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Copper Homeostasis in Gram-Positive Bacteria

  • Marc Solioz
Chapter
Part of the SpringerBriefs in Molecular Science book series (BRIEFSMOLECULAR)

Abstract

Copper homeostasis in Gram-positive bacteria essentially requires three components: a copper exporting ATPase (founding member CopA), a copper chaperone (founding member CopZ), and a copper-responsive regulator (founding member CopY) which regulates the expression of these functions. GSH works as a back-up protective system. These four components are also part of the more complex copper homeostatic mechanism of Gram-negative organisms, discussed in Chap.  4, but will only be discussed in detail in this Chapter. Copper reduction at the plasma membrane, which is specific to Gram-positive bacteria will also be discussed here. Finally, copper regulons, which are apparently specific to Firmicutes, are presented. Most of the findings described here derive from Enterococcus hirae and L. lactis, but other organisms are considered as necessary.

Keywords

ATPase Chaperone Repressor CopA CopZ CopY Gram-positive Lactococcus Enterococcus Regulon 

References

  1. 1.
    Odermatt A, Suter H, Krapf R et al (1992) An ATPase operon involved in copper resistance by Enterococcus hirae. Ann NY Acad Sci 671:484–486PubMedGoogle Scholar
  2. 2.
    Odermatt A, Suter H, Krapf R et al (1993) Primary structure of two P-type ATPases involved in copper homeostasis in Enterococcus hirae. J Biol Chem 268:12775–12779PubMedGoogle Scholar
  3. 3.
    Itoh T, Takemoto K, Mori H et al (1999) Evolutionary instability of operon structures disclosed by sequence comparisons of complete microbial genomes. Mol Biol Evol 16:332–346PubMedGoogle Scholar
  4. 4.
    Shi L, Dong H, Reguera G et al (2016) Extracellular electron transfer mechanisms between microorganisms and minerals. Nat Rev Microbiol 14:651–662PubMedGoogle Scholar
  5. 5.
    Abicht HK, Gonskikh Y, Gerber SD et al (2013) Non-enzymatic copper reduction by menaquinone enhances copper toxicity in Lactococcus lactis IL1403. Microbiology 159:1190–1197PubMedGoogle Scholar
  6. 6.
    Tachon S, Brandsma JB, Yvon M (2010) NoxE NADH oxidase and the electron transport chain are responsible for the ability of Lactococcus lactis to decrease the redox potential of milk. Appl Environ Microbiol 76:1311–1319PubMedGoogle Scholar
  7. 7.
    Duwat P, Sourice S, Cesselin B et al (2001) Respiration capacity of the fermenting bacterium Lactococcus lactis and its positive effects on growth and survival. J Bacteriol 183:4509–4516PubMedPubMedCentralGoogle Scholar
  8. 8.
    Solioz M, Vulpe C (1996) CPx-type ATPases: a class of P-type ATPases that pump heavy metals. Trends Biochem Sci 21:237–241PubMedGoogle Scholar
  9. 9.
    Magnani D, Barré O, Gerber SD et al (2008) Characterization of the CopR regulon of Lactococcus lactis IL1403. J Bacteriol 190:536–545PubMedGoogle Scholar
  10. 10.
    Tottey S, Rich PR, Rondet SA et al (2001) Two Menkes-type atpases supply copper for photosynthesis in Synechocystis PCC 6803. J Biol Chem 276:19999–20004PubMedGoogle Scholar
  11. 11.
    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 USA 91:9651–9654PubMedGoogle Scholar
  12. 12.
    Lewinson O, Lee AT, Rees DC (2009) A P-type ATPase importer that discriminates between essential and toxic transition metals. Proc Natl Acad Sci USA 106:4677–4682PubMedGoogle Scholar
  13. 13.
