Advertisement

Transcriptomic Responses of Bacterial Cells to Sublethal Metal Ion Stress

  • Jon L. HobmanEmail author
  • Kaneyoshi Yamamoto
  • Taku Oshima
Chapter
Part of the Microbiology Monographs book series (MICROMONO, volume 6)

Abstract

Bacterial cellular responses to metal ion stress are often measured as changes in transcription of genes involved in metal ion homeostasis, during detoxification processes or during functioning of efflux systems. Although there has been evidence for other bacterial cellular responses to metal ion stress, a view of what these responses are has been difficult to obtain. Recent measurements from genome-wide transcriptional profiling in bacteria strongly suggests that the effects of metals on cells may be very wide-ranging, and the transcriptomic responses equally wide. This chapter integrates the known biological effects of metal ion stress with data from microarray and other gene regulation studies from different bacteria responding to these stresses. Metal ion stresses elicit responses in metal ion homeostasis, oxidative stress responses, membrane stress responses, amino acid synthesis, and the expression of other metal ion import systems.

Keywords

Metal Stress Oxidative Stress Response Transcriptomic Response Soft Lewis Acid Envelope Stress Response 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Aertson A, Michiels CW (2004) Stress and how bacteria cope with death and survival. Crit Rev Mirobiol 30:263–273 Google Scholar
  2. 2.
    Aderem A (2005) Systems biology: Its practice and challenges. Cell 121:511–513 PubMedGoogle Scholar
  3. 3.
    Alba BM, Gross CA (2004) Regulation of the Escherichia coli sigma-dependent envelope stress response. Mol Microbiol 52:613–619 PubMedGoogle Scholar
  4. 4.
    Albanesi D, Mansilla MC, Schujman GE, de Mendoza D (2005) Bacillus subtilis cysteine synthetase is a global regulator of the expression of genes involved in sulfur assimilation. J Bacteriol 187:7631–7638 PubMedGoogle Scholar
  5. 5.
    Andrews SC, Robinson AK, and Rodriguez-Quinones F (2003) Bacterial ion homeostasis. FEMS Microbiol Rev 27:215-237 PubMedGoogle Scholar
  6. 6.
    Ballatori N (2002) Transport of toxic metals by molecular mimicry. Env Health Persp 110:689–694 Google Scholar
  7. 7.
    Beard SJ, Hashim R, Membrillo-Hernandez J, Hughes MN, Poole RK (1997) Zinc(II) tolerance in Escherichia coli K-12: evidence that the zntA gene (o732) encodes a cation transport ATPase. Mol Microbiol 25:883–91 PubMedGoogle Scholar
  8. 8.
    Bencheikh-Latmani R, Williams SM, Haucke L, Criddle CS, Wu L, Zhou J, Tebo BM (2005) Global transcriptional profiling of Shewanella oneidensis MR-1 during Cr(VI) and U(VI) reduction. Appl Environ Microbiol 71:7453–7460 PubMedGoogle Scholar
  9. 9.
    Binet MR, Poole RK (2000) Cd(II), Pb(II) and Zn(II) ions regulate expression of the metal-transporting P-type ATPase ZntA in Escherichia coli. FEBS Lett 473:67–70 PubMedGoogle Scholar
  10. 10.
    Blattner FR, Plunkett G, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997) The complete genome sequence of Escherichia coli K-12. Science 277:1453–146 PubMedGoogle Scholar
  11. 11.
    Boos W, Lucht JM (1996) Periplasmic binding protein-dependent ABC transporters. In: Niedhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Brooks Low K, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella cellular and molecular biology, 2nd edn. ASM, Washington, DC, pp 1175–1209 Google Scholar
  12. 12.
    Braun V, Mahren S, Ogierman M (2003) Regulation of the FecI-type ECF sigma factor by transmembrane signalling. Curr Opin Microbiol 6:173–180 PubMedGoogle Scholar
  13. 13.
    Braun V, Mahren S, Sauter A (2006) Gene regulation by transmembrane signalling. BioMetals 19:103–113 PubMedGoogle Scholar
  14. 14.
    Brocklehurst KR, Hobman JL, Lawley B, Blank L, Marshall SJ, Brown NL, Morby AP (1999) ZntR is a Zn(II)-responsive MerR-like transcriptional regulator of zntA in Escherichia coli. Mol Microbiol 31:893–902 PubMedGoogle Scholar
  15. 15.
    Brown NL, Stoyanov JV, Kidd SP, Hobman JL (2003) The MerR family of transcriptional regulators. FEMS Microbiol Rev 27:145–163 PubMedGoogle Scholar
  16. 16.
    Brown SD, Martin M, Deshpande S, Seal S, Huang K, Alm E, Yang Y, Wu L, Yan T, Liu X, Arkin A, Chourey K, Zhou J, Thompson DK (2006) Cellular response of Shewanella oneidensis to strontium stress. Appl Environ Microbiol 72:890–900 PubMedGoogle Scholar
  17. 17.
