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The Copper Metallome in Prokaryotic Cells

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Metallomics and the Cell

Part of the book series: Metal Ions in Life Sciences ((MILS,volume 12))

Abstract

As a trace element copper has an important role in cellular function like many other transition metals. Its ability to undergo redox changes [Cu(I) ↔ Cu(II)] makes copper an ideal cofactor in enzymes catalyzing electron transfers. However, this redox change makes copper dangerous for a cell since it is able to be involved in Fenton-like reactions creating reactive oxygen species (ROS). Cu(I) also is a strong soft metal and can attack and destroy iron-sulfur clusters thereby releasing iron which can in turn cause oxidative stress. Therefore, copper homeostasis has to be highly balanced to ensure proper cellular function while avoiding cell damage.

Throughout evolution bacteria and archaea have developed a highly regulated balance in copper metabolism. While for many prokaryotes copper uptake seems to be unspecific, others have developed highly sophisticated uptake mechanisms to ensure the availability of sufficient amounts of copper. Within the cytoplasm copper is sequestered by various proteins and molecules, including specific copper chaperones, to prevent cellular damage. Copper-containing proteins are usually located in the cytoplasmic membrane with the catalytic domain facing the periplasm, in the periplasm of Gram-negative bacteria, or they are secreted, limiting the necessity of copper to accumulate in the cytoplasm. To prevent cellular damage due to excess copper, bacteria and archaea have developed various copper detoxification strategies. In this chapter we attempt to give an overview of the mechanisms employed by bacteria and archaea to handle copper and the importance of the metal for cellular function as well as in the global nutrient cycle.

Please cite as: Met. Ions Life Sci. 12 (2013) 417–450

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Abbreviations

ABC:

ATP-binding cassette

AMO:

ammonia monooxygenase

BLAST:

Basic Local Alignment Search Tool

BLASTP:

BLAST analysis searching protein databases using a protein query

COX:

cytochrome oxidase

Cu-AO:

copper-containing amine oxidase

CuNIR:

copper-containing nitrite reductase

EPR:

electron paramagnetic resonance

GSH:

glutathione

HCO:

heme-copper oxygen reductase

ITC:

isothermal titration colorimetry

MCO:

multicopper oxidase

MFP:

membrane fusion protein

MFS:

major facilitator superfamily

MMO:

methane monooxygenase

N2OR:

nitrous oxide reductase

NO:

nitric oxide

NOR:

nitric oxide reductase

NRAMP:

natural resistance-associated macrophage protein

OB:

oligonucleotide/oligosaccharide binding

OMF:

outermembrane factor

ORF:

open reading frame

pMMO:

particulate methane monooxygenase

RND:

resistance-nodulation cell division

ROS:

reactive oxygen species

Rpe:

ribulose-5-phosphate 3-epimerase

sMMO:

soluble methane monooxygenase

SOD:

superoxide dismutase

TAT:

twin-argininine translocation

TBLASTN:

BLAST analysis searching translated nucleotide databases using aprotein query

TMH:

transmembrane helix

TM-MBS:

transmembrane metal-binding site

TNC:

trinuclear cluster

TPQ:

trihydroxyphenylalanine

TRASH:

name of a metal-binding domain containing a well conserved cysteine motif

References

  1. K.T. Yasunobu, M. Tanaka, Syst. Zool. 1974, 22, 570–589.

    Article  Google Scholar 

  2. L. Macomber, J. A. Imlay, Proc. Natl. Acad. Sci. USA 2009, 106, 8344–8349.

    Google Scholar 

  3. F. F. Xu, J. A. Imlay, Appl. Environ. Microbiol. 2012, 78, 3614–361421.

    Article  PubMed  CAS  Google Scholar 

  4. C. L. Dupont, G. Grass, C. Rensing, Metallomics 2011, 3, 1109–1118.

    Article  PubMed  CAS  Google Scholar 

  5. C. Andreini, I. Bertini, A. Rosato, Acc. Chem. Res. 2009, 42, 1471–1479.

    Article  PubMed  CAS  Google Scholar 

  6. J. M. Arguello, J. Membr. Biol. 2003, 195, 93–108.

    CAS  Google Scholar 

  7. D. Raimunda, M. Gonzalez-Guerrero, B. W. Leeber, 3rd, J. M. Arguello, Biometals 2011, 24, 467–475.

    Article  PubMed  CAS  Google Scholar 

  8. N. J. Robinson, D. R. Winge, Annu. Rev. Biochem. 2010, 79, 537–562.

    Article  PubMed  CAS  Google Scholar 

  9. S. Tottey, C. J. Patterson, L. Banci, I. Bertini, I. C. Felli, A. Pavelkova, S.J. Dainty, R. Pernil, K. J. Waldron, A. W. Foster, N. J. Robinson, Proc. Natl. Acad. Sci. USA 2012, 109, 95–100.

    Google Scholar 

  10. S. Ekici, H. Yang, H. G. Koch, F. Daldal, MBio, 2012, 3, 10.1128/mBio.00293,11.

    Google Scholar 

  11. M. Gonzalez-Guerrero, J. M. Arguello, Proc. Natl. Acad. Sci. USA 2008, 105, 5992-5997.

    Google Scholar 

  12. J. M. Arguello, E. Eren, M. Gonzalez-Guerrero, Biometals 2007, 20, 233–248.

    Article  PubMed  CAS  Google Scholar 

  13. J. M. Arguello, M. Gonzalez-Guerrero, Structure 2008, 16, 833–834.

    Article  PubMed  CAS  Google Scholar 

  14. O. Lewinson, A. T. Lee, C. D. Rees, Proc. Natl. Acad. Sci. USA 2009, 106, 4677–4682.

    Google Scholar 

  15. Y. P. Tsai, H.T. Chen, Bioresour. Technol. 2011, 102, 11043–11047.

    Article  PubMed  CAS  Google Scholar 

  16. J. F. Lutkenhaus, J. Bacteriol. 1977, 131, 631–637.

    PubMed  CAS  Google Scholar 

  17. R. Balasubramanian, G. E. Kenney, A. C. Rosenzweig, J. Biol. Chem. 2011, 286, 37313–37319.

    CAS  Google Scholar 

  18. M. Mermod, D. Magnani, M. Solioz, J. V. Stoyanov, Biometals 2012, 25, 33–43.

    Article  PubMed  CAS  Google Scholar 

  19. G. Grass, S. Franke, N. Taudte, D. H. Nies, L. M. Kucharski, M. E. Maguire, C. Rensing, J. Bacteriol. 2005, 187, 1604–1611.

