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BioMetals

, Volume 29, Issue 3, pp 433–450 | Cite as

Restoration of growth by manganese in a mutant strain of Escherichia coli lacking most known iron and manganese uptake systems

  • Nadine Taudte
  • Nadezhda German
  • Yong-Guan Zhu
  • Gregor Grass
  • Christopher Rensing
Article

Abstract

The interplay of manganese and iron homeostasis and oxidative stress in Escherichia coli can give important insights into survival of bacteria in the phagosome and under differing iron or manganese bioavailabilities. Here, we characterized a mutant strain devoid of all know iron/manganese-uptake systems relevant for growth in defined medium. Based on these results an exit strategy enabling the cell to cope with iron depletion and use of manganese as an alternative for iron could be shown. Such a strategy would also explain why E. coli harbors some iron- or manganese-dependent iso-enzymes such as superoxide dismutases or ribonucleotide reductases. The benefits for gaining a means for survival would be bought with the cost of less efficient metabolism as indicated in our experiments by lower cell densities with manganese than with iron. In addition, this strain was extremely sensitive to the metalloid gallium but this gallium toxicity can be alleviated by low concentrations of manganese.

Keywords

Iron Manganese SOD Gallium 

Abbreviation

DIP

2,2′-dipyridyl

Notes

Acknowledgments

This work was supported by start-up funds at the University of Copenhagen for C.R. and by the Deutsche Forschungsgemeinschaft by Grant GR2061/1-2 to G. G. We thank Grit Schleuder for skilful technical assistance.