    Browning DF, Busby SJW (2004) The regulation of bacterial transcription initiation. Nat Rev Microbiol 2:1–9 Google Scholar
  18. 18.
    Bruins MR, Kapil S, Oehme FW (2000). Microbial resistance to metals in the environment. Ecotoxicol Environ Safety 45:198–207 PubMedGoogle Scholar
  19. 19.
    Brutsche S, Braun V (1997) SigX of Bacillus subtilis replaces the ECF sigma factor fecI of Escherichia coli and is inhibited by RsiX. Mol Gen Genet 256:416–425 PubMedGoogle Scholar
  20. 20.
    Busenlehner LS, Pennella MA, Giedroc DP (2003) The SmtB/ArsR family of metalloregulatory transcriptional repressors: structural insights into prokaryotic metal resistance. FEMS Microbiol Rev 27:131–143 PubMedGoogle Scholar
  21. 21.
    Carlin A, Shi W, Dey S, Rosen BP (1995) The ars operon of Escherichia coli confers arsenical and antimonial resistance. J Bacteriol 177:981–6 PubMedGoogle Scholar
  22. 22.
    Changela A, Chen K, Xue Y, Holschen J, Outten CE, O'Halloran TV, Mondragon A (2003) Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301:1383–1387 PubMedGoogle Scholar
  23. 23.
    Coombs JM, Barkay T (2004) Molecular evidence for the evolution of metal homeostasis genes by lateral gene transfer in bacteria from the deep terrestrial subsurface. Appl Environ Microbiol 70:1698–1707 PubMedGoogle Scholar
  24. 24.
    Coombs JM, Barkay T (2005) New findings on evolution of metal homeostasis genes: evidence from comparative genome analysis of bacteria and archaea. Appl Environ Microbiol 71:7083–7091 PubMedGoogle Scholar
  25. 25.
    Csonka LN, Epstein W (1996) Osmoregulation. In: Niedhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Brooks Low K, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella cellular and molecular biology, 2nd edn. ASM, Washington, DC, pp 1210–1223 Google Scholar
  26. 26.
    Dartigalongue C, Missiakas D, Raina S (2001) Characterization of the Escherichia coli sigma E regulon. J Biol Chem 276:20866–20875 PubMedGoogle Scholar
  27. 27.
    Danese PN, Silhavy TJ (1998) CpxP, a stress-combative member of the Cpx regulon. J Bacteriol 180:831–839 PubMedGoogle Scholar
  28. 28.
    Demple B (1996) Redox signalling and gene control in the Escherichia coli soxRS oxidative stress regulon- a review. Gene 179:53–57 PubMedGoogle Scholar
  29. 29.
    De Wulf P, McGuire AM, Liu X, Lin ECC (2002) Genome-wide profiling of promoter recognition by the two-component response regulator CpxR-P in Escherichia coli. J Biol Chem 277:26652–26661 PubMedGoogle Scholar
  30. 30.
    Dorel C, Lejeune P, Rodrigue A (2006) The Cpx system of Escherichia coli, a strategic signalling pathway for confronting adverse conditions and for settling biofilm communities? Res Microbiol 157:306–314 PubMedGoogle Scholar
  31. 31.
    Duffus JH (2002) “Heavy metals”-A meaningless term? Pure Appl Chem 74:793–807 Google Scholar
  32. 32.
    Earhart CF (1996) Uptake and metabolism of iron and molybdenum. In: Niedhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Brooks Low K, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella cellular and molecular biology, 2nd edn. ASM, Washington, DC, pp 1075–1090 Google Scholar
  33. 33.
    Egler M, Grosse C, Grass G, Nies DH (2005) Role of the extracytoplasmic function protein family sigma factor RpoE in metal resistance of Escherichia coli. J Bacteriol 187:2297–2307 PubMedGoogle Scholar
  34. 34.
    Eguchi Y, Okada T, Minagawa S, Oshima T, Mori H, Yamamoto K, Ishihama A, Utsumi R (2004) A signal transduction cascade between EvgA/EvgS and PhoP/PhoQ two-component systems of Escherichia coli. J Bacteriol 186:3006–3014 PubMedGoogle Scholar
  35. 35.
    Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress Part I: Mechanisms involved in metal induced oxidative damage. Curr Top Med Chem 1:529–539 PubMedGoogle Scholar
  36. 36.
    Forman SJ, Kumar KS, Redeker AG, Hochstein P (1980) Hemolytic anaemia in Wilson's disease: clinical findings and biochemical mechanism. Am J Hematol 9:269–276 PubMedGoogle Scholar
  37. 37.
    Franke S, Grass G, Nies DH (2001) The product of the ybdE gene of the Escherichia coli chromosome is involved in detoxification of silver ions. Microbiology 147:965–972 PubMedGoogle Scholar
  38. 38.