    Article  PubMed  CAS  Google Scholar 

  20. G. Grass, M. D. Wong, B. P. Rosen, R. L. Smith, C. Rensing, J. Bacteriol. 2002, 184, 864–866.

    Article  PubMed  CAS  Google Scholar 

  21. R. Janulczyk, J. Pallon, L. Bjorck, Mol. Microbiol. 1999, 34, 596–606.

    Article  PubMed  CAS  Google Scholar 

  22. J. S. Cavet, G. P. Borrelly, N. L. Robinson, FEMS Microbiol. Rev. 2003, 27, 165–181.

    CAS  Google Scholar 

  23. M. Solioz, J. V. Stoyanov, FEMS Microbiol. Rev. 2003, 27, 183–195.

    CAS  Google Scholar 

  24. K. Y. Djoko, Z. Xiao, D. L. Huffman, A. G. Wedd, Inorg. Chem. 2007, 46, 4560–4568

    Article  PubMed  CAS  Google Scholar 

  25. F. Arnesano, L. Banci, I. Bertini, I. C. Felli, C. Luchinat, A. R. Thompsett, J. Am. Chem. Soc. 2003, 125, 7200–7208.

    Article  PubMed  CAS  Google Scholar 

  26. F. Arnesano, L. Banci, I. Bertini, S. Mangani, A. R. Thompsett, Proc. Natl. Acad. Sci. USA 2003, 100, 3814–3819.

    Google Scholar 

  27. F. Arnesano, L. Banci, I. Bertini, A. R. Thompsett, Structure 2002, 10, 1337–1347.

    Article  PubMed  CAS  Google Scholar 

  28. S. Chillappagari, M. Miethke, H. Trip, O. P. Kuipers, M. A. Marahiel, J. Bacteriol. 2009 191, 2362–2370.

    Article  PubMed  CAS  Google Scholar 

  29. J. S. Cha, D. A. Cooksey, Appl. Environ. Microbiol. 1993, 59, 1671–1674.

    PubMed  CAS  Google Scholar 

  30. S. F. Altschul, T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, D. J. Lipman, Nucleic Acids Res. 1997, 25, 3389–3402.

    Article  PubMed  CAS  Google Scholar 

  31. Y. H. Hu, H. L. Wang, M. Zhang, L. Sun, J. Microbiol. 2009, 47, 277–286.

    Article  PubMed  CAS  Google Scholar 

  32. M.W. Fitch, D. W. Graham, R. G. Arnold, S. K. Agarwal, P. Phelps, G. E. Speitel Jr, G. Georgiou, Appl. Environ. Microbiol. 1993, 59, 2771–2776.

    PubMed  CAS  Google Scholar 

  33. J. A. Zahn, A. A. DiSpirito, J. Bacteriol. 1996, 178, 1018–1029.

    PubMed  CAS  Google Scholar 

  34. A. A. DiSpirito, J. A. Zahn, D. W. Graham, H. J. Kim, C. K. Larive, T. S. Derrick, C. D. Cox, A.Taylor, J. Bacteriol. 1998, 180, 3606–3613.

    PubMed  CAS  Google Scholar 

  35. H. J. Kim, D. W. Graham, A. A. DiSpirito, M. A. Alterman, N. Galeva, C. K. Larive, D. Asunskis, P. M. Sherwood, Science 2004, 305, 1612–1615.

    Article  PubMed  CAS  Google Scholar 

  36. J. Anttila, P. Heinonen, T. Nenonen, A. Pino, H. Iwai, E. Kauppi, R. Soliymani, M. Baumann, J. Saksi, N. Suni, T. Haltia, Biochim. Biophys. Acta 2011, 1807, 311–318.

    Article  CAS  Google Scholar 

  37. K. Nicolaisen, A. Hahn, M. Valdebenito, S. Moslavac, A. Samborski, I. Maldener, C. Wilken, A. Valladares, E. Flores, K. Hantke, E. Schleiff, Biochim. Biophys. Acta 2010, 1798, 2131–2140.

    Article  CAS  Google Scholar 

  38. J. Beaudoin, R. Ioannoni, L. Lopez-Maury, J. Bahler, S. Ait-Mohand, B. Guerin, S. C. Dodani, C. J. Chang, S. Labbe, J. Biol. Chem. 2011, 286, 34356–34372.

    CAS  Google Scholar 

  39. M. Gonzalez-Guerrero, D. Raimunda, X. Cheng, J. M. Arguello, Mol. Microbiol. 2010, 78, 1246–1258.

    Article  PubMed  CAS  Google Scholar 

  40. B. K. Hassani, C. Astier, W. Nitschke, S. Ouchane, J. Biol. Chem. 2010, 285, 19330–19337.

    CAS  Google Scholar 

  41. G. Grass, C. Rensing, Biochem. Biophys. Res. Commun. 2001, 286, 902–908.

    Article  PubMed  CAS  Google Scholar 

  42. F. W. Outten, C. E. Outten, J. Hale, T. V. O’Halloran, J. Biol. Chem. 2000, 275, 31024–31029

    CAS  Google Scholar 

  43. P. G. Ridge, Y. Zhang, V. N. Gladyshev, PLoS One 2008, 3, e1378.

    Article  PubMed  CAS  Google Scholar 

  44. F. L. Sousa, R. J. Alves, M. A. Ribeiro, J. B. Pereira-Leal, M.Teixeira, M. M. Pereira, Biochim. Biophys. Acta 2012, 1817, 629–637.

    Article  CAS  Google Scholar 

  45. F. L. Sousa, R. J. Alves, J. B. Rereira-Leal, M. Teixeira, M. M. Pereira, A Bioinformatics Classifier and Database for Heme-Copper Oxygen Reductases, PLoS One 2011. 6, e19117.

