Skip to main content
SpringerLink
Log in

Copper Homeostasis in Gram-Negative Bacteria

  • Chapter
  • First Online:
Copper and Bacteria

Part of the book series: SpringerBriefs in Molecular Science ((SB BIOMETALS))

Abstract

Copper homeostasis in Gram-negative organisms is complicated by the two cell membranes and the periplasmic space. The thinking of how copper enters bacteria like E. coli has undergone some changes recently and new concepts have emerged. Also, the elusive CopZ-like copper chaperone has finally been discovered in E. coli. While the extrusion of excess copper via the CopA copper ATPase and the CusCFBA transporter and the regulation of these systems appear fairly clear, there are still major open questions concerning the metallation of cuproenzymes. Some provocative new concepts will be proposed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Tottey S, Rich PR, Rondet SA et al (2001) Two Menkes-type atpases supply copper for photosynthesis in Synechocystis PCC 6803. J Biol Chem 276:19999–20004

    Article  PubMed  CAS  Google Scholar 

  2. Phung LT, Ajlani G, Haselkorn R (1994) P-type ATPase from the cyanobacterium Synechococcus 7942 related to the human Menkes and Wilson disease gene products. Proc Natl Acad Sci U S A 91:9651–9654

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Lewinson O, Lee AT, Rees DC (2009) A P-type ATPase importer that discriminates between essential and toxic transition metals. Proc Natl Acad Sci U S A 106:4677–4682

    Article  PubMed  PubMed Central  Google Scholar 

  4. Odermatt A, Krapf R, Solioz M (1994) Induction of the putative copper ATPases, CopA and CopB, of Enterococcus hirae by Ag+ and Cu2+, and Ag+ extrusion by CopB. Biochem Biophys Res Commun 202:44–48

    Article  PubMed  CAS  Google Scholar 

  5. Koch HG, Winterstein C, Saribas AS et al (2000) Roles of the ccoGHIS gene products in the biogenesis of the cbb3-type cytochrome c oxidase. J Mol Biol 297:49–65

    Article  PubMed  CAS  Google Scholar 

  6. Hassani BK, Astier C, Nitschke W et al (2010) CtpA a copper-translocating P-type ATPase involved in the biogenesis of multiple copper-requiring enzymes. J Biol Chem 285:19330–19337

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Koh EI, Henderson JP (2015) Microbial copper-binding siderophores at the host-pathogen interface. J Biol Chem 290:18967–18974

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Wilson BR, Bogdan AR, Miyazawa M et al (2016) Siderophores in iron metabolism: from mechanism to therapy potential. Trends Mol Med 22:1077–1090

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Koh EI, Robinson AE, Bandara N et al (2017) Copper import in Escherichia coli by the yersiniabactin metallophore system. Nat Chem Biol 13:1016–1021

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Noinaj N, Guillier M, Barnard TJ et al (2010) TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol 64:43–60

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Cavet JS (2014) Copper as a magic bullet for targeted microbial killing. Chem Biol 21:921–922

    Article  PubMed  CAS  Google Scholar 

  12. Solioz M (2016) Copper oxidation state and mycobacterial infection. Mycobact Dis 6:210–213

    Article  Google Scholar 

  13. Kim HJ, Graham DW, DiSpirito AA et al (2004) Methanobactin, a copper-acquisition compound from methane-oxidizing bacteria. Science 305:1612–1615

    Article  PubMed  CAS  Google Scholar 

  14. Kenney GE, Rosenzweig AC (2013) Genome mining for methanobactins. BMC Biol 11:17

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. DiSpirito AA, Semrau JD, Murrell JC et al (2016) Methanobactin and the link between copper and bacterial methane oxidation. Microbiol Mol Biol Rev 80:387–409

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Balasubramanian R, Kenney GE, Rosenzweig AC (2011) Dual pathways for copper uptake by methanotrophic bacteria. J Biol Chem 286:37313–37319