References

  1. Al-Maghrebi M, Fridovich I, Benov L (2002) Manganese supplementation relieves the phenotypic deficits seen in superoxide-dismutase-null Escherichia coli. Arch Biochem Biophys 402:104–109CrossRefPubMedGoogle Scholar
  2. Andrews SC (2011) Making DNA without iron—induction of a manganese-dependent ribonucleotide reductase in response to iron starvation. Mol Microbiol 80:286–289. doi: 10.1111/j.1365-2958.2011.07594.x CrossRefPubMedGoogle Scholar
  3. Anjem A, Varghese S, Imlay JA (2009) Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Mol Microbiol 72:844–858. doi: 10.1111/j.1365-2958.2009.06699.x CrossRefPubMedPubMedCentralGoogle Scholar
  4. Archibald F (1983) Lactobacillus plantarum, an organism not requiring iron. FEMS Microbiol Lett 19:29–32CrossRefGoogle Scholar
  5. Archibald F (1986) Manganese: its acquisition by and function in the lactic acid bacteria. Crit Rev Microbiol 13:63–109. doi: 10.3109/10408418609108735 CrossRefPubMedGoogle Scholar
  6. Archibald FS, Duong MN (1984) Manganese acquisition by Lactobacillus plantarum. J Bacteriol 158:1–8PubMedPubMedCentralGoogle Scholar
  7. Archibald FS, Fridovich I (1981) Manganese and defenses against oxygen toxicity in Lactobacillus plantarum. J Bacteriol 145:442–451PubMedPubMedCentralGoogle Scholar
  8. Bachmann BJ (1972) Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol Rev 36:525–557PubMedPubMedCentralGoogle Scholar
  9. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287CrossRefPubMedGoogle Scholar
  10. Becker KW, Skaar EP (2014) Metal limitation and toxicity at the interface between host and pathogen. FEMS Microbiol Rev 38:1235–1249. doi: 10.1111/1574-6976.12087 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Beriault R, Hamel R, Chenier D, Mailloux RJ, Joly H, Appanna VD (2007) The overexpression of NADPH-producing enzymes counters the oxidative stress evoked by gallium, an iron mimetic. Biometals 20:165–176CrossRefPubMedGoogle Scholar
  12. Beyer WF Jr, Fridovich I (1991) In vivo competition between iron and manganese for occupancy of the active site region of the manganese-superoxide dismutase of Escherichia coli. J Biol Chem 266:303–308PubMedGoogle Scholar
  13. Boyer E, Bergevin I, Malo D, Gros P, Cellier MF (2002) Acquisition of Mn(II) in addition to Fe(II) is required for full virulence of Salmonella enterica serovar Typhimurium. Infect Immun 70:6032–6042CrossRefPubMedPubMedCentralGoogle Scholar
  14. Carpenter C, Payne SM (2014) Regulation of iron transport systems in Enterobacteriaceae in response to oxygen and iron availability. J Inorg Biochem 133:110–117. doi: 10.1016/j.jinorgbio.2014.01.007 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cellier MF (2012) Nramp: from sequence to structure and mechanism of divalent metal import. Curr Top Membr 69:249–293. doi: 10.1016/B978-0-12-394390-3.00010-0 CrossRefPubMedGoogle Scholar
  16. Chitambar CR (2004) Apoptotic mechanisms of gallium nitrate: basic and clinical investigations. Oncology (Williston Park) 18:39–44Google Scholar
  17. Chitambar CR, Narasimhan J, Guy J, Sem DS, O’Brien WJ (1991) Inhibition of ribonucleotide reductase by gallium in murine leukemic L1210 cells. Cancer Res 51:6199–6201PubMedGoogle Scholar
  18. Cotruvo JA Jr, Stubbe J (2010) An active dimanganese(III)-tyrosyl radical cofactor in Escherichia coli class Ib ribonucleotide reductase. Biochemistry 49:1297–1309. doi: 10.1021/bi902106n CrossRefPubMedPubMedCentralGoogle Scholar
  19. Daly MJ (2009) A new perspective on radiation resistance based on Deinococcus radiodurans. Nat Rev Microbiol 7:237–245CrossRefPubMedGoogle Scholar
  20. Daly MJ et al (2004) Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science 306:1025–1028CrossRefPubMedGoogle Scholar
  21. Daly MJ et al (2007) Protein oxidation implicated as the primary determinant of bacterial radioresistance. PloS Biol 5:e92CrossRefPubMedPubMedCentralGoogle Scholar