    Article  PubMed  CAS  Google Scholar 

  46. E. Frangipani, D. Haas, FEMS Microbiol. Lett. 2009, 298, 234–240.

    CAS  Google Scholar 

  47. D. L. Swem, L. R. Swem, A. Setterdahl, C. E. Bauer, J. Bacteriol. 2005, 187, 8081–8087.

    Article  PubMed  CAS  Google Scholar 

  48. D. Buhler, R. Rossmann, S. Landolt, S. Balsiger, H. M. Fischer, H. Hennecke, J. Biol. Chem. 2010, 285, 15704–15713.

    CAS  Google Scholar 

  49. F. Arnesano, L. Banci, I. Bertini, M. Martinelli, J. Proteome Res. 2005, 4, 63–70.

    Google Scholar 

  50. Y. V. Chinenov, J. Mol. Med. 2000, 78, 239–242.

    CAS  Google Scholar 

  51. E. Balatri, L. Banci, I. Bertini, F. Cantini, S. Ciofi-Baffoni, Structure 2003, 11, 1431-1443

    Article  PubMed  CAS  Google Scholar 

  52. G. S. Siluvai, M. Mayfield, M. J. Nilges, S. Debeer George, N. J. Blackburn, J. Am. Chem. Soc. 2010, 132, 5215–5226.

    Article  PubMed  CAS  Google Scholar 

  53. G. S. Siluvai, M. Nakano, M. Mayfield, N. J. Blackburn, J. Biol. Inorg. Chem. 2011, 16, 285–297.

    Article  PubMed  CAS  Google Scholar 

  54. G. S. Siluvai, M. M. Nakano, M. Mayfield, M. J. Nilges, N. J. Blackburn, Biochemistry 2009, 48, 12133–12144.

    Article  PubMed  CAS  Google Scholar 

  55. L. Banci, I. Bertini, G. Cavallaro, S. Ciofi-Baffoni, FEBS J. 2011, 278, 2244–2262.

    Article  PubMed  CAS  Google Scholar 

  56. D. J. Kosman, J. Biol. Inorg. Chem. 2010, 15, 15–28.

    Article  PubMed  CAS  Google Scholar 

  57. T. Sakurai, K. Kataoka, Chem. Rec. 2007, 7, 220–229.

    Article  PubMed  CAS  Google Scholar 

  58. H. Claus, Arch. Microbiol. 2003, 179, 145–150.

    PubMed  CAS  Google Scholar 

  59. S. Uthandi, B. Saad, M. A. Humbard, J. A. Maupin-Furlow, Appl. Environ. Microbiol. 2010, 76, 733–743.

    Article  PubMed  CAS  Google Scholar 

  60. H. Claus, Micron 2004, 35, 93–96.

    Article  PubMed  CAS  Google Scholar 

  61. M. Ferrer, A. Beloqui, P.N. Golyshin, Methods Mol. Biol. 2010, 668, 189–202.

    CAS  Google Scholar 

  62. A. Piscitelli, C. Pezzella, P. Giardina, V. Faraco, S. Giovanni, Bioeng. Bugs 2010, 1, 252–262

    Google Scholar 

  63. G. Grass, C. Rensing, J. Bacteriol. 2001, 183, 2145–2147.

    Article  PubMed  CAS  Google Scholar 

  64. S. A. Roberts, A. Weichsel, G. Grass, K. Thakali, J. T. Hazzard, G. Tollin, C. Rensing, W. R. Montfort, Proc. Natl. Acad. Sci. USA 2002, 99, 2766–2771.

    Google Scholar 

  65. S. A. Roberts, G. F. Wildner, G. Grass, A. Weichsel, A. Ambrus, C. Rensing, W. R. Montfort, J. Biol. Chem. 2003, 278, 31958–31963.

    CAS  Google Scholar 

  66. G. Grass, K. Thakali, P. E. Klebba, D. Thieme, A. Muller, G. F. Wildner, C. Rensing, J. Bacteriol. 2004, 186, 5826–5833.

    Article  PubMed  CAS  Google Scholar 

  67. S. K. Singh, G. Grass, C. Rensing, W. R. Montfort, J. Bacteriol. 2004, 186, 7815–7817.

    Article  PubMed  CAS  Google Scholar 

  68. K. Y. Djoko, X. L. Chong, A. G. Wedd, Z. Xiao, J. Am. Chem. Soc. 2010, 132, 2005–2015.

    Article  PubMed  CAS  Google Scholar 

  69. S. K. Singh, S. A. Roberts, S. F. McDevitt, A. Weichsel, G. F. Wildner, G. B. Grass, C. Rensing, W. R. Montfort, J. Biol. Chem. 2011, 286, 37849–37857.

    CAS  Google Scholar 

  70. S. Y. Lim, M. H. Joe, S. S. Song, M. H. Lee, J. W. Foster, Y. K. Park, S. Y. Choi, I. S. Lee, Mol. Cells 2002, 14, 177–184.

    Google Scholar 

  71. M. E. Achard, J. J. Tree, J. A. Holden, K. R. Simpfendorfer, O. L. Wijburg, R. A. Strugnell, M. A. Schembri, M. J. Sweet, M. P. Jennings, A. G. McEwan, Infect. Immun. 2010, 78, 2312–2319.

    Article  PubMed  CAS  Google Scholar 

  72. H. B. Gray, B. G. Malmstrom, R. J. P. Williams, J. Biol. Inorg. Chem. 2000, 5, 551–559.

    Article  PubMed  CAS  Google Scholar 

  73. F. De Rienzo, R. R. Gabdoulline, M. C. Menziani, R. C. Wade, Protein Sci. 2000, 9, 1439–1454.

    Article  PubMed  Google Scholar 

  74. Z. W. Chen, M. J. Barber, W. S. McIntire, F. S. Mathews,. Acta Crystallogr. D Biol. Crystallogr. 1998, 54, 253–268.

    Article  CAS  Google Scholar 

  75. J. Elguindi, J. Wagner, C. Rensing, J. Appl. Microbiol. 2009, 106, 1448–1455.

    CAS  Google Scholar 

  76. P. Pietrangeli, S. Nocera, B. Mondovi, L. Morpurgo, Biochim. Biophys. Acta 2003, 1647, 152–156.

    Article  CAS  Google Scholar 

  77. M. C. Wilce, D. M. Dooley, H. C. Freeman, J. M. Guss, H. Matsunami, W. S. McIntire, C. E. Ruggiero, K. Tanizawa, H. Yamaguchi, Biochemistry 1997, 36, 16116–16133.