    Chillappagari S, Miethke M, Trip H et al (2009) Copper acquisition is mediated by YcnJ and regulated by YcnK and CsoR in Bacillus subtilis. J Bacteriol 191:2362–2370PubMedPubMedCentralGoogle Scholar
  14. 14.
    Fukuhara T, Kobayashi K, Kanayama Y et al (2016) Identification and characterization of the zosA gene involved in copper uptake in Bacillus subtilis 168. Biosci Biotechnol Biochem 80:600–609PubMedGoogle Scholar
  15. 15.
    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 194:5675–5687PubMedPubMedCentralGoogle Scholar
  16. 16.
    Wang L, Zhu M, Zhang Q et al (2017) Diisonitrile natural product SF2768 functions as a chalkophore that mediates copper acquisition in Streptomyces thioluteus. ACS Chem Biol 12:3067–3075PubMedGoogle Scholar
  17. 17.
    Capdevila DA, Edmonds KA, Giedroc DP (2017) Metallochaperones and metalloregulation in bacteria. Essays Biochem 61:177–200PubMedPubMedCentralGoogle Scholar
  18. 18.
    Lin SJ, Culotta VC (1995) The ATX1 gene of Saccharomyces cerevisiae encodes a small metal homeostasis factor that protects cells against reactive oxygen toxicity. Proc Natl Acad Sci USA 92:3784–3788PubMedGoogle Scholar
  19. 19.
    Odermatt A, Solioz M (1995) Two trans-acting metalloregulatory proteins controlling expression of the copper-ATPases of Enterococcus hirae. J Biol Chem 270:4349–4354PubMedGoogle Scholar
  20. 20.
    Barkay T, Miller SM, Summers AO (2003) Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol Rev 27:355–384PubMedGoogle Scholar
  21. 21.
    Morby AP, Hobman JL, Brown NL (1995) The role of cysteine residues in the transport of mercuric ions by the Tn501 MerT and MerP mercury-resistance proteins. Mol Microbiol 17:25–35PubMedGoogle Scholar
  22. 22.
    Fan B, Grass G, Rensing C et al (2001) Escherichia coli CopA N-terminal Cys(X)2Cys motifs are not required for copper resistance or transport. Biochem Biophys Res Commun 286:414–418PubMedGoogle Scholar
  23. 23.
    Hou ZZ, Narindrasorasak S, Bhushan B et al (2001) Functional analysis of chimeric proteins of the Wilson Cu(I)-ATPase (ATP7B) and ZntA, a Pb(II)/Zn(II)/Cd(II)-ATPase from Escherichia coli. J Biol Chem e-pubGoogle Scholar
  24. 24.
    Mattle D, Sitsel O, Autzen HE et al (2013) On allosteric modulation of P-type Cu-ATPases. J Mol Biol 425:229–2308Google Scholar
  25. 25.
    Wimmer R, Herrmann T, Solioz M et al (1999) NMR structure and metal interactions of the CopZ copper chaperone. J Biol Chem 274:22597–22603PubMedGoogle Scholar
  26. 26.
    Banci L, Bertini I, Cantini F et al (2009) An NMR study of the interaction of the N-terminal cytoplasmic tail of the Wilson disease protein with copper(I)-HAH1. J Biol Chem 284:9354–9360PubMedPubMedCentralGoogle Scholar
  27. 27.
    Singleton C, Banci L, Ciofi-Baffoni S et al (2008) Structure and Cu(I)-binding properties of the N-terminal soluble domains of Bacillus subtilis CopA. Biochem J 411:571–579PubMedGoogle Scholar
  28. 28.
    Banci L, Bertini I, Chasapis CT et al (2007) Interaction of the two soluble metal-binding domains of yeast Ccc2 with copper(I)-Atx1. Biochem Biophys Res Commun 364:645–649PubMedGoogle Scholar
  29. 29.
    Achila D, Banci L, Bertini I et al (2006) Structure of human Wilson protein domains 5 and 6 and their interplay with domain 4 and the copper chaperone HAH1 in copper uptake. Proc Natl Acad Sci USA 103:5729–5734PubMedGoogle Scholar
  30. 30.
    Banci L, Bertini I, Cantini F et al (2005) A NMR study of the interaction of a three-domain construct of ATP7A with copper(I) and copper(I)-HAH1: the interplay of domains. J Biol Chem 280:38259–38263PubMedGoogle Scholar