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Ve T, Mathisen K, Helland R et al (2012) The Methylococcus capsulatus (Bath) secreted protein, MopE*, binds both reduced and oxidized copper. PLoS ONE 7:e43146

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Zhang XX, Rainey PB (2008) Regulation of copper homeostasis in Pseudomonas fluorescens SBW25. Environ Microbiol 10:3284–3294

    Article  PubMed  CAS  Google Scholar 

  19. Wijekoon CJ, Young TR, Wedd AG et al (2015) CopC protein from Pseudomonas fluorescens SBW25 features a conserved novel high-affinity Cu(II) binding site. Inorg Chem 54:2950–2959

    Article  PubMed  CAS  Google Scholar 

  20. Lawton TJ, Kenney GE, Hurley JD et al (2016) The CopC family: structural and bioinformatic insights into a diverse group of periplasmic copper binding proteins. Biochemistry 55:2278–2290

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Hirooka K, Edahiro T, Kimura K et al (2012) Direct and indirect regulation of the ycnKJI operon involved in copper uptake through two transcriptional repressors, YcnK and CsoR, in Bacillus subtilis. J Bacteriol 194:5675–5687

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Cha JS, Cooksey DA (1993) Copper hypersensitivity and uptake in Pseudomonas syringae containing cloned components of the copper resistance operon. Appl Environ Microbiol 59:1671–1674

    PubMed  PubMed Central  CAS  Google Scholar 

  23. Gu W, Farhan Ul Haque M, Semrau JD (2017) Characterization of the role of copCD in copper uptake and the “copper-switch” in Methylosinus trichosporium OB3b. FEMS Microbiol Lett 164:fnx094

    Google Scholar 

  24. Kanamaru K, Kashiwagi S, Mizuno T (1994) A copper-transporting P-type ATPase found in the thylakoid membrane of the cyanobacterium Synechococcus species PCC7942. Mol Microbiol 13:369–377

    Article  PubMed  CAS  Google Scholar 

  25. Verméglio A, Lavergne J, Rappaport F (2016) Connectivity of the intracytoplasmic membrane of Rhodobacter sphaeroides: a functional approach. Photosynth Res 127:13–24

    Article  PubMed  CAS  Google Scholar 

  26. Niederman RA (2016) Development and dynamics of the photosynthetic apparatus in purple phototrophic bacteria. Biochim Biophys Acta 1857:232–246

    Article  PubMed  CAS  Google Scholar 

  27. Ekici S, Yang H, Koch HG et al (2012) Novel transporter required for biogenesis of cbb3-type cytochrome c oxidase in Rhodobacter capsulata. MBio 3:e00293-11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Ekici S, Turkarslan S, Pawlik G et al (2014) Intracytoplasmic copper homeostasis controls cytochrome c oxidase production. MBio 5

    Google Scholar 

  29. Wang Y, Hodgkinson V, Zhu S et al (2011) Advances in the understanding of mammalian copper transporters. Adv Nutr 2:129–137

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Beaudoin J, Ioannoni R, Lopez-Maury L et al (2011) Mfc1 is a novel forespore membrane copper transporter in meiotic and sporulating cells. J Biol Chem 286:34356–34372

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Beaudoin J, Ioannoni R, Labbe S (2012) Mfc1 is a novel copper transporter during meiosis. Commun Integr Biol 5:118–121

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Beaudoin J, Ekici S, Daldal F et al (2013) Copper transport and regulation in Schizosaccharomyces pombe. Biochem Soc Trans 41:1679–1686

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Khalfaoui-Hassani B, Verissimo AF, Koch HG et al (2016) Uncovering the transmembrane metal binding site of the novel bacterial major facilitator superfamily-type copper importer CcoA. MBio 7:e01981-15

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Meydan S, Klepacki D, Karthikeyan S et al (2017) Programmed ribosomal frameshifting generates a copper transporter and a copper chaperone from the same gene. Mol Cell 65:207–219