    Gaetke LM, Chow CK (2003) Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology 189:147–163 PubMedGoogle Scholar
  39. 39.
    Galperin MY (2006) Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188:4169–4182 PubMedGoogle Scholar
  40. 40.
    Geslin C, Llanos J, Prieur D, Jeanthon C (2001) The manganese and iron superoxide dismutases protect Escherichia coli from heavy metal toxicity. Res Microbiol 152:901–905 PubMedGoogle Scholar
  41. 41.
    Grainger DC, Hurd D, Harrison M, Holdstock J, Busby SJ (2005) Studies of the distribution of Escherichia coli cAMP-receptor protein and RNA polymerase along the E. coli chromosome. Proc Natl Acad Sci USA 102:17693–17698 PubMedGoogle Scholar
  42. 42.
    Grainger DC, Overton TW, Hobman JL, Constantinidou C, Tamai E, Wade JT, Struhl K, Reppas N, Church G, Busby SJW (2004) Genomic studies with Escherichia coli MelR protein: applications of chromatin immunoprecipitation and microarrays. J Bacteriol 186:6938–6943 PubMedGoogle Scholar
  43. 43.
    Grass G, Franke S, Taudte N, Nies DH, Kucharski LM, Maguire ME, Rensing C (2005) The metal permease ZupT from Escherichia coli is a transporter with a broad substrate spectrum. J Bacteriol 187:1604–1611 PubMedGoogle Scholar
  44. 44.
    Grass G, Fan B, Rosen BP, Franke S, Nies DH, Rensing C (2001) ZitB (YbgR), a member of the cation diffusion facilitator family, is an additional zinc transporter in Escherichia coli. J Bacteriol 183:4664–4667 PubMedGoogle Scholar
  45. 45.
    Grass G, Fricke B, Nies DH (2005) Control of expression of a periplasmic nickel efflux pump by periplasmic nickel concentrations. Biometals 18:437–448 PubMedGoogle Scholar
  46. 46.
    Grass G, Wong MD, Rosen BP, Smith RL, Rensing C (2002) ZupT is a Zn(II) uptake system in Escherichia coli. J Bacteriol 184:864–866 PubMedGoogle Scholar
  47. 47.
    Griffith KL, Shah IM, Wolf RE Jr (2004) Proteolytic degradation of Escherichia coli transcription activators SoxS and MarA as the mechanism for reversing the induction of the superoxide (SoxRS) and multiple antibiotic resistance (Mar) regulons. Mol Microbiol 51:1801–1816 PubMedGoogle Scholar
  48. 48.
    Groisman EA (2001) The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183:1835–1842 PubMedGoogle Scholar
  49. 49.
    Grunden AM, Shanmugam KT (1997) Molybdate transport and regulation in bacteria. Arch Microbiol 168:345–354 PubMedGoogle Scholar
  50. 50.
    Gupta A, Matsui K, Lo JF, Silver S (1999) Molecular basis for resistance to silver cations in Salmonella. Nature Med 5:183–188 PubMedGoogle Scholar
  51. 51.
    Gyaneshwar P, Paliy O, McAuliffe J, Popham DL, Jordan MI, Kustu S (2005) Sulfur and nitrogen limitation in Escherichia coli K-12: specific homeostatic responses. J Bacteriol 187:1074–1090 PubMedGoogle Scholar
  52. 52.
    Hagiwara D, Sugiura M, Oshima T, Mori H, Aiba H, Yamashino T, Mizuno T (2003) Genome-wide analyses revealing a signaling network of the RcsC-YojN-RcsB phosphorelay system in Escherichia coli. J Bacteriol 185:5735-46 PubMedGoogle Scholar
  53. 53.
    Hagiwara D, Yamashino T, Mizuno T (2004) A genome-wide view of the Escherichia coli BasS-BasR two-component system implicated in iron-responses. Biosci Biotechnol Biochem 68:1758–1767 PubMedGoogle Scholar
  54. 54.
    Hantke K (2001) Iron and metal regulation in bacteria. Curr Opin Microbiol 4:172–177 PubMedGoogle Scholar
  55. 55.
    Hansen JM, Zhang H, Jones DP (2006) Differential oxidation of thiredoxin-1, thioredoxin-2, and glutathione by metal ions. Free Radical Biol Med 40:138–145 Google Scholar
  56. 56.
    Harrison JJ, Ceri H, Roper NJ, Badry EA, Sproule KM, Turner RJ (2005) Persister cells mediate tolerance to metal oxyanions in Escherichia coli. Microbiology 151:3181–3195 PubMedGoogle Scholar
  57. 57.
    Hayashi K, Morooka N, Yamamoto Y, Choi S, Ohtsubo E, Baba T, Wanner BL, Mori H, Horiuchi T (2006) Highly accurate genome sequences of the Escherichia coli K-12 strains MG1655 and W3110. Mol Syst Biol 2:E1–E5 Google Scholar
  58. 58.