  31. 31.
    Banci L, Bertini I, Ciofi-Baffoni S et al (2005) An NMR study of the interaction between the human copper(I) chaperone and the second and fifth metal-binding domains of the Menkes protein. FEBS J 272:865–871PubMedGoogle Scholar
  32. 32.
    Banci L, Bertini I, Ciofi-Baffoni S et al (2004) Solution structures of a cyanobacterial metallochaperone: insight into an atypical copper-binding motif. J Biol Chem 279:27502–27510PubMedGoogle Scholar
  33. 33.
    Anastassopoulou I, Banci L, Bertini I et al (2004) Solution structure of the apo and copper(I)-loaded human metallochaperone HAH1. Biochemistry 43:13046–13053PubMedGoogle Scholar
  34. 34.
    Banci L, Bertini I, Del Conte R et al (2003) X-ray absorption and NMR spectroscopic studies of CopZ, a copper chaperone in Bacillus subtilis: the coordination properties of the copper ion. Biochemistry 42:2467–2474PubMedGoogle Scholar
  35. 35.
    Banci L, Bertini I, Del Conte R et al (2001) Copper trafficking: the solution structure of Bacillus subtilis CopZ. Biochemistry 40:15660–15668PubMedGoogle Scholar
  36. 36.
    Arnesano F, Banci L, Bertini I et al (2001) Solution structure of the Cu(I) and apo forms of the yeast metallochaperone, Atx1. Biochemistry 40:1528–1539PubMedGoogle Scholar
  37. 37.
    Jordan IK, Natale DA, Koonin EV et al (2001) Independent evolution of heavy metal-associated domains in copper chaperones and copper-transporting ATPases. J Mol Evol 53:622–633PubMedGoogle Scholar
  38. 38.
    Rosenzweig AC (2001) Copper delivery by metallochaperone proteins. Acc Chem Res 34:119–128PubMedGoogle Scholar
  39. 39.
    Boal AK, Rosenzweig AC (2009) Structural biology of copper trafficking. Chem Rev 109:4760–4779PubMedPubMedCentralGoogle Scholar
  40. 40.
    Kay KL, Zhou L, Tenori L et al (2017) Kinetic analysis of copper transfer from a chaperone to its target protein mediated by complex formation. Chem Commun (Camb) 53:1397–1400Google Scholar
  41. 41.
    Banci L, Bertini I, Ciofi-Baffoni S et al (2006) The delivery of copper for thylakoid import observed by NMR. Proc Natl Acad Sci USA 103:8320–8325PubMedGoogle Scholar
  42. 42.
    Arnesano F, Banci L, Bertini I et al (2004) A docking approach to the study of copper trafficking proteins; interaction between metallochaperones and soluble domains of copper ATPases. Structure (Camb) 12:669–676Google Scholar
  43. 43.
    Banci L, Bertini I, Ciofi-Baffoni S et al (2003) Understanding copper trafficking in bacteria: interaction between the copper transport protein CopZ and the N-terminal domain of the copper ATPase CopA from Bacillus subtilis. Biochem 42:1939–1949Google Scholar
  44. 44.
    Lutsenko S (2016) Copper trafficking to the secretory pathway. Metallomics 8:840–852PubMedPubMedCentralGoogle Scholar
  45. 45.
    Harrison MD, Jones CE, Solioz M et al (2000) Intracellular copper routing: the role of copper chaperones. Trends Biochem Sci 25:29–32PubMedGoogle Scholar
  46. 46.
    Robinson NJ, Winge DR (2010) Copper metallochaperones. Annu Rev Biochem 79:537–562PubMedPubMedCentralGoogle Scholar
  47. 47.
    Pedersen PL, Carafoli E (1987) Ion motive ATPases. I. Ubiquity, properties, and significance to cell function. Trends Biochem Sci 12:146–150Google Scholar
  48. 48.
    Pedersen PL, Carafoli E (1987) Ion motive ATPases. II. Energy coupling and work output. Trends Biochem Sci 12:186–189Google Scholar
  49. 49.
    Toyoshima C, Nakasako M, Nomura H et al (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature 405:647–655PubMedGoogle Scholar