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Drees SL, Klinkert B, Helling S et al (2017) One gene, two proteins: coordinated production of a copper chaperone by differential transcript formation and translational frameshifting in Escherichia coli. Mol Microbiol 106:635–645

    Article  PubMed  CAS  Google Scholar 

  36. Gupta A, Lutsenko S (2009) Human copper transporters: mechanism, role in human diseases and therapeutic potential. Future Med Chem 1:1125–1142

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Outten FW, Outten CE, Hale J et al (2000) Transcriptional activation of an Escherichia coli copper efflux regulon by the chromosomal MerR homologue, CueR. J Biol Chem 275:31024–31029

    Article  PubMed  CAS  Google Scholar 

  38. Djoko KY, Chong LX, Wedd AG et al (2010) Reaction mechanisms of the multicopper oxidase CueO from Escherichia coli support its functional role as a cuprous oxidase. J Am Chem Soc 132:2005–2015

    Article  PubMed  CAS  Google Scholar 

  39. Grass G, Thakali K, Klebba PE et al (2004) Linkage between catecholate siderophores and the multicopper oxidase CueO in Escherichia coli. J Bacteriol 186:5826–5833

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Tree JJ, Kidd SP, Jennings MP et al (2005) Copper sensitivity of cueO mutants of Escherichia coli K-12 and the biochemical suppression of this phenotype. Biochem Biophys Res Commun 328:1205–1210

    Article  PubMed  CAS  Google Scholar 

  41. Grass G, Rensing C (2001) CueO is a multi-copper oxidase that confers copper tolerance in Escherichia coli. Biochem Biophys Res Commun 286:902–908

    Article  PubMed  CAS  Google Scholar 

  42. Singh SK, Grass G, Rensing C et al (2004) Cuprous oxidase activity of CueO from Escherichia coli. J Bacteriol 186:7815–7817

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Wu T, Wang S, Wang Z et al (2015) A multicopper oxidase contributes to the copper tolerance of Brucella melitensis 16M. FEMS Microbiol Lett 362:1–7

    PubMed  Google Scholar 

  44. Mancini S, Kumar R, Mishra V et al (2017) Desulfovibrio DA2_CueO is a novel multicopper oxidase with cuprous, ferrous, and phenol oxidase activity. Microbiol 163:1229–1236

    Article  CAS  Google Scholar 

  45. Rowland JL, Niederweis M (2013) A multicopper oxidase is required for copper resistance in Mycobacterium tuberculosis. J Bacteriol 195:3724–3733

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Wagner D, Maser J, Moric I et al (2006) Elemental analysis of the Mycobacterium avium phagosome in Balb/c mouse macrophages. Biochem Biophys Res Commun 344:1346–1351

    Article  PubMed  CAS  Google Scholar 

  47. Hodgkinson V, Petris MJ (2012) Copper homeostasis at the host-pathogen interface. J Biol Chem 287:13549–13555

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Hasan NM, Lutsenko S (2012) Regulation of copper transporters in human cells. Curr Top Membr 69:137–161

    Article  PubMed  CAS  Google Scholar 

  49. Achard ME, Tree JJ, Holden JA et al (2010) The multi-copper oxidase CueO of Salmonella enterica serovar Typhimurium is required for systemic virulence. Infect Immun 78:2312–2319

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Osman D, Cavet JS (2011) Metal sensing in Salmonella: implications for pathogenesis. Adv Microb Physiol 58:175–232

    Article  PubMed  CAS  Google Scholar 

  51. Huston WM, Jennings MP, McEwan AG (2002) The multicopper oxidase of Pseudomonas aeruginosa is a ferroxidase with a central role in iron acquisition. Mol Microbiol 45:1741–1750

    Article  PubMed  CAS  Google Scholar 

  52. Huston WM, Naylor J, Cianciotto NP et al (2008) Functional analysis of the multi-copper oxidase from Legionella pneumophila. Microbes Infect 10:497–503