    Article  PubMed  CAS  Google Scholar 

  78. H. C. Dawkes, S. E. Phillips, Curr. Opin. Struct. Biol. 2001, 11, 666–673.

    Article  PubMed  CAS  Google Scholar 

  79. M. Kataoka, H. Oya, A. Tominaga, M. Otsu, T. Okajima, K. Tanizawa, H. Yamaguchi, J. Synchrotron Radiat. 2011, 18, 58–61.

    Google Scholar 

  80. R. S. Hanson, T. E. Hanson, Microbiol. Rev. 1996, 60, 439–471.

    PubMed  CAS  Google Scholar 

  81. A. K. Nielsen, K. Gerdes, J. C. Murrell, Mol. Microbiol. 1997, 25, 399–409.

    Article  PubMed  CAS  Google Scholar 

  82. J. C. Murrell, I. R. McDonald, B. Gilbert, Trends Microbiol. 2000, 8, 221–225.

    Article  PubMed  CAS  Google Scholar 

  83. H. H. Nguyen, S. J. Elliott, J. H. Yip, S. I. Chan, J. Biol. Chem. 1998, 273, 7957–7966.

    CAS  Google Scholar 

  84. J. D. Semrau, D. Zolandz, M. E. Lidstrom, S. I. Chan, J. Inorg. Biochem. 1995, 58, 235–244.

    CAS  Google Scholar 

  85. C. W. Knapp, D. A. Fowle, E. Kulczycki, J. A. Roberts, D. W. Graham, Proc. Natl. Acad. Sci. USA 2007, 104, 12040–12045.

    Google Scholar 

  86. R. L. Lieberman, A. C. Rosenzweig, Nature 2005, 434, 177–182.

    Article  PubMed  CAS  Google Scholar 

  87. A. S. Hakemian, K. C. Kondapalli, J. Telser, B. M. Hoffman, T. L. Stemmler, A. C. Rosenzweig, Biochemistry 2008, 47, 6793–6801.

    Article  PubMed  CAS  Google Scholar 

  88. S. M. Smith, S. Rawat, J. Telser, B. M. Hoffman, T. L. Stemmler, A. C. Rosenzweig, Biochemistry 2011, 50, 10231–10240.

    Article  PubMed  CAS  Google Scholar 

  89. R. Balasubramanian, S. M. Smith, S. Rawat, L. A. Yatsunyk, T. L. Stemmler, A. C. Rosenzweig, Nature 2010, 465, 115–119.

    Article  PubMed  CAS  Google Scholar 

  90. J. M. Bollinger Jr., Nature 2010, 465, 40–41.

    Article  PubMed  CAS  Google Scholar 

  91. R. A. Himes, K. Barnese, K. D. Karlin, Angew. Chem. Int. Ed Engl. 2010, 49, 6714–6716.

    Google Scholar 

  92. R. M. Martinez-Espinosa, J. A. Cole, D. J. Richardson, N. J. Watmough, Biochem. Soc. Trans. 2011, 39, 175–178.

    Article  PubMed  CAS  Google Scholar 

  93. B. Kraft, M. Strous, H. E. Tegetmeyer, J. Biotechnol. 2011, 155, 104–117.

    Article  PubMed  CAS  Google Scholar 

  94. W. G. Zumft, Microbiol. Mol. Biol. Rev. 1997, 61, 533–616.

    PubMed  CAS  Google Scholar 

  95. S. A. Ensign, M. R. Hyman, D. J. Arp, J. Bacteriol. 1993, 175, 1971–1980.

    PubMed  CAS  Google Scholar 

  96. I. Schmidt, E. Bock, Antonie Van Leeuwenhoek 1998, 73, 271–278.

    Article  PubMed  CAS  Google Scholar 

  97. S. Gilch, O. Meyer, I. Schmidt, Biol. Chem. 2009, 390, 863–873.

    Article  PubMed  CAS  Google Scholar 

  98. S. Gilch, O. Meyer, I. Schmidt, Biometals 2010, 23, 613–622.

    Article  PubMed  CAS  Google Scholar 

  99. M. B. Lund, J. M. Smith, C.A. Francis, ISME J. 2012, doi: 10.1038/ismej.2012.40. [Epub ahead of print]

    Google Scholar 

  100. H. Iwasaki, S. Shidara, H. Suzuki, T. Mori, J. Biochem. 1963, 53, 299–303.

    PubMed  CAS  Google Scholar 

  101. I. M. Wasser, S. de Vries, P. Moenne-Loccoz, I. Schroder, K. D. Karlin, KD. Chem. Rev. 2002, 102, 1201–1234.

    Article  CAS  Google Scholar 

  102. E. T. Adman, W. J. Godden, S. Turley, J. Biol. Chem. 1995, 270, 27458–27474.

    CAS  Google Scholar 

  103. M. E. Murphy, S. Turley, E. T. Adman, J. Biol. Chem. 1997, 272, 28455–28460.

    CAS  Google Scholar 

  104. J. A. Farrar, A. J. Thomson, M. R. Cheesman, M. D. Dooley, W. G. Zumft, FEBS Lett. IB 1991 , 294, 11–15.

    CAS  Google Scholar 

  105. T. Rasmussen, B. C. Berks, J. Sanders-Loehr, M.D. Dooley, W. G. Zumft, A. J. Thomson, Biochemistry 2000, 39, 12753–12756.

    Article  PubMed  CAS  Google Scholar 

  106. T. Haltia, K. Brown, M. Tegoni, C. Cambillau, M. Saraste, K. Mattila, K. Djinovic-Carugo, Biochem. J. 2003, 369, 77–88.

    Article  PubMed  CAS  Google Scholar 

  107. W. G. Zumft, H. Korner, Antonie Van Leeuwenhoek 1997, 71, 43–58.

    Article  PubMed  CAS  Google Scholar 

  108. P. Wunsch, M. Herb, H. Wieland, U. M. Schiek, W. G. Zumft, J. Bacteriol. 2003, 185, 887–896.

    Article  PubMed  CAS  Google Scholar 

  109. A. Pomowski, W. G. Zumft, P. M. Kroneck, O. Einsle, Nature 2011, 477, 234–237.

    Article  PubMed  CAS  Google Scholar 

  110. J. Ollivier, S. Towe, A. Bannert, B. Hai, E.M. Kastl, A. Meyer, M. X. Su, K. Kleineidam, M. Schloter, FEMS Microbiol. Ecol. 2011, 78, 3–16.

