Skip to main content
SpringerLink
Log in
Book cover

Molecular Microbiology of Heavy Metals pp 235–257Cite as

Manganese: Uptake, Biological Function, and Role in Virulence

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

Abstract

Recent data have demonstrated that bacterial homologs of eukaryotic Nramp transporters as well as members of the LraI family of proteins are both highly selective Mn2+ transporters. Mutation of these transporters in several pathogenic bacterial species causes decreased virulence in a variety of model systems. This implies that the Mn2+ ions are required for one or more processes essential for bacterial virulence. However, Mn2+ has few known enzymatic roles compared to other divalent cations. This review will describe what is currently known about the two classes of prokaryotic Mn2+ transporters, how each is regulated and the virulence deficits that arise when they are mutated. Finally, possible enzymatic roles for Mn2+ will be outlined, and their potential for a role in virulence discussed.

Keywords

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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

Chapter
USD   29.95
Price excludes VAT (Canada)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (Canada)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.00
Price excludes VAT (Canada)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (Canada)
  • Durable hardcover 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

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Agranoff D, Monahan IM, Mangan JA, Butcher PD, Krishna S (1999) Mycobacterium tuberculosis expresses a novel pH-dependent divalent cation transporter belonging to the Nramp family. J Exp Med 190:717–724

    CrossRef  PubMed  CAS  Google Scholar 

  2. Ando M, Manabe YC, Converse PJ, Miyazaki E, Harrison R, Murphy JR, Bishai WR (2003) Characterization of the role of the divalent metal ion-dependent transcriptional repressor MntR in the virulence of Staphylococcus aureus. Infect Immun 71:2584–2590

    CrossRef  PubMed  CAS  Google Scholar 

  3. Archambaud C, Gouin E, Pizarro-Cerda J, Cossart P, Dussurget O (2005) Translation elongation factor EF-Tu is a target for Stp, a serine-threonine phosphatase involved in virulence of Listeria monocytogenes. Molec Microbiol 56:383–396

    CrossRef  CAS  Google Scholar 

  4. Archibald F (1986) Manganese: its acquisition by and function in the lactic acid bacteria. Crit Rev Microbiol 13:63–109

    CrossRef  PubMed  CAS  Google Scholar 

  5. Archibald FS, Duong MN (1984) Manganese acquisition by Lactobacillus plantarum. J Bacteriol 158:1–8

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  7. Bartsevich VV, Pakrasi HB (1996) Manganese transport in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 271:26057–26061

    CrossRef  PubMed  CAS  Google Scholar 

  8. Bates CS, Toukoki C, Neely MN, Eichenbaum Z (2005) Characterization of MtsR, a new metal regulator in group A Streptococcus, involved in iron acquisition and virulence. Infect Immun 73:5743–5753

    CrossRef  PubMed  CAS  Google Scholar 

  9. Bearden SW, Perry RD (1999) The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol Microbiol 32:403–414

    CrossRef  PubMed  CAS  Google Scholar 

  10. Berry AM, Paton JC (1996) Sequence heterogeneity of PsaA, a 37-kilodalton putative adhesin essential for virulence of Streptococcus pneumoniae. Infect Immun 64:5255–5262

    PubMed  CAS  Google Scholar 

  11. Boechat N, Lagier-Roger B, Petit S, Bordat Y, Rauzier J, Hance AJ, Gicquel B, Reyrat JM (2002) Disruption of the gene homologous to mammalian Nramp1 in Mycobacterium tuberculosis does not affect virulence in mice. Infect Immun 70:4124–4131

    CrossRef  PubMed  CAS  Google Scholar 

  12. Boitel B, Ortiz-Lombardia M, Duran R, Pompeo F, Cole ST, Cervenansky C, Alzari PM (2003) PknB kinase activity is regulated by phosphorylation in two Thr residues and dephosphorylation by PstP, the cognate phospho-Ser/Thr phosphatase, in Mycobacterium tuberculosis. Mol Microbiol 49:1493–1508

    CrossRef  PubMed  CAS  Google Scholar 

  13. Boyd J, Oza MN, Murphy JR (1990) Molecular cloning and DNA sequence analysis of a diphtheria toxin iron-dependent regulatory element (dtxR) from Corynebacterium. Proc Natl Acad Sci USA 87:5968–5972

    CrossRef  PubMed  CAS  Google Scholar 

  14. 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 70:6032–6042

    CrossRef  PubMed  CAS  Google Scholar 

  15. Brown IN, Glynn AA, Plant J (1982) Inbred mouse strain resistance to Mycobacterium lepraemurium follows the Ity/Lsh pattern. Immunology 47:149–156

