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Understanding How Cells Allocate Metals

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Molecular Microbiology of Heavy Metals

Part of the book series: Microbiology Monographs ((MICROMONO,volume 6))

Abstract

Life depends upon multiple metals. It is estimated that approximately one-third of all gene products require a metal for folding and/or catalysis. How does the correct metal locate to the correct protein? Provision of sufficient atoms of each of the metals required by protein metal-binding sites is a challenge for cell biology. This is often especially true for iron, which is poorly soluble under aerobic conditions. Protein metal-binding sites follow universal affinity series. Under such a regime, exclusion of the wrong metals from metalloproteins is arguably an even greater challenge. High-fidelity homeostasis must match the number of some metal cations to the number of bonafide metal-binding sites. Selective protein–protein interactions also limit access of some atoms to the required subsets of proteins. Here we provide an overview of the contributions of metal sensors, metallochaperones, metal transporters and metal-storage proteins to the allocation of metals in cells. In this chapter an emphasis is placed on studies of the cell biology of metals in cyanobacteria.

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References

  1. Abdel-Ghany SE, Muller-Moule P, Niyogi KK, Pilon M, Shikanai T (2005) Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17:1233–1251

    Article  PubMed  CAS  Google Scholar 

  2. Akerlund T, Nordstrom K, Bernander R (1995) Analysis of cell size and DNA content in exponentially growing and stationary-phase batch cultures of Escherichia coli. J Bacteriol 177:6791–6797

    PubMed  CAS  Google Scholar 

  3. Atanassova A, Zamble DB (2005) Escherichia coli HypA is a zinc metalloprotein with a weak affinity for nickel. J Bacteriol 187:4689–4697

    Article  PubMed  CAS  Google Scholar 

  4. Bairoch A (1993) A possible mechanism for metal-ion induced DNA-protein dissociation in a family of prokaryotic transcriptional regulators. Nucleic Acids Res 21:2515

    Article  PubMed  CAS  Google Scholar 

  5. Banci L, Bertini I, Del Conte R (2003) Solution structure of apo CopZ from Bacillus subtilis: further analysis of the changes associated with the presence of copper. Biochemistry 42:13422–13428

    Article  PubMed  CAS  Google Scholar 

  6. Banci L, Bertini I, Ciofi-Baffoni S, Su XC, Borrelly GP, Robinson NJ (2004) Solution structures of a cyanobacterial metallochaperone: insight into an atypical copper-binding motif. J Biol Chem 279:27502–27510

    Article  PubMed  CAS  Google Scholar 

  7. Banci L, Bertini I, Ciofi-Baffoni S, Kandias NG, Robinson NJ, Spyroulias GA, Su XC, Tottey S, Vanarotti M (2006) The delivery of copper for thylakoid import observed by NMR. Proc Natl Acad Sci USA 103:8320–8325

    Article  PubMed  CAS  Google Scholar 

  8. Banerjee S, Wei B, Bhattacharyya-Pakrasi M, Pakrasi HB, Smith TJ (2003) Structural determinants of metal specificity in the zinc transport protein ZnuA from Synechocystis 6803. J Mol Biol 333:1061–1069

    Article  PubMed  CAS  Google Scholar 

  9. Bartsevich VV, Pakrasi HB (1995) Molecular identification of an ABC transporter complex for manganese: analysis of a cyanobacterial mutant strain impaired in the photosynthetic oxygen evolution process. EMBO J 14:1845–1853

    PubMed  CAS  Google Scholar 

  10. Blindauer CA, Harrison MD, Parkinson JA, Robinson AK, Cavet JS, Robinson NJ, Sadler PJ (2001) A metallothionein containing a zinc finger within a four-metal cluster protects a bacterium from zinc toxicity. Proc Natl Acad Sci USA 98:9593–9598

    Article  PubMed  CAS  Google Scholar 

  11. Blindauer CA, Harrison MD, Robinson AK, Parkinson JA, Bowness PW, Sadler PJ, Robinson NJ (2002) Multiple bacteria encode metallothioneins and SmtA-like zinc fingers. Mol Microbiol 45:1421–1432