  50. 50.
    Lutsenko S, Kaplan JH (1995) Organization of P-type ATPases: significance of structural diversity. Biochemistry 34:15607–15613PubMedGoogle Scholar
  51. 51.
    Gourdon P, Liu XY, Skjorringe T et al (2011) Crystal structure of a copper-transporting PIB-type ATPase. Nature 475:59–64PubMedGoogle Scholar
  52. 52.
    Lübben M, Portmann R, Kock G et al (2009) Structural model of the CopA copper ATPase of Enterococcus hirae based on chemical cross-linking. Biometals 22:363–375PubMedGoogle Scholar
  53. 53.
    Smith AT, Smith KP, Rosenzweig AC (2014) Diversity of the metal-transporting P-type ATPases. J Biol Inorg Chem 19:947–960PubMedPubMedCentralGoogle Scholar
  54. 54.
    Takatsu H, Tanaka G, Segawa K et al (2014) Phospholipid flippase activities and substrate specificities of human type IV P-type ATPases localized to the plasma membrane. J Biol Chem 289:33543–33556PubMedGoogle Scholar
  55. 55.
    Axelsen KB, Palmgren MG (1998) Evolution of substrate specificities in the P-type ATPase superfamily. J Mol Evol 46:84–101PubMedGoogle Scholar
  56. 56.
    Ogawa H, Haga T, Toyoshima C (2000) Soluble P-type ATPase from an archaeon, Methanococcus jannaschii. FEBS Lett 471:99–102PubMedGoogle Scholar
  57. 57.
    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 202:44–48PubMedGoogle Scholar
  58. 58.
    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 24:467–475PubMedPubMedCentralGoogle Scholar
  59. 59.
    Raimunda D, Padilla-Benavides T, Vogt S et al (2013) Periplasmic response upon disruption of transmembrane Cu transport in Pseudomonas aeruginosa. Metallomics 5:144–151PubMedGoogle Scholar
  60. 60.
    Bork P (2000) Powers and pitfalls in genome analysis: the 70% hurdle. Genome Res 10:398–400PubMedGoogle Scholar
  61. 61.
    Solioz M, Odermatt A (1995) Copper and silver transport by CopB-ATPase in membrane vesicles of Enterococcus hirae. J Biol Chem 270:9217–9221PubMedGoogle Scholar
  62. 62.
    Mana-Capelli S, Mandal AK, Arguello JM (2003) Archaeoglobus fulgidus CopB is a thermophilic Cu2+-ATPase: functional role of its histidine-rich-N-terminal metal binding domain. J Biol Chem 278:40534–40541PubMedGoogle Scholar
  63. 63.
    Bingham MJ, Ong TJ, Ingledew WJ et al (1996) ATP-dependent copper transporter, in the golgi apparatus of rat hepatocytes, transports Cu(II) not Cu(I). Am J Physiol 271:G741–G746PubMedGoogle Scholar
  64. 64.
    Voskoboinik I, Brooks H, Smith S et al (1998) ATP-dependent copper transport by the Menkes protein in membrane vesicles isolated from cultured Chinese hamster ovary cells. FEBS Lett 435:178–182PubMedGoogle Scholar
  65. 65.
    Voskoboinik I, Mar J, Camakaris J (2003) Mutational analysis of the Menkes copper P-type ATPase (ATP7A). Biochem Biophys Res Commun 301:488–494PubMedGoogle Scholar
  66. 66.
    Voskoboinik I, Strausak D, Greenough M et al (1999) Functional analysis of the N-terminal CXXC metal-binding motifs in the human menkes copper-transporting P-type ATPase expressed in cultured mammalian cells. J Biol Chem 274:22008–22012PubMedGoogle Scholar
  67. 67.
    Hanson SR, Donley SA, Linder MC (2001) Transport of silver in virgin and lactating rats and relation to copper. J Trace Elem Med Biol 15:243–253PubMedGoogle Scholar
  68. 68.
    Gonzalez-Guerrero M, Eren E, Rawat S et al (2008) Structure of the two transmembrane Cu+ transport sites of the Cu+-ATPases. J Biol Chem 283:29753–29759PubMedPubMedCentralGoogle Scholar
  69. 69.