    Article  PubMed  CAS  Google Scholar 

  53. Rodriguez-Montelongo L, Volentini SI, Farias RN et al (2006) The Cu(II)-reductase NADH dehydrogenase-2 of Escherichia coli improves the bacterial growth in extreme copper concentrations and increases the resistance to the damage caused by copper and hydroperoxide. Arch Biochem Biophys 451:1–7

    Article  PubMed  CAS  Google Scholar 

  54. Volentini SI, Farias RN, Rodriguez-Montelongo L et al (2011) Cu(II)-reduction by Escherichia coli cells is dependent on respiratory chain components. Biometals 24:827–835

    Article  PubMed  CAS  Google Scholar 

  55. Abicht HK, Gonskikh Y, Gerber SD et al (2013) Non-enzymatic copper reduction by menaquinone enhances copper toxicity in Lactococcus lactis IL1403. Microbiol 159:1190–1197

    Article  CAS  Google Scholar 

  56. Mermod M, Magnani D, Solioz M et al (2012) The copper-inducible ComR (YcfQ) repressor regulates expression of ComC (YcfR), which affects copper permeability of the outer membrane of Escherichia coli. Biometals 25:33–43

    Article  PubMed  CAS  Google Scholar 

  57. Yu Z, Reichheld SE, Savchenko A et al (2010) A comprehensive analysis of structural and sequence conservation in the TetR family transcriptional regulators. J Mol Biol 400:847–864

    Article  PubMed  CAS  Google Scholar 

  58. Padilla-Benavides T, George Thompson AM, McEvoy MM et al (2014) Mechanism of ATPase-mediated Cu+ export and delivery to periplasmic chaperones: the interaction of Escherichia coli CopA and CusF. J Biol Chem 289:20492–20501

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Kim EH, Nies DH, McEvoy MM et al (2011) Switch or funnel: how RND-type transport systems control periplasmic metal homeostasis. J Bacteriol 193:2381–2387

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Long F, Su CC, Zimmermann MT et al (2010) Crystal structures of the CusA efflux pump suggest methionine-mediated metal transport. Nature 467:484–488

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Lei HT, Bolla JR, Bishop NR et al (2014) Crystal structures of CusC review conformational changes accompanying folding and transmembrane channel formation. J Mol Biol 426:403–411

    Article  PubMed  CAS  Google Scholar 

  62. Su CC, Long F, Lei HT et al (2012) Charged amino acids (R83, E567, D617, E625, R669, and K678) of CusA are required for metal ion transport in the Cus efflux system. J Mol Biol 422:429–441

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Chacon KN, Mealman TD, McEvoy MM et al (2014) Tracking metal ions through a Cu/Ag efflux pump assigns the functional roles of the periplasmic proteins. Proc Natl Acad Sci U S A 111:15373–15378

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Patel SJ, Padilla-Benavides T, Collins JM et al (2014) Functional diversity of five homologous Cu+-ATPases present in Sinorhizobium meliloti. Microbiol 160:1237–1251

    Article  CAS  Google Scholar 

  65. Rademacher C, Masepohl B (2012) Copper-responsive gene regulation in bacteria. Microbiol 158:2451–2464

    CAS  Google Scholar 

  66. Giner-Lamia J, Lopez-Maury L, Reyes JC et al (2012) The CopRS two-component system is responsible for resistance to copper in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 159:1806–1818

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Schelder S, Zaade D, Litsanov B et al (2011) The two-component signal transduction system CopRS of Corynebacterium glutamicum is required for adaptation to copper-excess stress. PLoS ONE 6:e22143

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Hu YH, Wang HL, Zhang M et al (2009) Molecular analysis of the copper-responsive CopRSCD of a pathogenic Pseudomonas fluorescens strain. J Microbiol 47:277–286