    Article  PubMed  CAS  Google Scholar 

  12. Blindauer CA, Polfer NC, Keiper SE, Harrison MD, Robinson NJ, Langridge-Smith PR, Sadler PJ (2003) Inert site in a protein zinc cluster. J Am Chem Soc 125:3226–3227

    Article  PubMed  CAS  Google Scholar 

  13. Blindauer CA, Sadler PJ (2005) How to hide zinc in a small protein. Acc Chem Res 38:62–69

    Article  PubMed  CAS  Google Scholar 

  14. Borrelly GP, Blindauer CA, Scmid R, Butler CS, Cooper CE, Harvey I, Sadler PJ, Robinson NJ (2004a) A novel copper site in a cyanobacterial metallochaperone. Biochem J 378:293–297

    Article  PubMed  CAS  Google Scholar 

  15. Borrelly GP, Rondet SA, Tottey S, Robinson NJ (2004b) Chimeras of P-type ATPases and their transcriptional regulators: contributions of a cytosolic amino-terminal domain to metal specificity. Mol Microbiol 53:217–227

    Article  PubMed  CAS  Google Scholar 

  16. 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

    Article  PubMed  CAS  Google Scholar 

  17. Brocks JJ, Logan GA, Buick R, Summons RE (1999) Archaen molecular fossils and the early rise of eukaryotes. Science 285:1033–1036

    Article  PubMed  CAS  Google Scholar 

  18. Brown NL, Barrett SR, Camakaris J, Lee BT Rouch DA (1995) Molecular genetics and transport analysis of the copper-resistance determinant (pco) from Escherichia coli plasmid pRJ1004. Mol Microbiol 17:1153–1166

    Article  PubMed  CAS  Google Scholar 

  19. Bryson B (2004) A short history of nearly everything. Black Swan, London

    Google Scholar 

  20. Buckler DR, Zhou Y, Stock AM (2002) Evidence of intradomain and interdomain flexibility in an OmpR/PhoB homolog from Thermatoga maritime. Structure 10:153–164

    Article  PubMed  CAS  Google Scholar 

  21. Busenlehner LS, Weng TC, Penner-Hahn JE, Giedroc DP (2002) Elucidation of primary (alpha(3)N) and vestigial (alpha(5)) heavy metal-binding sites in Staphylococcus aureus pI258 CadC: evolutionary implications for metal ion selectivity of ArsR/SmtB metal sensor proteins. J Mol Biol 319:685–701

    Article  PubMed  CAS  Google Scholar 

  22. 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

    Article  PubMed  CAS  Google Scholar 

  23. Carroll MC, Girouard JB, Ulloa JL, Subramaniam JR, Wong PC, Valentine JS, Culotta VC (2004) Mechanisms for activating Cu- and Zn-containing superoxide dismutase in the absence of the CCS Cu chaperone. Proc Natl Acad Sci USA 101:5964–5969

    Article  PubMed  CAS  Google Scholar 

  24. Cavet JS, Meng W, Pennella MA, Appelhoff RJ, Giedroc DP, Robinson NJ (2002) A nickel-cobalt-sensing ArsR-SmtB family repressor. Contributions of cytosol and effector binding sites to metal selectivity. J Biol Chem 277:38441–38448

    Article  PubMed  CAS  Google Scholar 

  25. Cavet JS, Graham AI, Meng W, Robinson NJ (2003a) A cadmium-lead-sensing ArsR-SmtB repressor with novel sensory sites. Complementary metal discrimination by NmtR and CmtR in a common cytosol. J Biol Chem 278:44560–44566

    Article  PubMed  CAS  Google Scholar 

  26. Cavet JS, Borrelly GP, Robinson NJ (2003b) Zn, Cu and Co in cyanobacteria: selective control of metal availability. FEMS Microbiol Rev 27:165–181

    Article  PubMed  CAS  Google Scholar 

  27. 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

    Article  PubMed  CAS  Google Scholar 

  28. Chivers PT, Tahirov TH (2005) Structure of Pyrococcus horikoshii NikR: nickel sensing and implications for the regulation of DNA recognition. J Mol Biol 348:597–607

