Antonie van Leeuwenhoek

, Volume 81, Issue 1–4, pp 3–13 | Cite as

Defences against oxidative stress during starvation in bacteria

  • Diane McDougald
  • Lan Gong
  • Sujatha Srinivasan
  • Erika Hild
  • Lyndal Thompson
  • Kathy Takayama
  • Scott A. Rice
  • S. Kjelleberg
Article

Abstract

It now seems clear that starvation adaptation is important for cells to initiate long-term survival under conditions of not only nutrient depletion but to develop resistance to other stresses, most notably oxidative stress. Clearly, oxidative stress is a condition likely to be perceived by many bacteria, for example, in the form of reactive oxygen species derived from metabolic processes or from near-UV exposure. We have found evidence for a large degree of overlap in the cell's use of global regulators to deal with both starvation and oxidative stress. Both SpoT and AI-2 signalling pathways are important regulators of starvation and stress adaptation as well as the alternative sigma factor, RpoE. We also present evidence that suggests that AI-2 signalling can mediate starvation adaptation at the molecular level by increasing the stability of the mRNAs so that cells are prepared for rapid response to nutrient addition. Moreover, such extracellular signals mediate intraspecies communication to enable enhanced survival and stress resistance of neighbouring bacterial cells. It is likely that bacteria rely on a suite of effects between cells and on transcription, translation and post-translational processes, mediated by global regulators and signalling molecules, to meet their needs for growth and survival.

oxidative stress quorum sensing sigma factors signalling systems SpoT starvation vibrio 