    Helmann JD (2002) The extracytoplasmic function (ECF) sigma factors. Adv Microb Physiol 46:47–110 PubMedGoogle Scholar
  59. 59.
    Herring CD, Raffaelle M, Allen TE, Kanin EI, Landick R, Ansari AZ, Palsson BO (2005) Immobilization of Escherichia coli RNA polymerase and location of binding sites by use of chromatin immunoprecipitation and microarrays. J Bacteriol 187:6166–6174 PubMedGoogle Scholar
  60. 60.
    Hidalgo E, Bollinger JM Jr, Bradley TM, Walsh CT, Demple B (1995) Binuclear [2Fe-2S] clusters in the Escherichia coli SoxR protein and role of the metal centers in transcription. J Biol Chem 270:20908–20914 PubMedGoogle Scholar
  61. 61.
    Hirakawa H, Inazumi Y, Masaki T, Hirata T, Yamaguchi A (2005) Indole induces the expression of multidrug exporter genes in Escherichia coli. Mol Microbiol 55:1113–26 PubMedGoogle Scholar
  62. 62.
    Hobman JL (2007) Molecular techniques for the study of toxic metal resistance mechanisms in bacteria. In: Crawford RL (ed) Manual of environmental microbiology, 3rd edn. ASM, Washington, DC (in press) Google Scholar
  63. 63.
    Hobman JL, Jones AC, and Constantinidou C (2007) An introduction to microarray technology. In: Falciani F (ed) Microarray technology. Taylor and Francis, Oxford (in press) Google Scholar
  64. 64.
    Hobman JL, Wilkie J, Brown NL (2005) A design for life: prokaryotic metal-binding MerR family regulators. Biometals 18:429–436 PubMedGoogle Scholar
  65. 65.
    Hu P, Brodie EL, Suzuki Y, McAdams HH, Anderson GL (2005) Whole-genome transcriptional analysis of heavy metal stress in Caulobacter crescentus. J Bacteriol 187:8437–8449 PubMedGoogle Scholar
  66. 66.
    Hughes MN, Poole RK (1989) Metals and microorganisms. Chapman and Hall, London Google Scholar
  67. 67.
    Hultberg B, Andersson A, Isaksson A (2001) Interaction of metals and thiols in cell damage and glutathione distribution: potentiation of mercury toxicity by dithiothreitol. Toxicology 156:93–100 PubMedGoogle Scholar
  68. 68.
    Imlay JA (2003) Pathways of oxidative damage. Ann Rev Microbiol 57:395–418 Google Scholar
  69. 69.
    Imlay JA (2006) Iron-sulphur clusters and the problem with oxygen. Mol Microbiol 59:1073–1082 PubMedGoogle Scholar
  70. 70.
    Kabir MS, Yamashita D, Koyama S, Oshima T, Kurokawa K, Maeda M, Tsunedomi R, Murata M, Wada C, Mori H, Yamada M (2005) Cell lysis directed by σEin early stationary phase and effect of induction of the rpoE gene on global gene expression in Escherichia coli. Microbiology 151:2721–2735 PubMedGoogle Scholar
  71. 71.
    Kasprzak KS (2002) Oxidative DNA and protein damage in metal-induced toxicity and carcinogenesis. Free Radical Biol Med 32:958–967 Google Scholar
  72. 72.
    Kato A, Tanabe H, Utsumi R (1999) Molecular characterization of the PhoP-PhoQ two-component system in Escherichia coli K-12: identification of extracellular Mg2+-responsive promoters. J Bacteriol 181:5516–5520 PubMedGoogle Scholar
  73. 73.
    Kaur A, Pan M, Meislin M, Facciotti MT, El-Geweley R, Baliga NS (2006) A systems view of haloarchaeal strategies to withstand stress from transition metals. Genome Res 16:841–854 PubMedGoogle Scholar
  74. 74.
    Kershaw CJ, Brown NL, Constantinidou C, Patel MD, Hobman JL (2005) The expression profile of Escherichia coli K-12 in response to minimal, optimal and excess copper concentrations. Microbiology 151:1187–1198 PubMedGoogle Scholar
  75. 75.
    Kimura T, Nishioka H (1997) Intracellular generation of superoxide by copper sulphate in Escherichia coli. Mutat Res 389:237–242 PubMedGoogle Scholar
  76. 76.
    Kredich NM (1996) Biosynthesis of cystine. In: Niedhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Brooks Low K, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella cellular and molecular biology, 2nd edn. ASM, Washington, DC, pp 514–527 Google Scholar
  77. 77.
    Lee JW, Helmann JD (2006) The PerR transcription factor senses H2O2by metal-catalysed histidine oxidation. Nature 440:363–367 PubMedGoogle Scholar
  78. 78.