    Article  PubMed  CAS  Google Scholar 

  69. Bansal-Mutalik R, Nikaido H (2014) Mycobacterial outer membrane is a lipid bilayer and the inner membrane is unusually rich in diacyl phosphatidylinositol dimannosides. Proc Natl Acad Sci U S A 111:4958–4963

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Speer A, Rowland JL, Haeili M et al (2013) Porins increase copper susceptibility of Mycobacterium tuberculosis. J Bacteriol 195:5133–5140

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Ward SK, Hoye EA, Talaat AM (2008) The global responses of Mycobacterium tuberculosis to physiological levels of copper. J Bacteriol 190:2939–2946

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Wolschendorf F, Ackart D, Shrestha TB et al (2011) Copper resistance is essential for virulence of Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 108:1621–1626

    Article  PubMed  PubMed Central  Google Scholar 

  73. Darwin KH (2015) Mycobacterium tuberculosis and copper: a newly appreciated defense against an old foe? J Biol Chem 290:18962–18966

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Fahey RC, Brown WC, Adams WB et al (1978) Occurrence of glutathione in bacteria. J Bacteriol 133:1126–1129

    PubMed  PubMed Central  CAS  Google Scholar 

  75. Newton GL, Arnold K, Price MS et al (1996) Distribution of thiols in microorganisms: mycothiol is a major thiol in most actinomycetes. J Bacteriol 178:1990–1995

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Gaballa A, Newton GL, Antelmann H et al (2010) Biosynthesis and functions of bacillithiol, a major low-molecular-weight thiol in Bacilli. Proc Natl Acad Sci U S A 107:6482–6486

    Article  PubMed  PubMed Central  Google Scholar 

  77. Kim EK, Cha CJ, Cho YJ et al (2008) Synthesis of γ-glutamylcysteine as a major low-molecular-weight thiol in lactic acid bacteria Leuconostoc spp. Biochem Biophys Res Commun 369:1047–1051

    Article  PubMed  CAS  Google Scholar 

  78. Schafer FQ, Buettner GR (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30:1191–1212

    Article  PubMed  CAS  Google Scholar 

  79. Obeid MH, Oertel J, Solioz M et al (2016) Mechanism of attenuation of uranyl toxicity by glutathione in Lactococcus lactis. Appl Environ Microbiol 82:3563–3571

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Helbig K, Bleuel C, Krauss GJ et al (2008) Glutathione and transition-metal homeostasis in Escherichia coli. J Bacteriol 190:5431–5438

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Potter AJ, Trappetti C, Paton JC (2012) Streptococcus pneumoniae uses glutathione to defend against oxidative stress and metal ion toxicity. J Bacteriol 194:6248–6254

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Latinwo LM, Donald C, Ikediobi C et al (1998) Effects of intracellular glutathione on sensitivity of Escherichia coli to mercury and arsenite. Biochem Biophys Res Commun 242:67–70

    Article  PubMed  CAS  Google Scholar 

  83. Vasak M, Meloni G (2011) Chemistry and biology of mammalian metallothioneins. J Biol Inorg Chem 16:1067–1078

    Article  PubMed  CAS  Google Scholar 

  84. Huckle JW, Morby AP, Turner JS et al (1993) Isolation of a prokaryotic metallothionein locus and analysis of transcriptional control by trace metal ions. Mol Microbiol 7:177–187

    Article  PubMed  CAS  Google Scholar 

  85. Gold B, Deng H, Bryk R et al (2008) Identification of a copper-binding metallothionein in pathogenic mycobacteria. Nat Chem Biol 4:609–616

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Vita N, Platsaki S, Basle A et al (2015) A four-helix bundle stores copper for methane oxidation. Nature 525:140–143

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Vita N, Landolfi G, Basle A et al (2016) Bacterial cytosolic proteins with a high capacity for Cu(I) that protect against copper toxicity. Sci Rep 6:39065

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Baslé A, Platsaki S, Dennison C (2017) Visualizing copper storage: the importance of thiolate-coordinated tetranuclear clusters. Angew Chem Int Ed Engl 56:8697–8700