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References

  1. Almirón M, Link AJ, Furlong D & Kolter R (1992) A novel DNA binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 6: 2646-2654.PubMedGoogle Scholar
  2. Bassler BL (1999) How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr. Opin. Microbiol. 2: 582-587.PubMedCrossRefGoogle Scholar
  3. Bassler BL, Wright M & Silverman MR (1994). Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol. Microbiol. 13: 273-286.PubMedGoogle Scholar
  4. Bassler BL, Greenberg EP & Stevens AM (1997) Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi. J. Bacteriol. 179: 4043-4045.PubMedGoogle Scholar
  5. Cashel M (2000). Stringent response. In: Lederberg J (Ed) Encyclopedia of Microbiology. (pp 467-477). Academic Press, San Diego, CA.Google Scholar
  6. Cashel M, Gentry DR, Hernandez VJ & Vinella, D (1996) The stringent response. In: Neidhardt FC, Curtiss R, Gross CA, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff W, Riley M, Schaechter M & Umbarger HE (Eds) Escherichia coli and Salmonell typhimurium: Cellular and Molecular Biology. (pp 1458-1496). American Society for Microbiology Press, Washington, DCGoogle Scholar
  7. Chatterji D & Ojha AK (2001) Revisiting the stringent response, ppGpp and starvation signaling. Curr. Opin. Microbiol. 4: 160-165.PubMedCrossRefGoogle Scholar
  8. deNys R, Steinberg PD, Rogers CN, Charlton TS & Duncan MW (1996) Quantitative variation of secondary metabolites in the sea hare Aplysia parvula and its host plant, Delisea pulchra. Marine Ecol. Prog. Series 130: 135-146.Google Scholar
  9. DiRusso CC & Nyström T (1998) The fats of Escherichia coli during infancy and old age: regulation by global regulators, alarmones and lipid intermediates. Mol. Microbiol. 27: 1-8.PubMedCrossRefGoogle Scholar
  10. Dukan S & Nystrom T (1998) Bacterial senescence: stasis results in increased and differential oxidation of cytoplasmic proteins leading to developmental induction of the heat shock regulon. Genes Dev. 12: 3431-3441.PubMedGoogle Scholar
  11. Eberl L, Christiansen G, Molin S & Givskov M (1996) Differentiation of Serratia liquefaciens into swarm cells is controlled by the expression of the flhD master operon. J. Bacteriol. 178: 554-559.PubMedGoogle Scholar
  12. Ferenci T (2001) Hungry bacteria-definition and properties of a nutritional state. Environ. Microbiol. 3: 605-611.PubMedCrossRefGoogle Scholar
  13. Flärdh K, Axberg T, Albertson N & Kjelleberg S (1994). Stringent control during carbon starvation of marine Vibrio sp. strain S14: molecular cloning, nucleotide sequence, and deletion of the relA gene. J. Bacteriol. 176: 5949-5957.PubMedGoogle Scholar
  14. Flavier AB, Schell MA & Denny TP (1998). An Rpos (σs) homologue regulates acylhomoserine lactone-dependent autoinduction in Ralstonia solanacearum. Mol. Microbiol. 28: 475-486.PubMedCrossRefGoogle Scholar
  15. Foster JW & Spector MP (1995) How Salmonella survive against the odds. Annu. Rev. Microbiol. 49: 145-174.PubMedCrossRefGoogle Scholar
  16. Gentry DR & Cashel M (1995). Cellular localization of the Eshcerichia coli SpoT protein. J. Bacteriol. 177: 3890-3893.PubMedGoogle Scholar
  17. Gentry DR, Hernandez VJ, Nguyen LH, Jensen DB & Cashel M (1993) Synthesis of the stationary-phase sigma factor σS is positively regulated by ppGpp. J. Bacteriol. 175: 7982-7989.PubMedGoogle Scholar
  18. Givskov M, DeNys R, Manefield M, Gram L, Maximilien R, Eberl L, Molin S, Steinberg P D & Kjelleberg S (1996) Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J. Bacteriol. 178: 6618-6622.PubMedGoogle Scholar
  19. Givskov M, Eberl L & Molin S (1997) Control of exoenzyme production, motility and cell differentiation in Serratia liquefaciens. FEMS Microbiol. Lett. 148: 115-122.CrossRefGoogle Scholar
  20. Givskov M, Eberl L, Moller S, Poulsen LK & Molin S (1994) Responses to nutrient starvation in Pseudomonas putida KT2442: analysis of general cross-protection, cell shape, and macromolecular content. J. Bacteriol. 176: 7-14.PubMedGoogle Scholar