    Blaby-Haas CE, Padilla-Benavides T, Stube R et al (2014) Evolution of a plant-specific copper chaperone family for chloroplast copper homeostasis. Proc Natl Acad Sci USA 111:E5480–E5487PubMedGoogle Scholar
  70. 70.
    Grønberg C, Sitsel O, Lindahl E et al (2016) Membrane anchoring and ion-entry dynamics in P-type ATPase copper transport. Biophys J 111:2417–2429PubMedPubMedCentralGoogle Scholar
  71. 71.
    Mattle D, Zhang L, Sitsel O et al (2015) A sulfur-based transport pathway in Cu+-ATPases. EMBO Rep 16:728–740PubMedPubMedCentralGoogle Scholar
  72. 72.
    Wijekoon CJ, Udagedara SR, Knorr RL et al (2017) Copper ATPase CopA from E. coli. Quantitative correlation between ATPase activity and vectorial copper transport. J Am Chem Soc 139:4266–4269PubMedGoogle Scholar
  73. 73.
    Hatori Y, Lewis D, Toyoshima C et al (2009) Reaction cycle of Thermotoga maritima copper ATPase and conformational characterization of catalytically deficient mutants. Biochemistry 48:4871–4880PubMedPubMedCentralGoogle Scholar
  74. 74.
    Bissig K-D, Voegelin TC, Solioz M (2001) Tetrathiomolybdate inhibition of the Enterococcus hirae CopB copper ATPase. FEBS Lett 507:367–370PubMedGoogle Scholar
  75. 75.
    Changela A, Chen K, Xue Y et al (2003) Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301:1383–1387PubMedGoogle Scholar
  76. 76.
    Banci L, Bertini I, Ciofi-Baffoni S et al (2010) Affinity gradients drive copper to cellular destinations. Nature 465:645–650PubMedGoogle Scholar
  77. 77.
    Giedroc DP, Arunkumar AI (2007) Metal sensor proteins: nature’s metalloregulated allosteric switches. Dalton Trans 3107–3120Google Scholar
  78. 78.
    Strausak D, Solioz M (1997) CopY is a copper-inducible repressor of the Enterococcus hirae copper ATPases. J Biol Chem 272:8932–8936PubMedGoogle Scholar
  79. 79.
    Cantini F, Banci L, Solioz M (2009) The copper-responsive repressor CopR of Lactococcus lactis is a ‘winged helix’ protein. Biochem J 417:493–499PubMedGoogle Scholar
  80. 80.
    Cobine P, Wickramasinghe WA, Harrison MD et al (1999) The Enterococcus hirae copper chaperone CopZ delivers copper(I) to the CopY repressor. FEBS Lett 445:27–30PubMedGoogle Scholar
  81. 81.
    Lu ZH, Solioz M (2001) Copper-induced proteolysis of the CopZ copper chaperone of Enterococcus hirae. J Biol Chem 276:47822–47827PubMedGoogle Scholar
  82. 82.
    Cobine PA, George GN, Jones CE et al (2002) Copper transfer from the Cu(I) chaperone, CopZ, to the repressor, Zn(II)CopY: metal coordination environments and protein interactions. Biochemistry 41:5822–5829PubMedGoogle Scholar
  83. 83.
    Portmann R, Magnani D, Stoyanov JV et al (2004) Interaction kinetics of the copper-responsive CopY repressor with the cop promoter of Enterococcus hirae. J Biol Inorg Chem 9:396–402PubMedGoogle Scholar
  84. 84.
    Fahey RC, Brown WC, Adams WB et al (1978) Occurrence of glutathione in bacteria. J Bacteriol 133:1126–1129PubMedPubMedCentralGoogle Scholar
  85. 85.
    Newton GL, Arnold K, Price MS et al (1996) Distribution of thiols in microorganisms: mycothiol is a major thiol in most actinomycetes. J Bacteriol 178:1990–1995PubMedPubMedCentralGoogle Scholar
  86. 86.
    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 USA 107:6482–6486PubMedGoogle Scholar
  87. 87.
    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 369:1047–1051PubMedGoogle Scholar
  88. 88.
    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 30:1191–1212PubMedGoogle Scholar
  89. 89.