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Rao NN, Gomez-Garcia MR, Kornberg A (2009) Inorganic polyphosphate: essential for growth and survival. Annu Rev Biochem 78:605–647

    Article  PubMed  CAS  Google Scholar 

  90. Hashemi F, Leppard GG, Kushner DJ (1994) Copper resistance in Anabaena variabilis: effects of phosphate nutrition and polyphosphate bodies. Microb Ecol 27:159–176

    Article  PubMed  CAS  Google Scholar 

  91. Keasling JD, Hupf GA (1996) Genetic manipulation of polyphosphate metabolism affects cadmium tolerance in Escherichia coli. Appl Microbiol Biotechnol 62:743–746

    CAS  Google Scholar 

  92. Keasling JD (1997) Regulation of intracellular toxic metals and other cations by hydrolysis of polyphosphate. Ann N Y Acad Sci 829:242–249

    Article  PubMed  CAS  Google Scholar 

  93. Van Veen HW, Abee T, Kortstee GJ et al (1994) Generation of a proton motive force by the excretion of metal-phosphate in the polyphosphate-accumulating Acinetobacter johnsonii strain 210A. J Biol Chem 269:29509–29514

    PubMed  Google Scholar 

  94. Grillo-Puertas M, Schurig-Briccio LA, Rodriguez-Montelongo L et al (2014) Copper tolerance mediated by polyphosphate degradation and low-affinity inorganic phosphate transport system in Escherichia coli. BMC Microbiol 14:72

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  95. Alvarez S, Jerez CA (2004) Copper ions stimulate polyphosphate degradation and phosphate efflux in Acidithiobacillus ferrooxidans. Appl Environ Microbiol 70:5177–5182

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Remonsellez F, Orell A, Jerez CA (2006) Copper tolerance of the thermoacidophilic archaeon Sulfolobus metallicus: possible role of polyphosphate metabolism. Microbiol 152:59–66

    Article  CAS  Google Scholar 

  97. Scheuring S, Nevo R, Liu LN et al (2014) The architecture of Rhodobacter sphaeroides chromatophores. Biochim Biophys Acta 1837:1263–1270

    Article  PubMed  CAS  Google Scholar 

  98. Stolle P, Hou B, Brüser T (2016) The Tat substrate CueO Is transported in an incomplete folding state. J Biol Chem 291:13520–13528

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Osman D, Patterson CJ, Bailey K et al (2013) The copper supply pathway to a Salmonella Cu, Zn-superoxide dismutase (SodCII) involves P1B-type ATPase copper-efflux and periplasmic CueP. Mol Microbiol 87:466–477

    Article  PubMed  CAS  Google Scholar 

  100. Pontel LB, Audero ME, Espariz M et al (2007) GolS controls the response to gold by the hierarchical induction of Salmonella-specific genes that include a CBA efflux-coding operon. Mol Microbiol 66:814–825

    Article  PubMed  CAS  Google Scholar 

  101. Checa SK, Espariz M, Audero ME et al (2007) Bacterial sensing of and resistance to gold salts. Mol Microbiol 63:1307–1318

    Article  PubMed  CAS  Google Scholar 

  102. Osman D, Waldron KJ, Denton H et al (2010) Copper homeostasis in Salmonella is atypical and copper-CueP is a major periplasmic metal complex. J Biol Chem 285:25259–25268

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. Yoon BY, Kim YH, Kim N et al (2013) Structure of the periplasmic copper-binding protein CueP from Salmonella enterica serovar Typhimurium. Acta Crystallogr D Biol Crystallogr 69:1867–1875

    Article  PubMed  CAS  Google Scholar 

  104. Brzezinski P, Gennis RB (2008) Cytochrome c oxidase: exciting progress and remaining mysteries. J Bioenerg Biomembr 40:521–531