  22. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640–6645CrossRefPubMedPubMedCentralGoogle Scholar
  23. Donovan A et al (2000) Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter. Nature 403:776–781CrossRefPubMedGoogle Scholar
  24. Espirito Santo C, Lam EW, Elowsky CG, Quaranta D, Domaille DW, Chang CJ, Grass G (2011) Bacterial killing by dry metallic copper surfaces. Appl Environ Microbiol 77:794–802. doi: 10.1128/AEM.01599-10 CrossRefPubMedGoogle Scholar
  25. Folsom JP, Parker AE, Carlson RP (2014) Physiological and proteomic analysis of Escherichia coli iron-limited chemostat growth. J Bacteriol 196:2748–2761. doi: 10.1128/JB.01606-14 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Franca MB, Panek AD, Eleutherio EC (2007) Oxidative stress and its effects during dehydration. Comp Biochem Physiol A 146:621–631. doi: 10.1016/j.cbpa.2006.02.030 CrossRefGoogle Scholar
  27. Fraser HI, Kvaratskhelia M, White MF (1999) The two analogous phosphoglycerate mutases of Escherichia coli. FEBS Lett 455:344–348CrossRefPubMedGoogle Scholar
  28. Fredrickson JK et al (2008) Protein oxidation: key to bacterial desiccation resistance? ISME J 2:393–403. doi: 10.1038/ismej.2007.116 CrossRefPubMedGoogle Scholar
  29. Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112. doi: 10.1146/annurev.bi.64.070195.000525 CrossRefPubMedGoogle Scholar
  30. Garénaux A, Caza M, Dozois CM (2011) The Ins and Outs of siderophore mediated iron uptake by extra-intestinal pathogenic Escherichia coli. Vet Microbiol 153:89–98. doi: 10.1016/j.vetmic.2011.05.023 CrossRefPubMedGoogle Scholar
  31. Grass G, Rensing C (2001) Genes involved in copper homeostasis in Escherichia coli. J Bacteriol 183:2145–2147CrossRefPubMedPubMedCentralGoogle Scholar
  32. Grass G, Franke S, Taudte N, Nies DH, Kucharski LM, Maguire ME, Rensing C (2005) The metal permease ZupT from Escherichia coli is a transporter with a broad substrate spectrum. J Bacteriol 187:1604–1611CrossRefPubMedPubMedCentralGoogle Scholar
  33. Harrington JR, Martens RJ, Cohen ND, Bernstein LR (2006) Antimicrobial activity of gallium against virulent Rhodococcus equi in vitro and in vivo. J Vet Pharmacol Ther 29:121–127CrossRefPubMedGoogle Scholar
  34. Hassan HM, Fridovich I (1977) Regulation of the synthesis of superoxide dismutase in Escherichia coli. Induction by methyl viologen. J Biol Chem 252:7667–7672PubMedGoogle Scholar
  35. Horsburgh MJ, Wharton SJ, Karavolos M, Foster SJ (2002) Manganese: elemental defence for a life with oxygen. Trends Microbiol 10:496–501CrossRefPubMedGoogle Scholar
  36. Hubbard JA, Lewandowska KB, Hughes MN, Poole RK (1986) Effects of iron-limitation of Escherichia coli on growth, the respiratory chains and gallium uptake. Arch Microbiol 146:80–86CrossRefPubMedGoogle Scholar
  37. Imlay JA (2003) Pathways of oxidative damage. Annu Rev Microbiol 57:395–418CrossRefPubMedGoogle Scholar
  38. Imlay JA (2008) Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77:55CrossRefGoogle Scholar
  39. Imlay KR, Imlay JA (1996) Cloning and analysis of sodC, encoding the copper-zinc superoxide dismutase of Escherichia coli. J Bacteriol 178:2564–2571PubMedPubMedCentralGoogle Scholar
  40. Imlay JA, Linn S (1988) DNA damage and oxygen radical toxicity. Science 240:1302–1309CrossRefPubMedGoogle Scholar
  41. Jakubovics NS, Smith AW, Jenkinson HF (2000) Expression of the virulence-related Sca (Mn2+) permease in Streptococcus gordonii is regulated by a diphtheria toxin metallorepressor-like protein ScaR. Mol Microbiol 38:140–153CrossRefPubMedGoogle Scholar
  42. Jordan A, Pontis E, Atta M, Krook M, Gibert I, Barbe J, Reichard P (1994) A second class I ribonucleotide reductase in Enterobacteriaceae: characterization of the Salmonella typhimurium enzyme. Proc Natl Acad Sci USA 91:12892–12896CrossRefPubMedPubMedCentralGoogle Scholar