    Article  PubMed  CAS  Google Scholar 

  29. Cobine PA, Pierrel F, Winge DR (2006) Copper trafficking to the mitochondrion and assembly of copper metalloenzymes. Biochim Biophys Acta 1763:759–772

    Article  PubMed  CAS  Google Scholar 

  30. Cook WJ, Kar SR, Taylor KB, Hall LM (1998) Crystal structure of the metallothionein repressor SmtB: a model for metalloregulatory proteins. J Mol Biol 275:337–346

    Article  PubMed  CAS  Google Scholar 

  31. Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12through a symbiotic relationship with bacteria. Nature 438:90–93

    Article  PubMed  CAS  Google Scholar 

  32. Culotta VC, Klomp LW, Strain J, Casareno RL, Krems B, Gitlin JD (1997) The copper chaperone for superoxide dismutase. J Biol Chem 272:23469–23472

    Article  PubMed  CAS  Google Scholar 

  33. Daniels MJ, Turner-Cavet JS, Selkirk R, Sun H, Parkinson JA, Sadler PJ, Robinson NJ (1998) Coordination of Zn2+(and Cd2+) by prokaryotic metallothionein. Involvement of His-imidazole. J Biol Chem 273:22957–22961

    Article  PubMed  CAS  Google Scholar 

  34. Eicken C, Pennella MA, Chen X, Koshlap KM, VanZile ML, Sacchettini JC, Giedroc DP (2003) A metal-ligand-mediated intersubunit allosteric switch in related SmtB/ArsR zinc sensor proteins. J Mol Biol 333:683–695

    Article  PubMed  CAS  Google Scholar 

  35. Eisenstein RS (2000) Iron regulatory proteins and the molecular control of mammalian iron metabolism. Annu Rev Nutr 20:627–662

    Article  PubMed  CAS  Google Scholar 

  36. Endo G, Silver S (1995) CadC, the transcriptional regulatory protein of the cadmium resistance system of Staphylococcus aureus plasmid pI258. J Bacteriol 177:4437–4441

    PubMed  CAS  Google Scholar 

  37. Ferguson-Miller S, Babcock GT (1996) Heme/copper terminal oxidases. Chem Rev 96:2889–2908

    Article  PubMed  CAS  Google Scholar 

  38. Finney LA, O'Halloran TV (2003) Transition metal speciation in the cell: insights from the chemistry of metal ion receptors. Science 300:931–936

    Article  PubMed  CAS  Google Scholar 

  39. Fraústo da Silva JJR, Williams RJP (2002) The biological chemistry of the elements: the inorganic chemistry of life. Clarendon Press, Oxford

    Google Scholar 

  40. Fulda S, Huang F, Hagemann M, Norling B (2000) Proteomics of Synechocystis sp. Strain PCC 6803. Identification of periplasmic proteins in cells grown at low and high salt concentrations. Eur J Biochem 267:5900–5907

    Article  PubMed  CAS  Google Scholar 

  41. Furukawa Y, Torres AS, O'Halloran TV (2004) Oxygen-induced maturation of SOD1: a key role for disulfide formation by the copper chaperone CCS. EMBO J 23:2872–2881

    Article  PubMed  CAS  Google Scholar 

  42. Glasfeld A, Guedon E, Helmann JD, Brennan RG (2003) Structure of the manganese-bound transport regulator of Bacillus subtilis. Nat Struct Biol 10:652–657

    Article  PubMed  CAS  Google Scholar 

  43. Guedon E, Helmann JD (2003) Origins of metal ion selectivity in the DtxR/MntR family of metalloregulators. Mol Microbiol 48:495–506

    Article  PubMed  CAS  Google Scholar 

  44. Harvie DR, Andreini C, Cavallaro G, Meng W, Connolly BA, Yoshida K, Fujita Y, Harwood CR, Radford DS, Tottey S, Cavet JS, Robinson NJ (2006) Predicting metals sensed by ArsR-SmtB repressors: allosteric interference by a non-effector metal. Mol Microbiol 59:1341–1356