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  105. Solioz M (2018) Copper and bacteria. Elsevier, Amsterdam

    Book  Google Scholar 

  106. Raimunda D, Padilla-Benavides T, Vogt S et al (2013) Periplasmic response upon disruption of transmembrane Cu transport in Pseudomonas aeruginosa. Metallomics 5:144–151

    Article  PubMed  CAS  Google Scholar 

  107. Raimunda D, Gonzalez-Guerrero M, Leeber BW III et al (2011) The transport mechanism of bacterial Cu+-ATPases: distinct efflux rates adapted to different function. Biometals 24:467–475

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  108. Gonzalez-Guerrero M, Raimunda D, Cheng X et al (2010) Distinct functional roles of homologous Cu+ efflux ATPases in Pseudomonas aeruginosa. Mol Microbiol 78:1246–1258

    Article  PubMed  CAS  Google Scholar 

  109. Buhler D, Rossmann R, Landolt S et al (2010) Disparate pathways for the biogenesis of cytochrome oxidases in Bradyrhizobium japonicum. J Biol Chem 285:15704–15713

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  110. Gurumoorthy P, Ludwig B (2015) Deciphering protein-protein interactions during the biogenesis of cytochrome c oxidase from Paracoccus denitrificans. FEBS J 282:537–549

    Article  PubMed  CAS  Google Scholar 

  111. Carr HS, Maxfield AB, Horng YC et al (2005) Functional analysis of the domains in Cox11. J Biol Chem 280:22664–22669

    Article  PubMed  CAS  Google Scholar 

  112. Banci L, Bertini I, Cantini F et al (2004) Solution structure of Cox11, a novel type of beta-immunoglobulin-like fold involved in CuB site formation of cytochrome c oxidase. J Biol Chem 279:34833–34839

    Article  PubMed  CAS  Google Scholar 

  113. Thompson AK, Smith D, Gray J et al (2010) Mutagenic analysis of Cox11 of Rhodobacter sphaeroides: insights into the assembly of Cu(B) of cytochrome c oxidase. Biochemistry 49:5651–5661

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  114. Horng YC, Cobine PA, Maxfield AB et al (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 

  115. Balatri E, Banci L, Bertini I et al (2003) Solution structure of Sco1: a thioredoxin-like protein Involved in cytochrome c oxidase assembly. Structure 11:1431–1443

    Article  PubMed  CAS  Google Scholar 

  116. Lohmeyer E, Schroder S, Pawlik G et al (2012) The ScoI homologue SenC is a copper binding protein that interacts directly with the cbb3-type cytochrome oxidase in Rhodobacter capsulata. Biochim Biophys Acta 1817:2005–2015

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Thompson AK, Gray J, Liu A et al (2012) The roles of Rhodobacter sphaeroides copper chaperones PCu(A)C and Sco (PrrC) in the assembly of the copper centers of the aa(3)-type and the cbb(3)-type cytochrome c oxidases. Biochim Biophys Acta 1817:955–964

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  118. Serventi F, Youard ZA, Murset V et al (2012) Copper starvation-inducible protein for cytochrome oxidase biogenesis in Bradyrhizobium japonicum. J Biol Chem 287:38812–38823

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  119. Trasnea PI, Utz M, Khalfaoui-Hassani B et al (2016) Cooperation between two periplasmic copper chaperones is required for full activity of the cbb -type cytochrome c oxidase and copper homeostasis in Rhodobacter capsulatus. Mol Microbiol 100:345–361

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  120. Banci L, Bertini I, Ciofi-Baffoni S et al (2005) A copper(I) protein possibly involved in the assembly of CuA center of bacterial cytochrome c oxidase. Proc Natl Acad Sci U. S. A 102:3994–3999

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  121. Abriata LA, Banci L, Bertini I et al (2008) Mechanism of Cu(A) assembly. Nat Chem Biol 4:599–601