    PubMed  CAS  Google Scholar 

  16. Canonne-Hergaux F, Gruenheid S, Ponka P, Gros P (1999) Cellular and subcellular localization of the Nramp2 iron transporter in the intestinal brush border and regulation by dietary iron. Blood 93:4406–4417

    PubMed  CAS  Google Scholar 

  17. Cellier MF, Bergevin I, Boyer E, Richer E (2001) Polyphyletic origins of bacterial Nramp transporters. Trends Genet 17:365–370

    CrossRef  PubMed  CAS  Google Scholar 

  18. Chaba R, Raje M, Chakraborti PK (2002) Evidence that a eukaryotic-type serine/threonine protein kinase from Mycobacterium tuberculosis regulates morphological changes associated with cell division. Eur J Biochem 269:1078–1085

    CrossRef  PubMed  CAS  Google Scholar 

  19. Chandler LE, Bartsevich VV, Pakrasi HB (2003) Regulation of manganese uptake in Synechocystis sp. 6803 by RfrA, a member of a novel family of proteins containing a repeated five-residues domain. Biochemistry 42:5508–5514

    CrossRef  PubMed  CAS  Google Scholar 

  20. Chao TC, Becker A, Buhrmester J, Puhler A, Weidner S (2004) The Sinorhizobium meliloti fur gene regulates, with dependence on Mn(II), transcription of the sitABCD operon, encoding a metal-type transporter. J Bacteriol 186:3609–3620

    CrossRef  PubMed  CAS  Google Scholar 

  21. Chua AC, Morgan EH (1997) Manganese metabolism is impaired in the Belgrade laboratory rat. J Comp Physiol B 167:361–369

    CrossRef  PubMed  CAS  Google Scholar 

  22. Courville P, Chaloupka R, Veyrier F, Cellier MF (2004) Determination of transmembrane topology of the Escherichia coli natural resistance-associated macrophage protein (Nramp) ortholog. J Biol Chem 279:3318–3326

    CrossRef  PubMed  CAS  Google Scholar 

  23. Dashper SG, Butler CA, Lissel JP, Paolini RA, Hoffmann B, Veith PD, O'Brien-Simpson NM, Snelgrove SL, Tsiros JT, Reynolds EC (2005) A novel Porphyromonas gingivalis FeoB plays a role in manganese accumulation. J Biol Chem 280:28095–28102

    CrossRef  PubMed  CAS  Google Scholar 

  24. Diaz-Mireles E, Wexler M, Sawers G, Bellini D, Todd JD, Johnston AW (2004) The Fur-like protein Mur of Rhizobium leguminosarum is a Mn2+-responsive transcriptional regulator. Microbiology 150:1447–1456

    CrossRef  PubMed  CAS  Google Scholar 

  25. Diaz-Mireles E, Wexler M, Todd JD, Bellini D, Johnston AW, Sawers RG (2005) The manganese-responsive repressor Mur of Rhizobium leguminosarum is a member of the Fur-superfamily that recognizes an unusual operator sequence. Microbiology 151:4071–4078

    CrossRef  PubMed  CAS  Google Scholar 

  26. Dintilhac A, Alloing G, Granadel C, Claverys JP (1997) Competence and virulence of Streptococcus pneumoniae: Adc and PsaA mutants exhibit a requirement for Zn and Mn resulting from inactivation of putative ABC metal permeases. Mol Microbiol 25:727–739

    CrossRef  PubMed  CAS  Google Scholar 

  27. Dintilhac A, Claverys JP (1997) The adc locus, which affects competence for genetic transformation in Streptococcus pneumoniae, encodes an ABC transporter with a putative lipoprotein homologous to a family of streptococcal adhesins. Res Microbiol 148:119–131

    CrossRef  PubMed  CAS  Google Scholar 

  28. Dornan D, Hupp TR (2001) Inhibition of p53-dependent transcription by BOX-I phospho-peptide mimetics that bind to p300. EMBO Rep 2:139–144

    CrossRef  PubMed  CAS  Google Scholar 

  29. Enkvetchakul D, Bhattacharyya J, Jeliazkova I, Groesbeck DK, Cukras CA, Nichols CG (2004) Functional characterization of a prokaryotic Kir channel. J Biol Chem 279:47076–47080

    CrossRef  PubMed  CAS  Google Scholar 

  30. Fleming MD, Romano MA, Su MA, Garrick LM, Garrick MD, Andrews NC (1998) Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proc Natl Acad Sci USA 95:1148–1153