    CAS  Google Scholar 

  111. J. H. Fan, L. M. Ma, J. Hazard. Mater. 2009, 164, 1392–1397.

    CAS  Google Scholar 

  112. V. Ochoa-Herrera, G. Leon, Q. Banihani, J. A. Field, R. Sierra-Alvarez, Sci. Total Environ. 2011, 412-413, 380–385.

    Google Scholar 

  113. M. Solioz, C. Vulpe, Trends Biochem. Sci. 1996, 21, 237–241.

    CAS  Google Scholar 

  114. A. Odermatt, H. Suter, R. Krapf, M. Solioz, Ann. N. Y. Acad. Sci. 1992, 671, 484–486.

    Article  PubMed  CAS  Google Scholar 

  115. M. Solioz, A. Odermatt, R. Krapf, FEBS Lett. 1994, 346, 44–47.

    Article  PubMed  CAS  Google Scholar 

  116. J. M. Arguello, A. K. Mandal, S. Mana-Capelli, Ann. N. Y. Acad. Sci. 2003, 986, 212–218.

    Article  PubMed  CAS  Google Scholar 

  117. M. Solioz, A. Odermatt, J. Biol. Chem. 1995, 270, 9217–9221.

    CAS  Google Scholar 

  118. C. Rensing, B. Fan, R. Sharma, B. Mitra, B. P. Rosen, Proc. Natl. Acad. Sci. USA 2000, 97, 652–656.

    Google Scholar 

  119. T. J. Ettema, A. B. Brinkman, P. P. Lamers, N. G. Kornet, W. M. de Vos, J. van der Oost, Microbiology 2006, 152, 1969–1979.

    Article  PubMed  CAS  Google Scholar 

  120. A. K. Mandal, W. D. Cheung, J. M. Arguello, J. Biol. Chem. 2002 , 277, 7201–7208.

    CAS  Google Scholar 

  121. J. M. Arguello, M. Gonzalez-Guerrero, D. Raimunda, Biochemistry 2011, 50, 9940–9949.

    Article  PubMed  CAS  Google Scholar 

  122. C. Rensing, S. Franke, in EcoSal. ( www.ecosal.org.), Eds R. I. Curtiss, J. B. Kaper, C. L. Squires, P. D. Karp, F. C. Neidhardt, J. M. Slauch, ASM Press, Washington, DC, 2007.

    Google Scholar 

  123. R. De la Iglesia, D. Valenzuela-Heredia, J. P. Pavissich, S. Freyhoffer, S. Andrade, J. A. Correa, B. Gonzalez, Lett. Appl. Microbiol. 2010, 50, 552–562.

    Article  PubMed  CAS  Google Scholar 

  124. B. Fan, B. P. Rosen, J. Biol. Chem. 2002, 277, 46987–46992.

    CAS  Google Scholar 

  125. A. Odermatt, R. Krapf, M. Solioz, Biochem. Biophys. Res. Commun. 1994, 202, 44–48.

    Article  PubMed  CAS  Google Scholar 

  126. L. Banci, I. Bertini, S. Ciofi-Baffoni, R. Del Conte, L. Gonnelli, Biochemistry 2003, 42, 1939–1949.

    Article  PubMed  CAS  Google Scholar 

  127. D. S. Radford, M.A. Kihlken, G. P. Borrelly, C. R. Harwood, N. E. Le Brun, J. S. Cavet, FEMS Microbiol. Lett. 2003, 220, 105–112.

    CAS  Google Scholar 

  128. M. Gonzalez-Guerrero, D. Hong, J. M. Arguello, J. Biol. Chem. 2009, 284, 20804–20811.

    CAS  Google Scholar 

  129. S. Mana-Capelli, A. K. Mandal, J. M. Arguello, J. Biol. Chem. 2003, 278, 40534–40541.

    CAS  Google Scholar 

  130. G. P. Munson, D. L. Lam, F. W. Outten, T. V. O’Halloran, J. Bacteriol. 2000, 182, 5864–5871.

    Article  PubMed  CAS  Google Scholar 

  131. A. Gupta, K. Matsui, J. F. Lo, S. Silver, Nat. Med. 1999, 5, 183–188.

    Article  PubMed  CAS  Google Scholar 

  132. S. Franke, G. Grass, D. H. Nies, Microbiology 2001, 147, 965–972.

    PubMed  CAS  Google Scholar 

  133. S. Franke, G. Grass, C. Rensing, D. H. Nies, J. Bacteriol. 2003, 185, 3804–3812.

    Article  PubMed  CAS  Google Scholar 

  134. D. H. Nies, S. Silver, J. Ind. Microbiol. 1995, 14, 186–199.

    CAS  Google Scholar 

  135. I. T. Paulsen, M. H. Brown, R. A. Skurray, Microbiol. Rev. 1996, 60, 575–608.

    PubMed  CAS  Google Scholar 

  136. M. H. Saier Jr., R. Tam, A. Reizer, J. Reizer, Mol. Microbiol. 1994 11, 841–847.

    Article  PubMed  CAS  Google Scholar 

  137. I. R. Loftin, S. Franke, S. A. Roberts, A. Weichsel, A. Heroux, W. R. Montfort, C. Rensing, M. M. McEvoy, Biochemistry 2005 44, 10533–10540.

    Article  PubMed  CAS  Google Scholar 

  138. E. H. Kim, C. Rensing, M. M. McEvoy, Nat. Prod. Rep. 2010, 27, 711–719.

    Article  PubMed  CAS  Google Scholar 

  139. J. T. Kittleson, I. R. Loftin, A. C. Hausrath, K. P. Engelhardt, C. Rensing, M. M. McEvoy, Biochemistry 2006, 45, 11096–11102.

    Article  PubMed  CAS  Google Scholar 

  140. I. R. Loftin, S. Franke, N. J. Blackburn, M. M. McEvoy, Protein Sci. 2007 16, 2287–2293.

    Article  PubMed  CAS  Google Scholar 

  141. Y. Xue, A. V. Davis, G. Balakrishnan, J. P. Stasser, B. M. Staehlin, P. Focia, T. G. Spiro, J. E. Penner-Hahn, T. V. O’Halloran, Nat. Chem. Biol. 2008, 4, 107–109.