  43. Kaneko Y, Thoendel M, Olakanmi O, Britigan BE, Singh PK (2007) The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J Clin Invest 117:877–888CrossRefPubMedPubMedCentralGoogle Scholar
  44. Kargalioglu Y, Imlay JA (1994) Importance of anaerobic superoxide dismutase synthesis in facilitating outgrowth of Escherichia coli upon entry into an aerobic habitat. J Bacteriol 176:7653–7658PubMedPubMedCentralGoogle Scholar
  45. Kehres DG, Maguire ME (2003) Emerging themes in manganese transport, biochemistry and pathogenesis in bacteria. FEMS Microbiol Rev 27:263–290CrossRefPubMedGoogle Scholar
  46. Korbashi P, Kohen R, Katzhendler J, Chevion M (1986) Iron mediates paraquat toxicity in Escherichia coli. J Biol Chem 261:12472–12476PubMedGoogle Scholar
  47. Lisher JP, Giedroc DP (2013) Manganese acquisition and homeostasis at the host-pathogen interface. Front Cell Infect Microbiol 3:91. doi: 10.3389/fcimb.2013.00091 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Macomber L, Imlay JA (2009) The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc Natl Acad Sci USA 106:8344–8349. doi: 10.1073/pnas.0812808106 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Makarova KS et al (2007) Deinococcus geothermalis: the pool of extreme radiation resistance genes shrinks. PloS One 2:e955CrossRefPubMedPubMedCentralGoogle Scholar
  50. Martin JE, Imlay JA (2011) The alternative aerobic ribonucleotide reductase of Escherichia coli, NrdEF, is a manganese-dependent enzyme that enables cell replication during periods of iron starvation. Mol Microbiol 80:319–334. doi: 10.1111/j.1365-2958.2011.07593.x CrossRefPubMedPubMedCentralGoogle Scholar
  51. Mattimore V, Battista JR (1996) Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J Bacteriol 178:633–637PubMedPubMedCentralGoogle Scholar
  52. McEwan AG (2009) New insights into the protective effect of manganese against oxidative stress. Mol Microbiol. doi: 10.1111/j.1365-2958.2009.06700.x PubMedGoogle Scholar
  53. Mergeay M, Nies D, Schlegel HG, Gerits J, Charles P, Van Gijsegem F (1985) Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J Bacteriol 162:328–334PubMedPubMedCentralGoogle Scholar
  54. Minton KW, Daly MJ (1995) A model for repair of radiation-induced DNA double-strand breaks in the extreme radiophile Deinococcus radiodurans. BioEssays 17:457–464. doi: 10.1002/bies.950170514 CrossRefPubMedGoogle Scholar
  55. Missiakas D, Raina S (1997) Protein folding in the bacterial periplasm. J Bacteriol 179:2465–2471PubMedPubMedCentralGoogle Scholar
  56. Monje-Casas F, Jurado J, Prieto-Alamo MJ, Holmgren A, Pueyo C (2001) Expression analysis of the nrdHIEF operon from Escherichia coli. Conditions that trigger the transcript level in vivo. J Biol Chem 276:18031–18037. doi: 10.1074/jbc.M011728200 CrossRefPubMedGoogle Scholar
  57. Niven DF, Ekins A, Al-Samaurai AA (1999) Effects of iron and manganese availability on growth and production of superoxide dismutase by Streptococcus suis. Can J Microbiol 45:1027–1032CrossRefPubMedGoogle Scholar
  58. Olakanmi O, Britigan BE, Schlesinger LS (2000) Gallium disrupts iron metabolism of mycobacteria residing within human macrophages. Infect Immun 68:5619–5627CrossRefPubMedPubMedCentralGoogle Scholar
  59. Park S, Imlay JA (2003) High levels of intracellular cysteine promote oxidative DNA damage by driving the Fenton reaction. J Bacteriol 185:1942–1950CrossRefPubMedPubMedCentralGoogle Scholar
  60. Patzer SI, Hantke K (2001) Dual repression by Fe(2+)-Fur and Mn(2+)-MntR of the mntH gene, encoding an NRAMP-like Mn(2+) transporter in Escherichia coli. J Bacteriol 183:4806–4813. doi: 10.1128/JB.183.16.4806-4813.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Pereira Ede J, Panek AD, Eleutherio EC (2003) Protection against oxidation during dehydration of yeast. Cell Stress Chaperones 8:120–124CrossRefPubMedGoogle Scholar