    CrossRef  PubMed  CAS  Google Scholar 

  31. Fleming MD, Trenor CC, Su MA, Foernzler D, Beier DR, Dietrich WF, Andrews NC (1997) Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat Genet 16:383–386

    PubMed  CAS  Google Scholar 

  32. Forbes JR, Gros P (2003) Iron, manganese, and cobalt transport by Nramp1 (Slc11a1) and Nramp2 (Slc11a2) expressed at the plasma membrane. Blood 102:1884–1892

    CrossRef  PubMed  CAS  Google Scholar 

  33. Franzon VL, Arondel J, Sansonetti PJ (1990) Contribution of superoxide dismutase and catalase activities to Shigella flexneri pathogenesis. Infect Immun 58:529–535

    PubMed  CAS  Google Scholar 

  34. Garcia B, Latasa C, Solano C, Garcia-del PF, Gamazo C, Lasa I (2004) Role of the GGDEF protein family in Salmonella cellulose biosynthesis and biofilm formation. Mol Microbiol 54:264–277

    CrossRef  PubMed  CAS  Google Scholar 

  35. Garrick MD, Kuo HC, Vargas F, Singleton S, Zhao L, Smith JJ, Paradkar P, Roth JA, Garrick LM (2006a) Comparison of mammalian cell lines expressing distinct isoforms of divalent metal transporter 1 in a tetracycline-regulated fashion. Biochem J 398:539–546

    CrossRef  PubMed  CAS  Google Scholar 

  36. Garrick MD, Singleton ST, Vargas F, Kuo HC, Zhao L, Knopfel M, Davidson T, Costa M, Paradkar P, Roth JA, Garrick LM (2006b) DMT1: which metals does it transport? Biol Res 39:79–85

    CrossRef  PubMed  CAS  Google Scholar 

  37. Gat O, Mendelson I, Chitlaru T, Ariel N, Altboum Z, Levy H, Weiss S, Grosfeld H, Cohen S, Shafferman A (2005) The solute-binding component of a putative Mn(II) ABC transporter (MntA) is a novel Bacillus anthracis virulence determinant. Molec Microbiol 58:533–551

    CrossRef  CAS  Google Scholar 

  38. Gentry DR, Cashel M (1996) Mutational analysis of the Escherichia coli spoT gene identifies distinct but overlapping regions involved in ppGpp synthesis and degradation. Mol Microbiol 19:1373–1384

    CrossRef  PubMed  CAS  Google Scholar 

  39. Gentry DR, Hernandez VJ, Nguyen LH, Jensen DB, Cashel M (1993) Synthesis of the stationary-phase sigma factor ss is positively regulated by ppGpp. J Bacteriol 175:7982–7989

    PubMed  CAS  Google Scholar 

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

    CrossRef  PubMed  CAS  Google Scholar 

  41. Glynn AA, Bradley DJ, Blackwell JM, Plant JE (1982) Genetics of resistance to infection. Lancet 2:151

    CrossRef  PubMed  CAS  Google Scholar 

  42. Golynskiy MV, Davis TC, Helmann JD, Cohen SM (2005) Metal-induced structural organization and stabilization of the metalloregulatory protein MntR. Biochemistry 44:3380–3389

    CrossRef  PubMed  CAS  Google Scholar 

  43. Goswami T, Bhattacharjee A, Babal P, Searle S, Moore E, Li M, Blackwell JM (2001) Natural-resistance-associated macrophage protein 1 is an H+/bivalent cation antiporter. Biochem J 354:511–519

    CrossRef  PubMed  CAS  Google Scholar 

  44. Groot MN, Klaassens E, De Vos WM, Delcour J, Hols P, Kleerebezem M (2005) Genome-based in silico detection of putative manganese transport systems in Lactobacillus plantarum and their genetic analysis. Microbiology 151:1229–1238

    CrossRef  PubMed  CAS  Google Scholar 

  45. Gros P, Skamene E, Forget A (1983) Cellular mechanisms of genetically controlled host resistance to Mycobacterium bovis (BCG). J Immunol 131:1966–1972

    PubMed  CAS  Google Scholar 

  46. Gruenheid S, Cellier M, Vidal S, Gros P (1995) Identification and characterization of a second mouse Nramp gene. Genomics 25:514–525

    CrossRef  PubMed  CAS  Google Scholar 

  47. Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL, Hediger MA (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388:482–488

    CrossRef  PubMed  CAS  Google Scholar 

  48. Hao Z, Chen S, Wilson DB (1999a) Cloning, expression and characterization of cadmium and manganese uptake genes from Lactobacillus plantarum. Appl Environ Microbiol 65:4746–4752