    Article  PubMed  CAS  Google Scholar 

  142. I. R. Loftin, N. J. Blackburn, M. M. McEvoy, J. Biol. Inorg. Chem. 200, 14, 905–912.

    Google Scholar 

  143. T. D. Mealman, I. Bagai, P. Singh, D. R. Goodlett, C. Rensing, H. Zhou, V. H. Wysocki, M. M. McEvoy, Biochemistry 2011, 50, 2559–2566.

    Article  PubMed  CAS  Google Scholar 

  144. I. Bagai, C. Rensing, N. J. Blackburn, M. M. McEvoy, Biochemistry 2008, 47, 11408–11414.

    Article  PubMed  CAS  Google Scholar 

  145. F. Long, C. C. Su, H. T. Lei, J. R. Bolla, S. V. Do, E. W. Yu, Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2012, 367, 1047–1058.

    Article  PubMed  CAS  Google Scholar 

  146. R. Kulathila, R. Kulathila, M. Indic, B. van den Berg, PLoS One 2011, 6, e15610.

    Article  PubMed  CAS  Google Scholar 

  147. V. Koronakis, A. Sharff, E. Koronakis, B. Luisi, C. Hughes, Nature 2000, 405, 914–919.

    Article  PubMed  CAS  Google Scholar 

  148. C. C. Su, F. Yang, F. Long, D. Reyon, M. D. Routh, D. W. Kuo, A. K. Mokhtari, J. D. Van Ornam, K. L. Rabe, J. A. Hoy, Y. J. Lee, K. R. Rajashankar, E. W. Yu, J. Mol. Biol. 2009, 393, 342–355.

    CAS  Google Scholar 

  149. H. Akama, T. Matsuura, S. Kashiwagi, H. Yoneyama, S. Narita, T. Tsukihara, A. Nakagawa, T. Nakae, J. Biol. Chem. 2004, 279, 25939–25942.

    CAS  Google Scholar 

  150. F. Long, C. C. Su, M. T. Zimmermann, S. E. Boyken, K. R. Rajashankar, R. L. Jernigan, E. W. Yu, Nature 2010, 467, 484–488.

    Article  PubMed  CAS  Google Scholar 

  151. C. C. Su, F. Long, M. T. Zimmermann, K. R. Rajashankar, R. L. Jernigan, E. W. Yu, Nature 2011, 470, 558–562.

    Article  PubMed  CAS  Google Scholar 

  152. I. Bagai, W. Liu, C. Rensing, N. J. Blackburn, M. M. McEvoy, J. Biol. Chem. 2007, 282, 35695–35702.

    CAS  Google Scholar 

  153. E. H. Kim, D.H. Nies, M. M. McEvoy, C. Rensing, J. Bacteriol. 2011, 193, 2381–2387.

    Article  PubMed  CAS  Google Scholar 

  154. L. B. Pontel, F. C. Soncini, Mol. Microbiol. 2009, 73, 212–225.

    Article  PubMed  CAS  Google Scholar 

  155. F. W. Outten, D. L. Huffman, J. A. Hale, T. V. O’Halloran, J. Biol. Chem. 2001, 276, 30670–30677.

    CAS  Google Scholar 

  156. B. Y. Yun, S. Piao, Y. G. Kim, H. R. Moon, E. J. Choi, Y. O. Kim, B. H. Nam, S. J. Lee, N. C. Ha, Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 2011, 67, 675–677.

    Article  CAS  Google Scholar 

  157. S. Elsen, M. Ragno, I. Attree, J. Bacteriol. 2011, 193, 3376–3378.

    Article  PubMed  CAS  Google Scholar 

  158. N. L. Brown, S. R. Barrett, J. Camakaris, B. T. Lee, D. A. Rouch, Mol. Microbiol. 1995, 17, 1153–1166.

    Article  PubMed  CAS  Google Scholar 

  159. S. M. Lee, G. Grass, C. Rensing, S. R. Barrett, C. J. Yates, J. V. Stoyanov, N. L. Brown, Biochem. Biophys. Res. Commun. 2002, 295, 616–620.

    Article  PubMed  CAS  Google Scholar 

  160. S. Monchy, M. A. Benotmane, R. Wattiez, S. van Aelst, V. Auquier, B. Borremans, M. Mergeay, S. Taghavi, D. van der Lelie, T. Vallaeys, Microbiology 2006, 152, 1765–1776.

    Article  PubMed  CAS  Google Scholar 

  161. V. Sendra, D. Cannella, B. Bersch, F. Fieschi, S. Menage, D. Lascoux, J. Coves, Biochemistry 2006, 45, 5557–5566.

    Article  PubMed  CAS  Google Scholar 

  162. B. Bersch, A. Favier, P. Schanda, S. van Aelst, T. Vallaeys, J. Coves, M. Mergeay, R. Wattiez, J. Mol. Biol. 2008, 380, 386–403.

    CAS  Google Scholar 

  163. V. Sendra, S. Gambarelli, B. Bersch, J. Coves, J. Inorg. Biochem. 2009, 103, 1721–1728.

    CAS  Google Scholar 

  164. C. Grosse, A. Anton, T. Hoffmann, S. Franke, G. Schleuder, D. H. Nies, Arch. Microbiol. 2004, 182, 109–118.

    Article  PubMed  CAS  Google Scholar 

  165. A. Zoropogui, S. Gambarelli, J. Coves, Biochem. Biophys. Res. Commun. 2008, 365, 735–739.

    Article  PubMed  CAS  Google Scholar 

  166. I. Petit-Haertlein, E. Girard, G. Sarret, J. L. Hazemann, P. Gourhant, R. Kahn, J. Coves, Biochemistry 2010, 49, 1913–1922.

    Article  PubMed  CAS  Google Scholar 

  167. K. Marrero, A. Sanchez, L. J. Gonzalez, T. Ledon, A. Rodriguez-Ulloa, L. Castellanos-Serra, C. Perez, R. Fando, Microbiology 2012, Epub ahead of print.