    Lee LJ, Barrett JA, Poole RK (2005) Genome-wide transcriptional response of chemostat-cultured Escherichia coli to zinc. J Bacteriol 187:1124–1134 PubMedGoogle Scholar
  79. 79.
    Leonhartsberger S, Huber A, Lottspeich F, Bock A (2001) The hydH/G Genes from Escherichia coli code for a zinc and lead responsive two-component regulatory system. J Mol Biol 307:93–105 PubMedGoogle Scholar
  80. 80.
    Li Y, Wray R, Blount P (2004) Intragenic suppression of gain-of-function mutations in the Escherichia coli mechanosensitive channel, MscL. Mol Microbiol 53:485–495 PubMedGoogle Scholar
  81. 81.
    Lippard SJ, Berg JM (1994) Overview of bioinorganic chemistry. In: Principles of bioinorganic chemistry. University Science Books, Mill Valley, California, pp 1–19 Google Scholar
  82. 82.
    Lippard SJ, Berg JM (1994) Control and utilization of metal-ion concentration in cells. In: Principles of bioinorganic chemistry. University Science Books, Mill Valley, California, pp 139–173 Google Scholar
  83. 83.
    Makui H, Roig E, Cole ST, Helmann JD, Gros P, Cellier MF (2000) Identification of the Escherichia coli K-12 Nramp orthologue (MntH) as a selective divalent metal ion transporter. Mol Microbiol 35:1065–1078 PubMedGoogle Scholar
  84. 84.
    Marina A, Mott C, Auyzenberg A, Hendrickson WA, Waldburger CD (2001) Structural and mutational analysis of the PhoQ histidine kinase catalytic domain. Insight into the reaction mechanism. J Biol Chem 276:41182–41190 PubMedGoogle Scholar
  85. 85.
    Martin RG, Rosner JL (2002) Genomics of the marA/soxS/rob regulon of Escherichia coli: identification of directly activated promoters by application of molecular genetics and informatics to microarray data. Mol Microbiol 44:1611–1624 PubMedGoogle Scholar
  86. 86.
    Martinez RJ, Wang Y, Raimondo MA, Coombs JM, Barkay T, Sobecky PA (2006) Horizontal transfer of PIB-type ATPases among bacteria isolated from radionuclide- and metal-contaminated subsurface soils. Appl Environ Microbiol, pp 3111–3118 Google Scholar
  87. 87.
    Mattie MD, Freedman JH (2004) Copper-inducible transcription: regulation by metal- and oxidative stress-responsive pathways. Am J Physiol Cell Physiol 286:C293–C301 PubMedGoogle Scholar
  88. 88.
    McHugh JP, Rodriguez-Quinones F, Abdul-Tehrani H, Svistunenko DA, Poole RK, Cooper CE, Andrews SC (2003) Global iron-dependent gene regulation in Escherichia coli. A new mechanism for iron homeostasis. J Biol Chem 278:29478–29486 PubMedGoogle Scholar
  89. 89.
    Mergeay M, Monchy S, Vallaeys T, Auquier V, Benotmane A, Bertin P, Taghavi S, Dunn J, van der Lelie D, Wattiez R (2003) Ralstonia metallidurans, a bacterium specially adapted to toxic metals: towards a catalogue of metal-responsive genes. FEMS Microbiol Rev 27:385–410 PubMedGoogle Scholar
  90. 90.
    Mergeay M, Nies D, Schlegel HG, Gerits J, Charles P, van Gijsegem F (1985) Alcalignes eutrophus is a Gram-negative facultative chemolithotroph with plasmid-bound resistance to heavy metals. J Bacteriol 162:328–334 PubMedGoogle Scholar
  91. 91.
    Minagawa S, Ogasawara H, Kato A, Yamamoto K, Eguchi Y, Oshima T, Mori H, Ishihama A, Utsumi R (2003) Identification and molecular characterization of the Mg2+stimulon of Escherichia coli. J Bacteriol 185:3696–3702 PubMedGoogle Scholar
  92. 92.
    Minagawa S, Okura R, Tsuchitani H, Hirao K, Yamamoto K, Utsumi R (2005) Isolation and molecular characterization of the locked-on mutant of Mg2+sensor PhoQ in Escherichia coli. Biosci Biotechnol Biochem 69:1281–1287 PubMedGoogle Scholar
  93. 93.
    Miyadai H, Tanaka-Masuda K, Matsuyama S, Tokuda H (2004) Effects of lipoprotein overproduction on the induction of DegP (HtrA) involved in quality control in the Escherichia coli periplasm. J Biol Chem 279:39807–39813 PubMedGoogle Scholar
  94. 94.
    Monchy S, Benotmane MA, Wattiez R, van Aelst S, Auquier V, Borremans B, Mergeay M, Taghavi S, van der Lelie D, Vallaeys T (2006) Transcriptomic and proteomic analyses of the pMOL30-encoded copper resistance in Cupriavidus metallidurans strain CH34. Microbiology 152:1765–1776 PubMedGoogle Scholar
  95. 95.