  21. Gong L, Takayama K & Kjelleberg S (2001) Near-ultraviolet resistance and carbon starvation survival in cool white light-exposed cells of Escherichia coli and Vibrio angustum S14. In 101th General Meeting of the American Society for Microbiology. American Society for Microbiology Press, Orlando. pp. Abstract Q111.Google Scholar
  22. Gong L, Takayama K & Kjelleberg S (2002) Role of spoT-dependent ppGpp accumulation in the survival of light-exposed starved bacteria. Microbiol. 148: 559-570.Google Scholar
  23. Hassett DJ, Ma J-F, Elkins JG, McDermott TR, Ochsner UA, West SEH, Huang C-T, Fredericks J, Burnett S, Stewart PS, McFeters G, Passador L & Iglewski B H (1999) Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol. Microbiol. 34: 1082-1093.PubMedCrossRefGoogle Scholar
  24. Hengge-Aronis R (1996) Regulation of gene expression during entry into stationary phase. In: Neidhardt FC, Curtiss R, Gross CA, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff W, Riley M, Schaechter M & Umbarger HE (Eds) Escherichia coli and Salmonella typhimurium Cellular and Molecular Biology, (pp 1497-1512). American Society for Microbiology Press, Washington, DCGoogle Scholar
  25. Hild E (2001) The role of extracytoplasmic function (ECF) sigma factor RpoE in the adaptive responses of the marine bacterium Vibrio angustum S14. Ph.D. Thesis University of New South Wales, Sydney, Australia.Google Scholar
  26. Hild E, Takayama K, Olsson R-M & Kjelleberg S (2000) Evidence for a role of rpoE in stressed and unstressed cells of marine Vibrio angustum strain S14. J. Bacteriol. 182, 6964-6974.PubMedCrossRefGoogle Scholar
  27. Huang X & Helmann JD (1998) Identification of target promoters for the Bacillus subtilis sx factor using a consensus-directed search. J. Mol. Biol. 279: 165-173.PubMedCrossRefGoogle Scholar
  28. Huang X, Decatur A, Sorokin A & Helmann JD (1997) The Bacillus subtilis sx protein is an extracytoplasmic function σ factor contributing to survival at high temperature. J. Bacteriol. 179: 2915-2921.PubMedGoogle Scholar
  29. Huang X, Fredrick KL & Helmann JD (1998) Promoter recognition by Bacillus subtilis sx W: autoregulation and partial overlap with the σ regulon. J. Bacteriol. 180: 3765-3770.PubMedGoogle Scholar
  30. Huang X, Gaballa A, Cao M & Helmann JD (1999) Identification of target promoters for the Bacillus subtilis extracytoplasmic function σ factor, σW. Mol. Microbiol. 31: 361-371.PubMedCrossRefGoogle Scholar
  31. Huisman GW, Siegele DA, Zambrano MM & Kolter R (1996). Morphological and physiological changes during stationary phase. In: Neidhardt FC, Curtiss R, Gross CA, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff W, Riley M, Schaechter M & Umbarger HE (Eds) Escherichia coli and Salmonell typhimurium: Cellular and Molecular Biology, (pp 1672-1682). American Society for Microbiology Press, Washington, DC.Google Scholar
  32. Jagger J (1981). Near-UV radiation effects on microorganisms. Photochem. Photobiol. 34: 761-768.PubMedGoogle Scholar
  33. Jenkins DE, Schultz JE & Matin A (1988). Starvation-induced cross protection against heat or H2O2 challange in Escherichia coli. J. Bacteriol. 170: 3910-3914.PubMedGoogle Scholar
  34. Jones GH, Paget MSB, Chamberlin L & Buttner MJ (1997). Sigma-E is required for the production of the antibiotic actinomycin in Streptomyces antibioticus. Mol. Microbiol. 23: 169-178.PubMedCrossRefGoogle Scholar
  35. Jørgensen F, Nybroe O & Knøchel S (1994) Effects of starvation and osmotic stress on viability and heat resistance of Psedomonas flourescens AH9. J. Appl. Bacteriol. 77: 340-347.Google Scholar
  36. Kjelleberg S, Östling J, Holmquist L, Flärdh K, Svenblad B, Jouper-Jaan Å, Weichart D & Albertson N (1993) Starvation and recovery of Vibrio. In: Pedrós-Alió RGC (Ed) Trends in Microbial Ecology, (pp 169-174). Spanish Society for Microbiology.Google Scholar