    Google Scholar 

  168. T. J. Tetaz, R. K. Luke, J. Bacteriol. 1983, 154, 1263–1268.

    PubMed  CAS  Google Scholar 

  169. J. S. Cha, D. A. Cooksey, Proc. Natl. Acad. Sci. USA 1991, 88, 8915–8919.

    Google Scholar 

  170. M. A. Mellano, D. A. Cooksey, J. Bacteriol. 1988, 170, 2879–2883.

    PubMed  CAS  Google Scholar 

  171. D. A. Cooksey, Mol. Microbiol. 1993, 7, 1–5.

    Article  PubMed  CAS  Google Scholar 

  172. S. Puig, E. M. Rees, D. J. Thiele, Structure 2002, 10, 1292–1295.

    Article  PubMed  CAS  Google Scholar 

  173. C. Petersen, L. B. Moller, Gene 2000, 261, 289–298.

    Article  PubMed  CAS  Google Scholar 

  174. A. Changela, K. Chen, Y. Xue, J. Holschen, C. E. Outten, T. V. O’Halloran, A. Mondragon, Science 2003, 301, 1383–1387.

    Article  PubMed  CAS  Google Scholar 

  175. J. V. Stoyanov, J. L. Hobman, N. L. Brown, Mol. Microbiol. 2001, 39, 502–511.

    Article  PubMed  CAS  Google Scholar 

  176. V. Adaikkalam, S. Swarup, Microbiology 2002, 148, 2857–2867.

    PubMed  CAS  Google Scholar 

  177. V. Peuser, J. Glaeser, G. Klug, Microbiology 2011, 157, 3306–3313.

    Article  PubMed  CAS  Google Scholar 

  178. N. R. Williamson, H. T. Simonsen, A. K. Harris, F. J. Leeper, G. P. Salmond, J. Ind. Microbiol. Biotechnol. 2006, 33, 151–158.

    Article  PubMed  CAS  Google Scholar 

  179. W. G. Reeve, R. P. Tiwari, N. B. Kale, M. J. Dilworth, A. R. Glenn, Mol. Microbiol. 2002, 43, 981–991.

    Article  PubMed  CAS  Google Scholar 

  180. D. J. Julian, C. J. Kershaw, N. L. Brown, J. L. Hobman, Antonie van Leeuwenhoek 2009, 96, 149–159.

    Article  PubMed  CAS  Google Scholar 

  181. A. Villafane, Y. Voskoboynik, I. Ruhl, D. Sannino, Y. Maezato, P. Blum, E. Bini, Microbiology 2011, 157, 2808–2817.

    Article  PubMed  CAS  Google Scholar 

  182. A. Odermatt, M. Solioz, J. Biol. Chem. 1995, 270, 4349–4354.

    CAS  Google Scholar 

  183. D. Strausak, M. Solioz, J. Biol. Chem. 1997, 272, 8932–8936.

    CAS  Google Scholar 

  184. D. Magnani, M. Solioz, Biometals 2005, 18, 407–412.

    Article  PubMed  CAS  Google Scholar 

  185. P. A. Cobine, G. N. George, C. E. Jones, W. A. Wickramasinghe, M. Solioz, C. T. Dameron, Biochemistry 2002, 41, 5822–5829.

    Article  PubMed  CAS  Google Scholar 

  186. P. A. Cobine, C. E. Jones, C. T. Dameron, J. Inorg. Biochem. 2002, 88, 192–196.

    CAS  Google Scholar 

  187. R. Portmann, K. R. Poulsen, R. Wimmer, M. Solioz, Biometals 2006, 19, 61–70.

    Article  PubMed  CAS  Google Scholar 

  188. H. Wunderli-Ye, M. Solioz, Biochem. Biophys. Res. Commun. 1999, 259, 443–449.

    Article  PubMed  CAS  Google Scholar 

  189. G. Multhaup, D. Strausak, K. D. Bissig, M. Solioz, Biochem. Biophys. Res. Commun. 2001, 288, 172–177.

    Article  PubMed  CAS  Google Scholar 

  190. R. Portmann, D. Magnani, J. V. Stoyanov, A. Schmechel, G. Multhaup, M. Solioz, J. Biol. Inorg. Chem. 2004, 9, 396–402.

    Article  PubMed  CAS  Google Scholar 

  191. P. Cobine, W. A. Wickramasinghe, M. D. Harrison, T. Weber, M. Solioz, C. T. Dameron, FEBS Lett. 1999, 445, 27–30.

    Article  PubMed  CAS  Google Scholar 

  192. F. Cantini, L. Banci, M. Solioz, Biochem. J. 2009, 417, 493–499.

    Article  PubMed  CAS  Google Scholar 

  193. A. Reyes, A. Leiva, V. Cambiazo, M. A. Mendez, M. Gonzalez, Biol. Res. 2006, 39, 87–93.

    Article  PubMed  CAS  Google Scholar 

  194. S. Shafeeq, H. Yesilkaya, T. G. Kloosterman, G. Narayanan, M. Wandel, P. W. Andrew, O. P. Kuipers, J. A. Morrissey, Mol. Microbiol. 2011, 81, 1255–1270.

    Article  PubMed  CAS  Google Scholar 

  195. T. Liu, S. Nakashima, K. Hirose, M. Shibasaka, M. Katsuhara, B. Ezaki, D. P. Giedroc, K. Kasamo, J. Biol. Chem. 2004, 279, 17810–17818.

    CAS  Google Scholar 

  196. T. Liu, X. Chen, Z. Ma, J. Shokes, L. Hemmingsen, R. A. Scott, D. P. Giedroc, Biochemistry 2008, 47, 10564–10575.

    Article  PubMed  CAS  Google Scholar 

  197. T. Liu, A. Ramesh, Z. Ma, S. K. Ward, L. Zhang, G. N. George, A. M. Talaat, J. C. Sacchettini, D. P. Giedroc, Nat. Chem. Biol. 2007, 3, 60–68.

    Article  PubMed  CAS  Google Scholar 

  198. D. Corbett, S. Schuler, S. Glenn, P. W. Andrew, J. S. Cavet, I. S. and Roberts, Mol. Microbiol. 2011, 81, 457–472.

    Google Scholar 

  199. G. T. Smaldone, J. D. Helmann, Microbiology 2007, 153, 4123–4128.

    Article  PubMed  CAS  Google Scholar 

  200. K. Sakamoto, Y. Agari, K. Agari, S. Kuramitsu, A. Shinkai, Microbiology 2010, 156, 1993–2005.

    Article  PubMed  CAS  Google Scholar 

  201. J. Baker, M. Sengupta, R. K. Jayaswal, J. A. Morrissey, Environ. Microbiol. 2011, 13, 2495–2507.

    Article  PubMed  CAS  Google Scholar 

  202. S. Dwarakanath, A. K. Chaplin, M. A. Hough, S. Rigali, E. Vijgenboom, J. A. Worrall, J. Biol. Chem. 2012, 287, 17833–17847.