    Article  PubMed  CAS  Google Scholar 

  45. Higham DP, Sadler PJ, Scawen MD (1984) Cadmium-resistant Pseudomonas putidasynthesizes novel cadmium proteins. Science 225:1043–1046

    Article  CAS  PubMed  Google Scholar 

  46. Higham DP, Sadler PJ, Scawen MD (1986) Cadmium-binding proteins in Pseudomonas: pseudothioneins. Environ Health Perspect 65:5–11

    Article  PubMed  CAS  Google Scholar 

  47. Hintze KJ, Theil EC (2006) Cellular regulation and molecular interactions of the ferritins. Cell Mol Life Sci 63:591–600

    Article  PubMed  CAS  Google Scholar 

  48. Horng YC, Cobine PA, Maxfield AB, Carr HS, Winge DR (2004) Specific copper transfer from the Cox17 metallochaperone to both Sco1 and Cox11 in the assembly of yeast cytochrome C oxidase. J Biol Chem 279:35334–35340

    Article  PubMed  CAS  Google Scholar 

  49. Huang F, Fulda S, Hagemann M, Norling B (2006) Proteomic screening of salt-stress-induced changes in plasma membranes of Synechocystis sp. strain PCC 6803. Proteomics 6:910–920

    Article  PubMed  CAS  Google Scholar 

  50. Huckle JW, Morby AP, Turner JS, Robinson NJ (1993) Isolation of a prokaryotic metalothionein locus and analysis of transcriptional control by trace metal ions. Mol Microbiol 7:177–187

    Article  PubMed  CAS  Google Scholar 

  51. Huffman DL, O'Halloran TV (2001) Function, structure, and mechanism of intracellular copper-trafficking proteins. Annu Rev Biochem 70:677–701

    Article  PubMed  CAS  Google Scholar 

  52. Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Åresolution. Nature 411:909–917

    Article  PubMed  CAS  Google Scholar 

  53. Katoh H, Hagino N, Grossman AR, Ogawa T (2001a) Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 183:2779–2784

    Article  PubMed  CAS  Google Scholar 

  54. Katoh H, Hagino N, Ogawa T (2001b) Iron-binding activity of FutA1 subunit of an ABC-type iron transporter in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Cell Physiol 42:823–827

    Article  PubMed  CAS  Google Scholar 

  55. Keren N, Kidd MJ, Penner-Hahn JE, Pakrasi HB (2002) A light-dependent mechanism for massive accumulation of manganese in the photosynthetic bacterium Synechocystis sp. PCC 6803. Biochemistry 41:15085–15092

    Article  PubMed  CAS  Google Scholar 

  56. Keren N, Aurora R, Pakrasi HB (2004) Critical roles of bacterioferritins in iron storage and proliferation of cyanobacteria. Plant Physiol 135:1666–1673

    Article  PubMed  CAS  Google Scholar 

  57. Kim HJ, Graham DW, DiSpirito AA, Alterman MA, Galeva N, Larive CK, Asunskis D, Sherwood PM (2004) Methanobactin, a copper-acquisition compound from methane-oxidizing bacteria. Science 305:1612–1615

    Article  PubMed  CAS  Google Scholar 

  58. Kondorosi E, Pierre M, Cren M, Haumann U, Buire M, Hoffmann B, Schell J, Kondorosi A (1991) Identification of NolR, a negative transacting factor controlling the nod regulon in Rhizobium meliloti. J Mol Biol 222:885–896

    Article  PubMed  CAS  Google Scholar 

  59. Kropat J, Tottey S, Birkenbihl RP, Depege N, Huijser P, Merchant S (2005) A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element. Proc Natl Acad Sci USA 102:18730–18735

    Article  PubMed  CAS  Google Scholar 

  60. Kuper J, Llamas A, Hecht H-J, Mendel RR, Schwarz G (2004) Structure of the molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism. Nature 430:803–806