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  122. Abicht HK, Scharer MA, Quade N et al (2014) How periplasmic thioredoxin TlpA reduces bacterial copper chaperone ScoI and cytochrome oxidase subunit II (CoxB) prior to metallation. J Biol Chem 289:32431–32444

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  123. Tottey S, Waldron KJ, Firbank SJ et al (2008) Protein-folding location can regulate manganese-binding versus copper- or zinc-binding. Nature 455:1138–1142

    Article  PubMed  CAS  Google Scholar 

  124. Waldron KJ, Firbank SJ, Dainty SJ et al (2010) Structure and metal-loading of a soluble periplasm cupro-protein. J Biol Chem 285:32504–32511

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  125. Rast A, Heinz S, Nickelsen J (2015) Biogenesis of thylakoid membranes. Biochim Biophys Acta 1847:821–830

    Article  PubMed  CAS  Google Scholar 

  126. Frain KM, Gangl D, Jones A et al (2016) Protein translocation and thylakoid biogenesis in cyanobacteria. Biochim Biophys Acta 1857:266–273

    Article  PubMed  CAS  Google Scholar 

  127. Rexroth S, Mullineaux CW, Ellinger D et al (2011) The plasma membrane of the cyanobacterium Gloeobacter violaceus contains segregated bioenergetic domains. Plant Cell 23:2379–2390

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  128. Scanlan J, Dumont MG, Murrell JC (2009) Involvement of MmoR and MmoG in the transcriptional activation of soluble methane monooxygenase genes in Methylosinus trichosporium OB3b. FEMS Microbiol Lett 301:181–187

    Article  PubMed  CAS  Google Scholar 

  129. Semrau JD, Jagadevan S, DiSpirito AA et al (2013) Methanobactin and MmoD work in concert to act as the ‘copper-switch’ in methanotrophs. Environ Microbiol 15:377–386

    Google Scholar 

  130. Kenney GE, Sadek M, Rosenzweig AC (2016) Copper-responsive gene expression in the methanotroph Methylosinus trichosporium OB3b. Metallomics 8:931–940

    Article  PubMed  CAS  Google Scholar 

  131. Fox PL (2003) The copper-iron chronicles: the story of an intimate relationship. Biometals 16:9–40

    Article  PubMed  CAS  Google Scholar 

  132. Sazinsky MH, LeMoine B, Orofino M et al (2007) Characterization and structure of a Zn2+ and [2Fe-2S]-containing copper chaperone from Archaeoglobus fulgidus. J Biol Chem 282:25950–25959

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  133. Schwarz G, Mendel RR (2006) Molybdenum cofactor biosynthesis and molybdenum enzymes. Annu Rev Plant Biol 57:623–647

    Article  PubMed  CAS  Google Scholar 

  134. Kuper J, Llamas A, Hecht HJ et al (2004) Structure of the molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism. Nature 430:803–806

    Article  PubMed  CAS  Google Scholar 

  135. Iobbi-Nivol C, Leimkuhler S (2013) Molybdenum enzymes, their maturation and molybdenum cofactor biosynthesis in Escherichia coli. Biochim Biophys Acta 1827:1086–1101

    Article  PubMed  CAS  Google Scholar 

  136. Morrison MS, Cobine PA, Hegg EL (2007) Probing the role of copper in the biosynthesis of the molybdenum cofactor in Escherichia coli and Rhodobacter sphaeroides. J Biol Inorg Chem 12:1129–1139

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department Clinical Research, University of Bern, Bern, Switzerland

    Marc Solioz

Authors
  1. Marc Solioz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marc Solioz .

Rights and permissions

Reprints and permissions

Copyright information

© 2018 The Author(s)

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Solioz, M. (2018). Copper Homeostasis in Gram-Negative Bacteria. In: Copper and Bacteria. SpringerBriefs in Molecular Science(). Springer, Cham. https://doi.org/10.1007/978-3-319-94439-5_4

Download citation

Publish with us

Policies and ethics

Search

Navigation