  37. Latifi A, Foglino M, Tanaka K, Williams P & Lazdunski A (1996) A hierarchial quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhlR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol. Microbiol. 21: 1137-1146.PubMedCrossRefGoogle Scholar
  38. Lonetta MA, Brown KL, Rudd KE & Buttner MJ (1994) Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase σ factors involved in the regulation of extracytoplasmic functions. Proc. Natl. Acad. Sci., USA 91: 7573-7577.CrossRefGoogle Scholar
  39. Manefield M, de NR, Kumar N, Read R, Givskov M, Steinberg P & Kjelleberg S (1999) Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology 145: 283-291.PubMedCrossRefGoogle Scholar
  40. Manefield M, Harris L, Rice SA, De Nys R & Kjelleberg S (2000) Inhibition of luminescence and virulence in the black tiger prawn (Penaeus monodon) pathogen Vibrio harveyi by intercellular signal antagonists. Appl. Environ. Microbiol. 66: 2079-2084.PubMedCrossRefGoogle Scholar
  41. Marouga R (1999) The outgrowth response in Vibrio angustum S14: Identification and regulation of immediate upshift proteins. Ph.D. Thesis University of Goteborg, Sweden.Google Scholar
  42. Marouga R & Kjelleberg S (1996) Synthesis of immediate upshift (Iup) proteins during recovery of marine Vibrio sp. strain S14 subjected to long-term carbon starvation. J. Bacteriol. 178: 817-822.PubMedGoogle Scholar
  43. Martinez-Salazar JM, Moreno S, Nájera R, Boucher JC, Espin G, Soberón-Chávez G & Deretic V (1996). Characterization of the genes coding for the putative sigma factor AlgU and its regulators MucA, MucB, MucC and MucD in Azotobacter vinelandii and evaluation of their roles in alginate biosynthesis. J. Bacteriol. 178: 1800-1808.PubMedGoogle Scholar
  44. Mathee K, Ciofu O, Sternberg C, Lindum PW, Campbell JIA, Jensen P, Johnsen AH, Givskov M, Ohman DE, Molin S, Høiby N & Kharazmi A (1999) Mucoid conversion of Pseudomonas aeruginosa by hydrogen peroxide: a mechanism for virulence activation in the cystic fibrosis lung. Microbiology 145: 1349-1357. Academic Press, San Diego, CA.Google Scholar
  45. Matin A (1990) Molecular analysis of the starvation stress in Escherichia coli. FEMS Microbiol. Ecol. 74: 185-196.CrossRefGoogle Scholar
  46. Matin A (2000) Bacterial starvation. In: Lederberg J (Ed) Encyclopedia of Microbiology. (pp 394-403).Google Scholar
  47. McDougald D, Rice SA & Kjelleberg S (1999) New perspectives on the viable but nonculturable response. Biologia 54: 617-623.Google Scholar
  48. McDougald, D Rice, SA & Kjelleberg S (2000) The marine pathogen, Vibrio vulnificus encodes a putative homologue of the Vibrio harveyi regulatory gene, luxR: a genetic and phylogenetic comparison. Gene 248: 213-221.PubMedCrossRefGoogle Scholar
  49. McDougald D, Rice SA & Kjelleberg S (2001) SmcR-dependent regulation of adaptive responses in Vibrio vulnificus. J. Bacteriol. 183: 758-762.PubMedCrossRefGoogle Scholar
  50. Moreno S, Guzmán J, Nájera R, Soberón-Chávez G & Espin G (1998) Role of the alternative σE factor AlgU in encystment of Azotobacter vinelandii. J. Bacteriol. 180: 2766-2769.PubMedGoogle Scholar
  51. Nitta T, Nagamitsu H, Murata M, Izu H & Yamada M (2000) Function of the σE regulon in dead-cell lysis in stationary-phase Escherichia coli. J. Bacteriol. 182: 5231-5237.PubMedCrossRefGoogle Scholar
  52. Nodwell JR & Losick R (1998). Purification of an extracellular signaling molecule involved in production of aerial mycelium by Streptomyces coelicolor. J. Bacteriol. 180: 1334-1337.PubMedGoogle Scholar
  53. Ochsner UA & Reiser J (1995) Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA. 96: 6424-6428.CrossRefGoogle Scholar
  54. Östling J, Holmquist L, Flärdh K, Svenblad B, Jouper-Jaan Å & Kjelleberg S (1993) Starvation and recovery of Vibrio. In: Kjelleberg S (Ed) Starvation in Bacteria, (pp 103-127). Plenum Press, New YorkGoogle Scholar