    Article  PubMed  CAS  Google Scholar 

  61. Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014

    Article  PubMed  CAS  Google Scholar 

  62. Leech HK, Raux E, McLean KJ, Munro AW, Robinson NJ, Borrelly GP, Malten M, Jahn D, Rigby SE, Heathcote P, Warren MJ (2003) Characterization of the cobaltochelatase CbiXL: evidence for a 4Fe-4S center housed within an MXCXXC motif. J Biol Chem 278:41900–41907

    Article  PubMed  CAS  Google Scholar 

  63. Lichtlen P, Schaffner W (2001) Putting its fingers on stressful situations: the heavy metal-regulatory transcription factor MTF-1. Bioessays 23:1010–1017

    Article  PubMed  CAS  Google Scholar 

  64. Lieberman RL, Rosenzweig AC (2005) Crystal structure of a membrane-bound metalloenzyme that catalyses the biological oxidation of methane. Nature 434:177–182

    Article  PubMed  CAS  Google Scholar 

  65. Liu T, Golden JW, Giedroc DP (2005) A zinc (II)/lead(II)/cadmium(II)-inducible operon from the cyanobacterium Anabaena is regulated by AztR, an alpha3N ArsR/SmtB metalloregulator. Biochemistry 44:8673–8683

    Article  PubMed  CAS  Google Scholar 

  66. Magnani D, Solioz M (2005) Copper chaperone cycling and degradation in the regulation of the cop operon of Enterococcus hirae. Biometals 18:407–412

    Article  PubMed  CAS  Google Scholar 

  67. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99:12246–12251

    Article  PubMed  CAS  Google Scholar 

  68. Maxfield AB, Heaton DN, Winge DR (2004) Cox17 is functional when tethered to the mitochondrial inner membrane. J Biol Chem 279:5072–5080

    Article  PubMed  CAS  Google Scholar 

  69. Merchant S (1998) Synthesis of metalloproteins involved in photosynthesis: plastocyanin and cytochromes. In: Rochaix J-D, Goldschmidt-Clermont M, Merchant S (eds) The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas. Kluwer, Dordrecht, pp 597–611

    Google Scholar 

  70. Molina-Heredia FP, Wastl J, Navarro JA, Bendall DS, Hervas M, Howe CJ, De La Rosa MA (2003) Photosynthesis: a new function for an old cytochrome? Nature 424:33–34

    Article  PubMed  CAS  Google Scholar 

  71. Morby AP, Turner JS, Huckle JW, Robinson NJ (1993) SmtB is a metal-dependent repressor of the cyanobacterial metallothionein gene smtA: identification of a Zn inhibited DNA-protein complex. Nucleic Acids Res 21:921–925

    Article  PubMed  CAS  Google Scholar 

  72. 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

    Article  PubMed  CAS  Google Scholar 

  73. Niederhoffer EC, Naranjo CM, Bradley KL, Fee JA (1990) Control of Escherichia coli superoxide dismutase (sodA and sodB) genes by the ferric uptake regulation (fur) locus. J Bacteriol 172:1930–1938

    PubMed  CAS  Google Scholar 

  74. Odermatt A, Solioz M (1995) Two trans-acting metalloregulatory proteins controlling expression of the copper-ATPases of Enterococcus hirae. J Biol Chem 270:4349–4354

    Article  PubMed  CAS  Google Scholar 

  75. Ogawa T, Bao DH, Katoh H, Shibata M, Pakrasi HB, Bhattacharyya-Pakrasi M (2002) A two-component signal transduction pathway regulates manganese homeostasis in Synechocystis 6803, a photosynthetic organism. J Biol Chem 277:28981–28986

    Article  PubMed  CAS  Google Scholar 

  76. Olafson RW, McCubbin WD, Kay CM (1988) Primary- and secondary-structural analysis of a unique prokaryotic metallothionein from a Synechococcus sp. cyanobacterium. Biochem J 251:691–699

    PubMed  CAS  Google Scholar 

  77. Olesen C, Sørensen TLM, Nielsen RC, Møller JV, Nissen P (2004) Dephosphorylation of the calcium pump coupled to counterion occlusion. Science 306:2251–2255