    Moore CM, Gaballa A, Hui M, Ye RW, Helmann JD (2005) Genetic and physiological responses of Bacillus subtilis to metal ion stress. Mol Microbiol 57:27–40 PubMedGoogle Scholar
  96. 96.
    Moore CM, Helmann JD (2005) Metal ion homeostasis in Bacillus subtilis. Curr Opin Microbiol 8:188–195 PubMedGoogle Scholar
  97. 97.
    Munson GP, Lam DL, Outten FW, O'Halloran TV (2000) Identification of a copper-responsive two-component system on the chromosome of Escherichia coli K-12. J Bacteriol 182:5864–5871 PubMedGoogle Scholar
  98. 98.
    Nieboer E, Richardson DHS (1980) The replacement of the nondescript term “heavy metals” by a biologically and chemically significant classification of metal ions. Env Poll (Ser B) 1:3–26 Google Scholar
  99. 99.
    Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750 PubMedGoogle Scholar
  100. 100.
    Nies DH (2004) Incidence and function of sigma factors in Ralstonia metallidurans and other bacteria. Arch Microbiol 181:255–268 PubMedGoogle Scholar
  101. 101.
    Nies DH, Brown NL (1998) Two-component systems in the regulation of heavy metal resistance. In: Silver S, Walden W (eds) Metal ions in gene regulation. Chapman Hall, London, pp 77–103 Google Scholar
  102. 102.
    Nies DH, Rehbein G, Hoffmann T, Baumann C, Grosse C (2006) Paralogs of genes encoding metal resistance proteins in Cupriavidus metallidurans strain CH34. J Mol Micro Biotechnol 11:82–93 Google Scholar
  103. 103.
    Nies DH, Silver S (1995) Ion efflux systems involved in bacterial metal resistances. J Indust Microbiol 14:186–199 Google Scholar
  104. 104.
    Onufryk C, Crouch ML, Fang FC, Gross CA (2005) Characterization of six lipoproteins in the σE regulon. J Bacteriol 187:4552–4561 PubMedGoogle Scholar
  105. 105.
    Oshima T, Aiba H, Masuda Y, Kanaya S, Sugiura M, Wanner BL, Mori H, Mizuno T (2002) Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli K-12. Mol Microbiol 46:281–291 PubMedGoogle Scholar
  106. 106.
    Outten CE, O'Halloran TV (2001) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292:2488–2492 PubMedGoogle Scholar
  107. 107.
    Outten CE, Outten FW, O'Halloran TV (1999) DNA distortion mechanism for transcriptional activation by ZntR, a Zn(II)-responsive MerR homologue in Escherichia coli. J Biol Chem 274:37517–37524 PubMedGoogle Scholar
  108. 108.
    Outten CE, Tobin DA, Penner-Hahn JE, O'Halloran TV (2001) Characterization of the metal receptor sites in Escherichia coli Zur, an ultrasensitive zinc(II) metalloregulatory protein. Biochemistry 40:10417–10423 PubMedGoogle Scholar
  109. 109.
    Outten FW, Huffman DL, Hale JA, O'Halloran TV (2001) The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J Biol Chem 276:30670–30677 PubMedGoogle Scholar
  110. 110.
    Outten FW, Outten CE, Hale JA, O'Halloran TV (2000) Transcriptional activation of an Escherichia coli copper efflux regulation by the chromosomal MerR homologue, CueR. J Biol Chem 275:31024–31029 PubMedGoogle Scholar
  111. 111.
    Patzer SI, Hantke K (1998) The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol Microbiol 28:1199–210 PubMedGoogle Scholar
  112. 112.
    Patzer SI, Hantke K (2001) Dual repression by Fe2+-Fur and Mn2+-MntR of the mntH gene, encoding an NRAMP-like Mn2+transporter in Escherichia coli. J Bacteriol 183:4806–4813 PubMedGoogle Scholar
  113. 113.
    Pearson RG (1963) Hard and soft acids and bases. J Am Chem Soc 85:3533–3539 Google Scholar
  114. 114.
    Pennella MA, Giedroc DP (2005) Structural determinants of metal selectivity in prokaryotic metal-responsive transcriptional regulators. Biometals 18:413–428 PubMedGoogle Scholar
  115. 115.
    Permina EA, Kazakov AE, Kalinina OV, Gelfand MS (2006) Comparative genomics of regulation of heavy metal resistance in eubacteria. BMC Microbiol 6:49 PubMedGoogle Scholar
  116. 116.
    Pomposiello PJ, Bennik MH, Demple B (2001) Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. J Bacteriol 183:3890–3902 PubMedGoogle Scholar
  117. 117.
    Pomposiello PJ, Demple B (2001) Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol 19:109–114 PubMedGoogle Scholar
  118. 118.