    Obeid MH, Oertel J, Solioz M et al (2016) Mechanism of attenuation of uranyl toxicity by glutathione in Lactococcus lactis. Appl Environ Microbiol 82:3563–3571PubMedPubMedCentralGoogle Scholar
  90. 90.
    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 242:67–70PubMedGoogle Scholar
  91. 91.
    Fu RY, Bongers RS, van Swam II et al (2006) Introducing glutathione biosynthetic capability into Lactococcus lactis subsp. cremoris NZ9000 improves the oxidative-stress resistance of the host. Metab Eng 8:662–671PubMedGoogle Scholar
  92. 92.
    Li Y, Hugenholtz J, Abee T et al (2003) Glutathione protects Lactococcus lactis against oxidative stress. Appl Environ Microbiol 69:5739–5745PubMedPubMedCentralGoogle Scholar
  93. 93.
    Zhang J, Fu RY, Hugenholtz J et al (2007) Glutathione protects Lactococcus lactis against acid stress. Appl Environ Microbiol 73:5268–5275PubMedPubMedCentralGoogle Scholar
  94. 94.
    Helbig K, Bleuel C, Krauss GJ et al (2008) Glutathione and transition-metal homeostasis in Escherichia coli. J Bacteriol 190:5431–5438PubMedPubMedCentralGoogle Scholar
  95. 95.
    Potter AJ, Trappetti C, Paton JC (2012) Streptococcus pneumoniae uses glutathione to defend against oxidative stress and metal ion toxicity. J Bacteriol 194:6248–6254PubMedPubMedCentralGoogle Scholar
  96. 96.
    Vasak M, Meloni G (2011) Chemistry and biology of mammalian metallothioneins. J Biol Inorg Chem 16:1067–1078PubMedGoogle Scholar
  97. 97.
    Gold B, Deng H, Bryk R et al (2008) Identification of a copper-binding metallothionein in pathogenic mycobacteria. Nat Chem Biol 4:609–616PubMedPubMedCentralGoogle Scholar
  98. 98.
    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 6:39065PubMedPubMedCentralGoogle Scholar
  99. 99.
    Blindauer CA (2011) Bacterial metallothioneins: past, present, and questions for the future. J Biol Inorg Chem 16:1011–1024PubMedGoogle Scholar
  100. 100.
    Portmann R, Poulsen KR, Wimmer R et al (2006) CopY-like copper inducible repressors are putative ‘winged helix’ proteins. Biometals 19:61–70PubMedGoogle Scholar
  101. 101.
    Barré O, Mourlane F, Solioz M (2007) Copper induction of lactate oxidase of Lactococcus lactis: a novel metal stress response. J Bacteriol 189:5947–5954PubMedPubMedCentralGoogle Scholar
  102. 102.
    Marty-Teysset C, de la Torre F, Garel J (2000) Increased production of hydrogen peroxide by Lactobacillus delbrueckii subsp. bulgaricus upon aeration: involvement of an NADH oxidase in oxidative stress. Appl Environ Microbiol 66:262–267PubMedPubMedCentralGoogle Scholar
  103. 103.
    Mermod M, Mourlane F, Waltersperger S et al (2010) Structure and function of CinD (YtjD) of Lactococcus lactis, a copper-induced nitroreductase involved in defense against oxidative stress. J Bacteriol 192:4172–4180PubMedPubMedCentralGoogle Scholar
  104. 104.
    Mancini S, Abicht HK, Gonskikh Y et al (2015) A copper-induced quinone degradation pathway provides protection against combined copper/quinone stress in Lactococcus lactis IL1403. Mol Microbiol 95:645–659PubMedGoogle Scholar
  105. 105.
    Leelakriangsak M, Huyen NT, Towe S et al (2008) Regulation of quinone detoxification by the thiol stress sensing DUF24/MarR-like repressor, YodB in Bacillus subtilis. Mol Microbiol 67:1108–1124PubMedGoogle Scholar

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© The Author(s) 2018

Authors and Affiliations

  1. 1.Department Clinical ResearchUniversity of BernBernSwitzerland

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