    Article  PubMed  CAS  Google Scholar 

  78. 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

    Article  PubMed  CAS  Google Scholar 

  79. Outten CE, O'Halloran TV (2001) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292:2488–2492

    Article  PubMed  CAS  Google Scholar 

  80. Panina EM, Mironov AA, Gelfand MS (2003) Comparative genomics of bacterial zinc regulons: enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins. Proc Natl Acad Sci USA 100:9912–9917

    Article  PubMed  CAS  Google Scholar 

  81. Pantopoulos K (2004) Iron metabolism and the IRE/IRP regulatory system: an update. Ann NY Acad Sci 1012:1–13

    Article  PubMed  CAS  Google Scholar 

  82. Patzer SI, Hantke K (1999) The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol Microbiol 32:887–889

    Article  Google Scholar 

  83. Pennella MA, Shokes JE, Cosper NJ, Scott RA, Giedroc DP (2003) Structural elements of metal selectivity in metal sensor proteins. Proc Natl Acad Sci USA 100:3713–3718

    Article  PubMed  CAS  Google Scholar 

  84. Pohl E, Haller JC, Mijovilovich A, Meyer-Klauke W, Garman E, Vasil ML (2003) Architecture of a protein central to iron homeostasis: crystal structure and spectroscopic analysis of the ferric uptake regulator. Mol Microbiol 47:903–915

    Article  PubMed  CAS  Google Scholar 

  85. Pufahl RA, Singer CP, Peariso KL, Lin SJ, Schmidt PJ, Fahrni CJ, Culotta VC, Penner-Hahn JE, O'Halloran TV (1997) Metal ion chaperone function of the soluble Cu(I) receptor Atx1. Science 278:853–856

    Article  PubMed  CAS  Google Scholar 

  86. Qiu X, Verlinde CL, Zhang S, Schmitt MP, Holmes RK, Hol WG (1995) Three-dimensional structure of the diphtheria toxin repressor in complex wih divalent cation co-repressors. Structure 3:87–100

    Article  PubMed  CAS  Google Scholar 

  87. Radford DS, Kihlken MA, Borrelly GP, Harwood CR, Le Brun NE, Cavet JS (2003) CopZ from Bacillus subtilis interacts in vivo with a copper exporting CPx-type ATPase CopA. FEMS Microbiol Lett 220:105–112

    Article  PubMed  CAS  Google Scholar 

  88. Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O'Halloran TV (1999) Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 284:805–808

    Article  PubMed  CAS  Google Scholar 

  89. Raven JA, Evans MCW, Korb RE (1999) The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynth Res 60:111–149

    Article  CAS  Google Scholar 

  90. Rensing C, Grass G (2003) Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27:197–213

    Article  PubMed  CAS  Google Scholar 

  91. Rivera MC, Lake JA (2004) The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431:152–155

    Article  PubMed  CAS  Google Scholar 

  92. Robinson NJ, Gupta A, Fordham-Skelton AP, Croy RR, Whitton BA, Huckle JW (1990) Prokaryotic metallothionein gene characterisation and expression: chromosome crawling by ligation-mediated PCR. Proc Biol Sci 242:241–247

    Article  PubMed  CAS  Google Scholar 

  93. Robinson NJ, Bird AJ, Turner JS (1997) Metallothionein gene regulation in cyanobacteria. In: Silver S, Walden W (eds) Metal Ions in Gene Regulation. Chapman and Hall, New York, pp 372–397

    Google Scholar 

  94. Robinson NJ, Whitehall SK, Cavet JS (2001) Microbial metallothioneins. Adv Microb Physiol 44:183–213

    Article  PubMed  CAS  Google Scholar 

  95. Rosenzweig AC, Huffman DL, Hou MY, Wernimont AK, Pufahl RA, O'Halloran TV (1999) Crystal structure of the Atx1 metallochaperone protein at 1.02 Åresolution. Structure 7:605–617

    Article  PubMed  CAS  Google Scholar 

  96. Rowe JL, Starnes GL, Chivers PT (2005) Complex transcriptional control links NikABCDE-dependent nickel transport with hydrogenase expression in Escherichia coli. J Bacteriol 187:6317–6323