    CAS  Google Scholar 

  203. Z. Ma, D. M. Cowart, R. A. Scott, D. P. Giedroc, Biochemistry 2009, 48, 3325–3334.

    Article  PubMed  CAS  Google Scholar 

  204. S. D. Mills, C. A. Jasalavich, D. A. Cooksey, J. Bacteriol. 1993, 175, 1656–1664.

    PubMed  CAS  Google Scholar 

  205. C. K. Lim, D. A. Cooksey, J. Bacteriol. 1993, 175, 4492–4498.

    PubMed  CAS  Google Scholar 

  206. D. A. Rouch, N. L. Brown, Microbiology 1997, 143 ( Pt 4), 1191–1202.

    Article  PubMed  CAS  Google Scholar 

  207. C. Q. Liu, P. Charoechai, N. Khunajakr, Y. M. Deng, Widodo, N. W. Dunn, Gene 2002, 297, 241–247.

    Google Scholar 

  208. S. Jang, J. A. Imlay, J. Biol. Chem. 2007, 282, 929–937.

    CAS  Google Scholar 

  209. C. E. Bagwell, K. K. Hixson, C. E. Milliken, D. Lopez-Ferrer, K. K. Weitz, PLoS One 2010, 5, e12427.

    Article  PubMed  CAS  Google Scholar 

  210. A. Anjem, S. Varghese, J. A. Imlay, Mol. Microbiol. 2009, 72, 844–858.

    Article  PubMed  CAS  Google Scholar 

  211. J. M. Sobota, J. A. Imlay, Proc. Natl. Acad. Sci. USA 2011, 108, 5402–5407.

    Google Scholar 

  212. J. S. Davila Costa, V. H. Albarracin, C. M. Abate, Ecotoxicol. Environ. Saf. 2011, 74, 2020–2028.

    Article  PubMed  CAS  Google Scholar 

  213. H. Qian, S. Yu, Z. Sun, X. Xie, W. Liu, Z. Fu, Aquat. Toxicol. 2010, 99, 405–412.

    Article  PubMed  CAS  Google Scholar 

  214. C. J. Kershaw, N. L. Brown, C. Constantinidou, M. D. Patel, J. L Hobman, Microbiology 2005, 151, 1187–1198.

    Google Scholar 

  215. K. Yamamoto, A. Ishihama, Mol. Microbiol. 2005, 56, 215–227.

    Article  PubMed  CAS  Google Scholar 

  216. S. K. Ward, E. A. Hoye, A. M. Talaat, J. Bacteriol. 2008, 190, 2939–2946.

    Article  PubMed  CAS  Google Scholar 

  217. G. M. Teitzel, A. Geddie, S. K. De Long, M. J. Kirisits, M. Whiteley, M. R. Parsek, J. Bacteriol. 2006, 188, 7242–7256.

    Article  PubMed  CAS  Google Scholar 

  218. M. R. Ash, L. X. Chong, M. J. Maher, M. G. Hinds, Z. Xiao, A. G. Wedd, Biochemistry 2011 , 50, 9237–9247.

    Article  PubMed  CAS  Google Scholar 

  219. G. Sarret, A. Favier, J. Coves, J. L. Hazemann, M. Mergeay, B. Bersch, J. Am. Chem. Soc. 2010, 132, 3770–3777.

    Article  PubMed  CAS  Google Scholar 

  220. J. Trepreau, E. de Rosny, C. Duboc, G. Sarret, I. Petit-Hartlein, A. P. Maillard, A. Imberty, O. Proux, J. Coves, Biochemistry 2011, 50, 9036–9045.

    Article  PubMed  CAS  Google Scholar 

  221. M. F. Cellier, P. Courville, C. Campion, Microbes Infect. 2007, 9, 1662–1670.

    Article  PubMed  CAS  Google Scholar 

  222. V. Hodgkinson, M. J. Petris, J. Biol. Chem. 2012, 287, 13549–13555.

    CAS  Google Scholar 

  223. H. Botella, G. Stadthagen, G. Lugo-Villarino, C. de Chastellier, O. Neyrolles, Trends Microbiol. 2012, 20, 106–112.

    Article  PubMed  CAS  Google Scholar 

  224. L. Decaria, I. Bertini, R. J. P. Williams, Metallomics 2011, 3, 56–60.

    Article  PubMed  CAS  Google Scholar 

  225. C. White, J. Lee, T. Kambe, K. Fritsche, M. J. Petris, J. Biol. Chem. 2009, 284, 33949–33956.

    CAS  Google Scholar 

  226. J. S. Klein, O. Lewinson, Metallomics 2011, 3, 1098–1108.

    Article  PubMed  CAS  Google Scholar 

  227. E. A. Cho, J. Seo, D. W. Lee, J. G. Pan, Enzyme Microb. Technol. 2011, 49, 100–104.

    CAS  Google Scholar 

  228. S. Galai, P. Lucas-Elio, M. N. Marzouki, A. Sanchez-Amat, J. Appl. Microbiol. 2011, 111, 1394–1405.

    CAS  Google Scholar 

  229. S. S. Phugare, D. C. Kalyani, S. N. Surwase, J. P. Jadhav, Ecotoxicol. Environ. Saf. 2011, 74, 1288–1296.

    Article  PubMed  CAS  Google Scholar 

  230. Y. Li, Z. Gong, X. Li, Y. Li, X. G. Wang, BMC Biochem. 2011, 12, 30.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by a Teaching Load Modification Grant for S.F.M., funded by a grant awarded to Skidmore and Union Colleges from the National Science Foundation’s Advance PAID project (NSF 0820080).

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  1. Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, DK-1870, Frederiksberg C, Denmark

    Christopher Rensing

  2. Department of Biology, Skidmore College, 815 North Broadway, Saratoga Springs, NY, 12866, USA

    Sylvia Franke McDevitt

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    Lucia Banci

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Rensing, C., McDevitt, S.F. (2013). The Copper Metallome in Prokaryotic Cells. In: Banci, L. (eds) Metallomics and the Cell. Metal Ions in Life Sciences, vol 12. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5561-1_12

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