  55. Östling J, Flärdh K & Kjelleberg S (1995) Isolation of a carbon starvation regulatory mutant in a marine Vibrio strain. J. Bacteriol. 177: 6978-6982.PubMedGoogle Scholar
  56. Östling J, Holmquist L & Kjelleberg S (1996) Global analysis of the carbon starvation response of a marine Vibrio species with disruptions in genes homologous to relA and SpoT. J. Bacteriol. 178: 4901-4908.PubMedGoogle Scholar
  57. Rather PN, Ding X, Baca-DeLancey R R & Siddiqui S (1999) Providencia stuartii genes activated by cell-to-cell signaling and identification of a gene required for production or activity of an extracellular factor. J. Bacteriol. 181: 7185-7191.PubMedGoogle Scholar
  58. Santos JM, Freire P, Vicente M & Arraiano CM (1999) The stationary-phase morphogene bolA from Escherichia coli is induced by stress during early stages of growth. Mol. Microbiol. 32: 789-798.PubMedCrossRefGoogle Scholar
  59. Seyfzadeh M (1994) Regulation of ribosomal RNA synthesis in Escherichia coli by a novel guanosine tetraphosphate induction pathway. University of California, Irvine, CA.Google Scholar
  60. Seyfzadeh M, Keener J & Nomura M (1993) spoT-dependent accumulation of guanosine tetraphosphate in response to fatty acid starvation in Eschericia coli. Proc. Natl. Acad. Sci., USA 90: 11004-11008.PubMedCrossRefGoogle Scholar
  61. Shao C-P & Hor L-I (2001) Regulation of metalloprotease gene expression in Vibrio vulnificus by a Vibrio harveyi LuxR homologue. J. Bacteriol. 183: 1369-1375.PubMedCrossRefGoogle Scholar
  62. Spector MP (1998) The starvation-stress response (SSR) of Salmonella. Adv. Microbiol. Physiol. 40: 233-279.Google Scholar
  63. Srinivasan S & Kjelleberg S (1998) Cycles of famine and feast-the starvation and outgrowth strategies of a marine Vibrio. J. Biosciences 23: 501-511.CrossRefGoogle Scholar
  64. Srinivasan S & Kjelleberg S (2001) Signal-responsive carbon starvation genes of marine Vibrio angustum S14. In Annual Meeting of the American Society for Microbiology.Google Scholar
  65. Srinivasan S, Ostling J, Charlton T, de Nys R, Takayama K & Kjelleberg S (1998) Extracellular signal molecule(s) involved in the carbon starvation response of marine Vibrio sp. strain S14. J. Bacteriol. 180: 201-209.PubMedGoogle Scholar
  66. Surette MG, Miller MB & Bassler BL (1999). Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc. Natl. Acad. Sci., USA 96: 1639-1644.PubMedCrossRefGoogle Scholar
  67. Thorne SH & Williams HD (1999) Cell density-dependent starvation survival of Rhizobium leguminosarum bv. phaseoli: identification of the role of an N-acyl homoserine lactone in adaptation to stationary-phase survival. J. Bacteriol. 181: 981-990.PubMedGoogle Scholar
  68. Ward MJ, Lew H, Treuner-Lange A & Zusman DR (1998) Regulation of motility behavior in Myxococcus xanthus may require an extracytoplasmic-function sigma factor. J. Bacteriol. 180: 5668-5675.PubMedGoogle Scholar
  69. Whiteley M, Parsek MR & Greenberg EP (2000) Regulation of quorum sensing by RpoS in Pseudomonas aeruginosa. J. Bacteriol. 182: 4356-4360.PubMedCrossRefGoogle Scholar
  70. Xu KD, Stewart PS, Xia F, Huang C-T & McFeters GA (1998) Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl. Environ. Microbiol. 64: 4035-4039.PubMedGoogle Scholar
  71. You Z, Fukushima J, Tanaka K, Kawamoto S & Okuda K (1998) Induction of entry into stationary growth phase in Pseudomonas aeruginosa by N-acylhomoserine lactone. FEMS Microbiol. Lett. 164: 99-106.PubMedCrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Diane McDougald
    • 1
  • Lan Gong
    • 1
  • Sujatha Srinivasan
    • 1
  • Erika Hild
    • 1
  • Lyndal Thompson
    • 1
  • Kathy Takayama
    • 1
  • Scott A. Rice
    • 1
  • S. Kjelleberg
    • 1
  1. 1.School of Biotechnology and Biomolecular Sciences, Microbiology and Immunology and The Centre for Marine Biofouling and Bio-InnovationUniversity of New South WalesSydneyAustralia

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