    Powell SR (2000) The antioxidant properties of zinc. J Nutr 130:1447S-1454S Google Scholar
  119. 119.
    Raivio TL (2005) Envelope stress responses and Gram-negative bacterial pathogenesis. Mol Microbiol 56:1119–28 PubMedGoogle Scholar
  120. 120.
    Raivio TL, Silhavy TJ (2001) Periplasmic stress and ECF sigma factors. Ann Rev Microbiol 55:591–624 Google Scholar
  121. 121.
    Regelmann AG, Lesley JA, Mott C, Stokes L, Waldburger CD (2002) Mutational analysis of the Escherichia coli PhoQ sensor kinase: differences with the Salmonella enterica serovar Typhimurium PhoQ protein and in the mechanism of Mg2+and Ca2+sensing. J Bacteriol 184:5468–5478 PubMedGoogle Scholar
  122. 122.
    Rensing C, Grass G (2003) Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27:197–213 PubMedGoogle Scholar
  123. 123.
    Rensing C, Mitra B, Rosen BP (1997) The zntA gene of Escherichia coli encodes a Zn(II)-translocating P-type ATPase. Proc Natl Acad Sci USA 94:14326–14331 PubMedGoogle Scholar
  124. 124.
    Rhodius VA, LaRossa RA (2003) Uses and pitfalls of microarrays for studying transcriptional regulation. Curr Opin Microbiol 6:114–119 PubMedGoogle Scholar
  125. 125.
    Riley M, Abe T, Arnaud MB, Berlyn MKB, Blattner FR, Chaudhuri RR, Glasner JD, Horiuchi T, Keseler IM, Kosuge T, Mori H, Perna NT, Plunkett III G, Rudd KE, Serres MH, Thomas GH, Thomson NR, Wishart D, Wanner BL (2006) Escherichia coli K-12: a cooperatively developed annotation snapshot—2005. Nucleic Acids Res 34:1–9 PubMedGoogle Scholar
  126. 126.
    Rodrigue A, Effantin G, Mandrand-Berthelot MA (2005) Identification of rcnA (yohM), a nickel and cobalt resistance gene in Escherichia coli. J Bacteriol 187:2912–2916 PubMedGoogle Scholar
  127. 127.
    Rouch DA, Lee BTO, Morby AP (1995) Understanding cellular responses to toxic agents: a model for mechanism-choice in bacterial metal resistance. J Ind Microbiol 14:132–141 PubMedGoogle Scholar
  128. 128.
    Ruiz N, Falcone B, Kahne D, Silhavy TJ (2005) Chemical conditionality: a genetic strategy to probe organelle assembly. Cell 121:307–317 PubMedGoogle Scholar
  129. 129.
    Ruiz N, Kahne D, Silhavy TJ (2006) Advances in understanding bacterial outer-membrane biogenesis. Nat Rev Microbiol 4:57–66 PubMedGoogle Scholar
  130. 130.
    Ruiz N, Silhavy TJ (2005) Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr Opin Microbiol 8:122–126 PubMedGoogle Scholar
  131. 131.
    Sato T, Kobayashi Y (1998) The ars operon in the skin element of Bacillus subtilis confers resistance to arsenate and arsnite. J Bacteriol 180:1655–1661 PubMedGoogle Scholar
  132. 132.
    Shah IM, Wolf RE Jr (2006) Inhibition of Lon-dependent degradation of the Escherichia coli transcription activator SoxS by interaction with “soxbox” DNA or RNA polymerase. Mol Microbiol 60:199–208 PubMedGoogle Scholar
  133. 133.
    Shi H, Hudson LG, Liu KJ (2004) Oxidative stress and apoptosis in metal ion-induced carcinogenesis. Free Radical Biol Med 37:582–593 Google Scholar
  134. 134.
    Shijuku T, Yamashino T, Ohashi H, Saito H, Kakegawa T, Ohta M, Kobayashi H (2002) Expression of chaA, a sodium ion extrusion system of Escherichia coli, is regulated by osmolarity and pH. Biochim Biophys Acta 1556:142–148 PubMedGoogle Scholar
  135. 135.
    Silver S (1996) Transport of inorganic cations. In: Niedhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Brooks Low K, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella Cellular and molecular biology, 2nd edn. ASM, Washington, DC, pp 1091–1102 Google Scholar
  136. 136.
    Silver S, Phung LT (2005) A bacterial view of the Periodic Table: genes and proteins for toxic inorganic ions. J Industr Microbiol Biotechnol 32:587–605 Google Scholar
  137. 137.
    Skovierova H, Rowley G, Rezuchova B, Homerova D, Lewis C, Roberts M, Kormanec J (2006) Identification of the σEregulon of Salmonella enterica serovar Typhimurium. Microbiology 152:1347–1359 PubMedGoogle Scholar
  138. 138.