    PubMed  CAS  Google Scholar 

  49. Hao Z, Reiske HR, Wilson DB (1999b) Characterization of cadmium uptake in Lactobacillus plantarum and isolation of cadmium and manganese uptake mutants. Appl Environ Microbiol 65:4741–4745

    PubMed  CAS  Google Scholar 

  50. Heinemeyer EA, Richter D (1978) Mechanism of the in vitro breakdown of guanosine 5′-diphosphate 3′-diphosphate in Escherichia coli. Proc Natl Acad Sci USA 75:4180–4183

    CrossRef  PubMed  CAS  Google Scholar 

  51. Hickman JW, Tifrea DF, Harwood CS (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci USA 102:14422–14427

    CrossRef  PubMed  CAS  Google Scholar 

  52. Hill PJ, Cockayne A, Landers P, Morrissey JA, Sims CM, Williams P (1998) SirR, a novel iron-dependent repressor in Staphylococcus epidermidis. Infect Immun 66:4123–4129

    PubMed  CAS  Google Scholar 

  53. Horsburgh MJ, Clements MO, Crossley H, Ingham E, Foster SJ (2001a) PerR controls oxidative stress resistance and iron storage proteins and is required for virulence in Staphylococcus aureus. Infect Immun 69:3744–3754

    CrossRef  PubMed  CAS  Google Scholar 

  54. Horsburgh MJ, Ingham E, Foster SJ (2001b) In Staphylococcus aureus, fur is an interactive regulator with PerR, contributes to virulence, and Is necessary for oxidative stress resistance through positive regulation of catalase and iron homeostasis. J Bacteriol 183:468–475

    CrossRef  PubMed  CAS  Google Scholar 

  55. Horsburgh MJ, Wharton SJ, Cox AG, Ingham E, Peacock S, Foster SJ (2002) MntR modulates expression of the PerR regulon and superoxide resistance in Staphylococcus aureus through control of manganese uptake. Mol Microbiol 44:1269–1286

    CrossRef  PubMed  CAS  Google Scholar 

  56. Ikeda JS, Janakiraman A, Kehres DG, Maguire ME, Slauch JM (2005) Transcriptional regulation of sitABCD of Salmonella enterica serovar Typhimurium by MntR and Fur. J Bacteriol 187:912–922

    CrossRef  PubMed  CAS  Google Scholar 

  57. 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 38:140–153

    CrossRef  PubMed  CAS  Google Scholar 

  58. Jakubovics NS, Smith AW, Jenkinson HF (2002) Oxidative stress tolerance is manganese (Mn2+) regulated in Streptococcus gordonii. Microbiology 148:3255–3263

    PubMed  CAS  Google Scholar 

  59. Janakiraman A, Slauch JM (2000) The putative iron transport system SitABCD encoded on SPI1 is required for full virulence of Salmonella typhimurium. Mol Microbiol 35:1146–1155

    CrossRef  PubMed  CAS  Google Scholar 

  60. Janulczyk R, Ricci S, Bjorck L (2003) MtsABC is important for manganese and iron transport, oxidative stress resistance, and virulence of Streptococcus pyogenes. Infect Immun 71:2656–2664

    CrossRef  PubMed  CAS  Google Scholar 

  61. Jenkinson HF (1994) Cell surface protein receptors in oral streptococci. FEMS Microbiol Lett 121:133–140

    CrossRef  PubMed  CAS  Google Scholar 

  62. Kehres DG, Janakiraman A, Slauch JM, Maguire ME (2002a) Regulation of Salmonella enterica serovar Typhimurium mntH transcription by H2O2, Fe2+, and Mn2+. J Bacteriol 184:3151–3158

    CrossRef  PubMed  CAS  Google Scholar 

  63. Kehres DG, Janakiraman A, Slauch JM, Maguire ME (2002b) SitABCD Is the alkaline Mn2+transporter of Salmonella enterica serovar Typhimurium. J Bacteriol 184:3159–3166

    CrossRef  PubMed  CAS  Google Scholar 

  64. Kehres DG, Zaharik ML, Finlay BB, Maguire ME (2000) The NRAMP proteins of Sal- monella typhimurium and Escherichia coli are selective manganese transporters involved in the response to reactive oxygen. Molec Microbiol 36:1085–1100

    CrossRef  CAS  Google Scholar 

  65. Kitten T, Munro CL, Michalek SM, Macrina FL (2000) Genetic characterization of a Streptococcus mutans LraI family operon and role in virulence. Infect Immun 68:4441–4451

