protein HspL is a VirB8 chaperone promoting Type IV secretion-mediated DNA transfer. J Biol Chem 285:19757–19766CrossRefGoogle Scholar
  62. Tsai YL, Chiang YR, Wu CF, Narberhaus F, Lai EM (2012) One out of Four: HspL but no other small heat shock protein of Agrobacterium tumefaciens acts as efficient virulence-promoting VirB8 chaperone. PLoS ONE 7:e49685CrossRefGoogle Scholar
  63. Yura T, Nakahigashi K (1999) Regulation of the heat-shock response. Curr Opin Microbiol 2:153–158CrossRefGoogle Scholar
  64. Yura T, Kawasaki Y, Kusukawa N, Nagai H, Wada C, Yano R (1990) Roles and regulation of the heat shock sigma factor sigma 32 in Escherichia coli. Antonie Van Leeuwenhoek 58:187–190CrossRefGoogle Scholar
  65. Zhou YN, Kusukawa N, Erickson JW, Gross CA, Yura T (1988) Isolation and characterization of Escherichia coli mutants that lack the heat shock sigma factor sigma 32. J Bacteriol 170:3640–3649CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Dvora Biran
    • 1
  • Or Rotem
    • 1
  • Ran Rosen
    • 1
  • Eliora Z. Ron
    • 1
    Email author
  1. 1.School of Molecular Cell Biology and Biotechnology, Faculty of Life SciencesTel Aviv UniversityTel AvivIsrael

Personalised recommendations