    Snyder WB, Davis LJ, Danese PN, Cosma CL, Silhavy TJ (1995) Overproduction of NlpE, a new outer membrane lipoprotein, suppresses the toxicity of periplasmic LacZ by activation of the Cpx signal transduction pathway. J Bacteriol 177:4216–4223 PubMedGoogle Scholar
  139. 139.
    Solioz M, Stoyanov JV (2003) Copper homeostasis in Enterococcus hirae. FEMS Microbiol Rev 27:183–195 PubMedGoogle Scholar
  140. 140.
    Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radical Biol Med 18:321–336 Google Scholar
  141. 141.
    Storz G, Hengge-Aronis R (2004) Bacterial stress responses. ASM, Washington Google Scholar
  142. 142.
    Stoyanov JV, Hobman JL, Brown NL (2001) CueR, (ybbI) of Escherichia coli is a MerR family regulator controlling expression of the copper exporter CopA. Mol Microbiol 39:502–511 PubMedGoogle Scholar
  143. 143.
    Twyman RM (2004) From genomics to proteomics. In: Principles of proteomics. Bios Scientific, Oxford, pp 1–22 Google Scholar
  144. 144.
    Ueda J-I, Takai M, Shimazu Y, Ozawa T (1998) Reactive oxygen species generated from the reaction of copper (II) complexes with biological reductants cause DNA strand scission. Arch Biochem Biophys 357:231–239 PubMedGoogle Scholar
  145. 145.
    Van der Lelie D, Schwuchow T, Schwidetzky U, Wuertz S, Baeyens W, Mergeay M, Nies DH (1997) Two-component regulatory system involved in transcriptional control of heavy-metal homeostasis in Alcaligenes eutrophus. Mol Microbiol 23:493–503 PubMedGoogle Scholar
  146. 146.
    Vescovi EG, Ayala YM, Di Cera E, Groisman EA (1997) Characterization of the bacterial sensor protein PhoQ. Evidence for distinct binding sites for Mg2+and Ca2+. J Biol Chem 272:1440–1443 PubMedGoogle Scholar
  147. 147.
    Wackett LP, Dodge AG, Ellis LBM (2004) Microbial genomics and the Periodic Table. Appl Environ Microbiol 70:647–655 PubMedGoogle Scholar
  148. 148.
    Wade JT, Struhl K (2004) Association of RNA polymerase with transcribed regions in Escherichi coli. Proc Natl Acad Sci USA 101:17777–17782 PubMedGoogle Scholar
  149. 149.
    Waldburger CD, Sauer RT (1996) Signal detection by the PhoQ sensor-transmitter. Characterization of the sensor domain and a response-impaired mutant that identifies ligand-binding determinants. J Biol Chem 271:26630–26636 PubMedGoogle Scholar
  150. 150.
    Wang A, Crowley DE (2005) Global gene expression responses to cadmium toxicity in Escherichia coli. J Bacteriol 187:3259–3266 PubMedGoogle Scholar
  151. 151.
    Wolanin PM, Thomason PA, Stock JB (2002) Histidine protein kinases: key signal transducers outside the animal kingdom. Genome Biology 3: reviews 3013.1–3013.8 Google Scholar
  152. 152.
    Yamamoto K, Ishihama A (2005) Transcriptional response of Escherichia coli to external zinc. J Bacteriol 187:6333–6340 PubMedGoogle Scholar
  153. 153.
    Yamamoto K, Ishihama A (2005) Transcriptional response of Escherichia coli to external copper. Mol Microbiol 56:215–227 PubMedGoogle Scholar
  154. 154.
    Yamamoto K, Ishihama A (2006) Characterization of copper-inducible promoters regulated by CpxA/CpxR in Escherichia coli. Biosci Biotechnol Biochem 70:1688–1695 PubMedGoogle Scholar
  155. 155.
    Yamamoto K, Ogasawara H, Fujita N, Utsumi R, Ishihama A (2002) Novel mode of transcription regulation of divergently overlapping promoters by PhoP, the regulator of two-component system sensing external magnesium availability. Mol Microbiol 45:423–438 PubMedGoogle Scholar
  156. 156.
    Zheng M, Doan B, Schneider TD, Storz G (1999) OxyR and SoxRS regulation of fur. J Bacteriol 181:4639–4643 PubMedGoogle Scholar
  157. 157.
    Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA, Storz G (2001) DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183:4562–4570 PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2007

Authors and Affiliations

  • Jon L. Hobman
    • 1
    Email author
  • Kaneyoshi Yamamoto
    • 2
  • Taku Oshima
    • 3
  1. 1.School of BiosciencesThe University of BirminghamBirminghamUK
  2. 2.Department of Advanced BioscienceKinki UniversityNaraJapan
  3. 3.Department of Bioinformatics and GenomicsGraduate School of Information Science, Nara Institute of Science and TechnologyNaraJapan

Personalised recommendations