    Article  PubMed  CAS  Google Scholar 

  97. Rutherford JC, Cavet JS, Robinson NJ (1999) Cobalt-dependent transcriptional switching by a dual-effector MerR-like protein regulates a cobalt-exporting variant CPx-type ATPase. J Biol Chem 274:25827–25832

    Article  PubMed  CAS  Google Scholar 

  98. Rutherford JC, Bird AJ (2004) Metal-responsive transcription factors that regulate iron, zinc and copper homeostasis in eukaryotic cells. Eukaryotic Cell 3:1–13

    Article  PubMed  CAS  Google Scholar 

  99. Schmidt PJ, Kunst C, Culotta VC (2000) Copper activation of superoxide dismutase 1 (SOD1) in vivo. Role for protein–protein interactions with the copper chaperone for SOD1. J Biol Chem 275:33771–33776

    Article  PubMed  CAS  Google Scholar 

  100. Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31:3381–3385

    Article  PubMed  CAS  Google Scholar 

  101. Shi J, Lindsay WP, Huckle JW, Morby AP, Robinson NJ (1992) Cyanobacterial metallothionein gene expressed in Escherichia coli: metal-binding properties of the expressed protein. FEBS Lett 303:159–163

    Article  PubMed  CAS  Google Scholar 

  102. Shi W, Wu J, Rosen BP (1994) Identification of a putative metal binding site in a new family of metalloregulatory proteins. J Biol Chem 269:19826–19829

    PubMed  CAS  Google Scholar 

  103. Shi W, Dong J, Scott RA, Ksenzenko MY, Rosen BP (1996) The role of arsenic-thiol interactions in metalloregulation of the ars operon. J Biol Chem 271:9291–9297

    Article  PubMed  CAS  Google Scholar 

  104. Shipman LW, Li D, Roessner CA, Scott AI, Sacchettini JC (2001) Crystal structure of precorrin-8x methyl mutase. Structure 9:587–596

    Article  PubMed  CAS  Google Scholar 

  105. Solioz M, Stoyanov JV (2003) Copper homeostasis in Enterococcus hirae. FEMS Microbiol Rev 27:183–195

    Article  PubMed  CAS  Google Scholar 

  106. Spence E, Sarcina M, Ray N, Moller SG, Mullineaux CW, Robinson C (2003) Membrane-specific targeting of green fluorescent protein by the Tat pathway in the cyanobacterium Synechocystis PCC6803. Mol Microbiol 48:1481–1489

    Article  PubMed  CAS  Google Scholar 

  107. 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

    Article  PubMed  CAS  Google Scholar 

  108. Terry N (1983) Limiting factors in photosynthesis: IV. Iron stress-mediated changes in light-harvesting and electron transport capacity and its effects on photosynthesis in vivo. Plant Physiol 71:855–860

    Article  PubMed  CAS  Google Scholar 

  109. Thelwell C, Robinson NJ, Turner-Cavet JS (1998) An SmtB-like repressor from Synechocystis PCC 6803 regulates a zinc exporter. Proc Natl Acad Sci USA 95:10728–10733

    Article  PubMed  CAS  Google Scholar 

  110. Tottey S, Rich PR, Rondet SAM, Robinson NJ (2001) Two Menkes-type ATPases supply copper for photosynthesis in Synechocystis PCC 6803. 276:19999–20004

    Google Scholar 

  111. Tottey S, Rondet SA, Borrelly GP, Robinson PJ, Rich PR, Robinson NJ (2002) A copper metallochaperone for photosynthesis and respiration reveals metal-specific targets, interaction with an importer, and alternative sites for copper acquisition. J Biol Chem 277:5490–5497

    Article  PubMed  CAS  Google Scholar 

  112. Tottey S, Harvie DR, Robinson NJ (2005) Understanding how cells allocate metals using metal sensors and metallochaperones. Acc Chem Res 38:775–783

    Article  PubMed  CAS  Google Scholar 

  113. Turner JS, Robinson NJ (1995) Cyanobacterial metallothioneins: biochemistry and molecular genetics. J Ind Microbiol 14:119–125