  62. Posey JE, Gherardini FC (2000) Lack of a role for iron in the Lyme disease pathogen. Science 288:1651–1653CrossRefPubMedGoogle Scholar
  63. Que Q, Helmann JD (2000) Manganese homeostasis in Bacillus subtilis is regulated by MntR, a bifunctional regulator related to the diphtheria toxin repressor family of proteins. Mol Microbiol 35:1454–1468CrossRefPubMedGoogle Scholar
  64. Rocha AG, Dancis A (2015) Life without Fe–S clusters. Mol Microbiol. doi: 10.1111/mmi.13273 PubMedGoogle Scholar
  65. Rowley DA, Halliwell B (1982) Superoxide-dependent formation of hydroxyl radicals from NADH and NADPH in the presence of iron salts. FEBS Lett 142:39–41CrossRefPubMedGoogle Scholar
  66. Sabri M et al (2008) Contribution of the SitABCD, MntH, and FeoB metal transporters to the virulence of avian pathogenic Escherichia coli O78 strain chi7122. Infect Immun 76:601–611CrossRefPubMedPubMedCentralGoogle Scholar
  67. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  68. Seib KL, Tseng HJ, McEwan AG, Apicella MA, Jennings MP (2004) Defenses against oxidative stress in Neisseria gonorrhoeae and Neisseria meningitidis: distinctive systems for different lifestyles. J Infect Dis 190:136–147CrossRefPubMedGoogle Scholar
  69. Shi L, Kehres DG, Maguire ME (2001) The PPP-family protein phosphatases PrpA and PrpB of Salmonella enterica serovar Typhimurium possess distinct biochemical properties. J Bacteriol 183:7053–7057. doi: 10.1128/JB.183.24.7053-7057.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Stojiljkovic I, Kumar V, Srinivasan N (1999) Non-iron metalloporphyrins: potent antibacterial compounds that exploit haem/Hb uptake systems of pathogenic bacteria. Mol Microbiol 31:429–442CrossRefPubMedGoogle Scholar
  71. Storz G, Imlay JA (1999) Oxidative stress. Curr Opin Microbiol 2:188–194CrossRefPubMedGoogle Scholar
  72. Tanaka N, Kanazawa M, Tonosaki K, Yokoyama N, Kuzuyama T, Takahashi Y (2015) Novel features of the ISC machinery revealed by characterization of Escherichia coli mutants that survive without iron-sulfur clusters. Mol Microbiol. doi: 10.1111/mmi.13271 Google Scholar
  73. Taudte N, Grass G (2010) Point mutations change specificity and kinetics of metal uptake by ZupT from Escherichia coli. Biometals 4:643–656. doi: 10.1007/s10534-010-9319-z CrossRefGoogle Scholar
  74. Touati D, Jacques M, Tardat B, Bouchard L, Despied S (1995) Lethal oxidative damage and mutagenesis are generated by iron in delta fur mutants of Escherichia coli: protective role of superoxide dismutase. J Bacteriol 177:2305–2314PubMedPubMedCentralGoogle Scholar
  75. Weinberg ED (1997) The Lactobacillus anomaly: total iron abstinence. Perspect Biol Med 40:578–583CrossRefPubMedGoogle Scholar
  76. Woodmansee AN, Imlay JA (2002) Reduced flavins promote oxidative DNA damage in non-respiring Escherichia coli by delivering electrons to intracellular free iron. J Biol Chem 277:34055–34066CrossRefPubMedGoogle Scholar
  77. Zaharik ML et al (2004) The Salmonella enterica serovar typhimurium divalent cation transport systems MntH and SitABCD are essential for virulence in an Nramp1G169 murine typhoid model. Infect Immun 72:5522–5525. doi: 10.1128/IAI.72.9.5522-5525.2004 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Nadine Taudte
    • 1
  • Nadezhda German
    • 2
  • Yong-Guan Zhu
    • 3
  • Gregor Grass
    • 1
    • 4
  • Christopher Rensing
    • 3
    • 5
  1. 1.Institute for Biology/MicrobiologyMartin-Luther-University Halle-WittenbergHalleGermany
  2. 2.Department of Pharmaceutical SciencesTexas Tech Health Science CenterAmarilloUSA
  3. 3.Institute of Urban EnvironmentChinese Academy of SciencesXiamenChina
  4. 4.Bundeswehr Institute of MicrobiologyMunichGermany
  5. 5.Department of Plant and Environmental SciencesUniversity of CopenhagenFrederiksbergDenmark

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