    Article  PubMed  CAS  Google Scholar 

  114. Turner JS, Glands PD, Samson AC, Robinson NJ (1996) Zn2+-sensing by the cyanobacterial metallothionein repressor SmtB: different motifs mediate metal-induced protein-DNA dissociation. Nucleic Acids Res 24:3714–3721

    Article  PubMed  CAS  Google Scholar 

  115. Tseng CP (1997) Regulation of fumarase (fumB) gene expression in Escherichia coli in response to oxygen, iron and heme availability: role of the arcA, fur, and hemA gene products. FEMS Microbiol Lett 157:67–72

    Article  PubMed  CAS  Google Scholar 

  116. Van de Meene AM, Hohmann-Marriott MF, Vermaas WF, Roberson RW (2006) The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803. Arch Microbiol 184:259–270

    Article  CAS  Google Scholar 

  117. VanZile ML, Cosper NJ, Scott RA, Giedroc DP (2000) The zinc metalloregulatory protein Synechococcus PCC7942 SmtB binds a single zinc ion per monomer with high affinity in a tetrahedral coordination geometry. Biochemistry 39:11818–11829

    Article  PubMed  CAS  Google Scholar 

  118. VanZile ML, Chen X, Giedroc DP (2002) Allosteric negative regulation of smt O/P binding of the zinc sensor, SmtB, by metal ions: a coupled equilibrium analysis. Biochemistry 41:9776–9786

    Article  PubMed  CAS  Google Scholar 

  119. Weigel M, Varotto C, Pesaresi P, Finazzi G, Rappaport F, Salamini F, Leister D (2003) Plastocyanin is indespensable for photosynthetic electron flow in Arabidopsis thaliana. J Biol Chem 278:31286–31289

    Article  PubMed  CAS  Google Scholar 

  120. White A, Ding X, van der Spek JC, Murphy JR, Ringe D (1998) Structure of the metal-ion-activated diphtheria toxin repressor/tox operator complex. Nature 394:502–506

    Article  PubMed  CAS  Google Scholar 

  121. Williams SG, Attridge SR, Manning PA (1993) The transcriptional activator HlyU of Vibrio cholerae: nucleotide sequence and role in virulence gene expression. Mol Microbiol 9:751–760

    Article  PubMed  CAS  Google Scholar 

  122. Wu J, Rosen BP (1991) The ArsR protein is a trans-acting regulatory protein. Mol Microbiol 5:1331–1336

    Article  PubMed  CAS  Google Scholar 

  123. Xiao Z, Loughlin F, George GN, Howlett GJ, Wedd AG (2004) C-terminal domain of the membrane copper transporter Ctr1 from Saccharomyces cerevisiae binds four Cu(I) ions as a cuprous-thiolate polynuclear cluster: sub-femtomolar Cu(I) affinity of three proteins involved in copper trafficking. J Am Chem Soc 126:3081–3090

    Article  PubMed  CAS  Google Scholar 

  124. Ye J, Kandegedara A, Martin P, Rosen BP (2005) Crystal structure of the Staphylococcus aureus pI258 CadC Cd(II)/Pb(II)/Zn(II)-responsive repressor. J Bacteriol 187:4214–4221

    Article  PubMed  CAS  Google Scholar 

  125. Yoon HS, Hackett JD, Pinto G, Bhattacharya D (2002) The single, ancient origin of chromist plastids. Proc Natl Acad Sci USA 99:15507–15512

    Article  PubMed  CAS  Google Scholar 

  126. Zheng M, Doan B, Schneider TD, Storz G (1999) OxyR and SoxRS regulation of fur. J Bacteriol 181:4639–4643

    PubMed  CAS  Google Scholar 

  127. Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Åresolution. Nature 409:739–743

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Nigel J. Robinson .

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Dietrich H. Nies Simon Silver

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Tottey, S., Harvie, D.R., Robinson, N.J. (2007). Understanding How Cells Allocate Metals. In: Nies, D.H., Silver, S. (eds) Molecular Microbiology of Heavy Metals. Microbiology Monographs, vol 6. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7171_2006_072

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