    CrossRef  PubMed  CAS  Google Scholar 

  66. Kliegman JI, Griner SL, Helmann JD, Brennan RG, Glasfeld A (2006) Structural basis for the metal-selective activation of the manganese transport regulator of Bacillus subtilis. Biochemistry 45:3493–3505

    CrossRef  PubMed  CAS  Google Scholar 

  67. Kolenbrander PE, Andersen RN, Baker RA, Jenkinson HF (1998) The adhesion-associated sca operon in Streptococcus gordonii encodes an inducible high-affinity ABC transporter for Mn2+uptake. J Bacteriol 180:290–295

    PubMed  CAS  Google Scholar 

  68. Lee JW, Helmann JD (2006a) Biochemical characterization of the structural Zn2+site in the Bacillus subtilis peroxide sensor PerR. J Biol Chem 281:23567–23578

    CrossRef  PubMed  CAS  Google Scholar 

  69. Lee JW, Helmann JD (2006b) The PerR transcription factor senses H2O2by metal-catalysed histidine oxidation. Nature 440:363–367

    CrossRef  PubMed  CAS  Google Scholar 

  70. Lieser SA, Davis TC, Helmann JD, Cohen SM (2003) DNA-binding and oligomerization studies of the manganese(II) metalloregulatory protein MntR from Bacillus subtilis. Biochemistry 42:12634–12642

    CrossRef  PubMed  CAS  Google Scholar 

  71. Loo CY, Mitrakul K, Voss IB, Hughes CV, Ganeshkumar N (2003) Involvement of the adc operon and manganese homeostasis in Streptococcus gordonii biofilm formation. J Bacteriol 185:2887

    CrossRef  PubMed  CAS  Google Scholar 

  72. Low YL, Jakubovics NS, Flatman JC, Jenkinson HF, Smith AW (2003) Manganese-dependent regulation of the endocarditis-associated virulence factor EfaA of Enterococcus faecalis. J Med Microbiol 52:113–119

    CrossRef  PubMed  CAS  Google Scholar 

  73. Lower BH, Kennelly PJ (2002) The membrane-associated protein-serine/threonine kinase from Sulfolobus solfataricus is a glycoprotein. J Bacteriol 184:2614–2619

    CrossRef  PubMed  CAS  Google Scholar 

  74. Lower BH, Kennelly PJ (2003) Open reading frame sso2387 from the archaeon Sulfolobus solfataricus encodes a polypeptide with protein-serine kinase activity. J Bacteriol 185:3436–3445

    CrossRef  PubMed  CAS  Google Scholar 

  75. Lucchini S, Liu H, Jin Q, Hinton JC, Yu J (2005) Transcriptional adaptation of Shigella flexneri during infection of macrophages and epithelial cells: insights into the strategies of a cytosolic bacterial pathogen. Infect Immun 73:88–102

    CrossRef  PubMed  CAS  Google Scholar 

  76. Makui H, Roig E, Cole ST, Helmann JD, Gros P, Cellier MF (2000) Identification of the Escherichia coli K-12 NRAMP orthologue (MntH) as a selective divalent metal ion transporter. Mol Microbiol 35:1065–1078

    CrossRef  PubMed  CAS  Google Scholar 

  77. Marra A, Lawson S, Asundi JS, Brigham D, Hromockyj AE (2002) In vivo characterization of the psa genes from Streptococcus pneumoniae in multiple models of infection. Microbiology 148:1483–1491

    PubMed  CAS  Google Scholar 

  78. Missiakas D, Raina S (1997) Signal transduction pathways in response to protein misfolding in the extracytoplasmic compartments of E. coli: role of two new phosphoprotein phosphatases PrpA and PrpB. EMBO J 16:1670–1685

    CrossRef  PubMed  CAS  Google Scholar 

  79. Morona JK, Morona R, Miller DC, Paton JC (2002) Streptococcus pneumoniae capsule biosynthesis protein CpsB is a novel manganese-dependent phosphotyrosine-protein phosphatase. J Bacteriol 184:577–583

    CrossRef  PubMed  CAS  Google Scholar 

  80. Mukhopadhyay S, Kapatral V, Xu W, Chakrabarty AM (1999) Characterization of a Hank's type serine/threonine kinase and serine/threonine phosphoprotein phosphatase in Pseudomonas aeruginosa. J Bacteriol 181:6615–6622

    PubMed  CAS  Google Scholar 

  81. Najdenski HM, Golkocheva EN, Vesselinova AM, Russmann H (2004) Comparison of the course of infection of virulent Yersinia enterocolitica serotype O:8 with an isogenic sodA mutant in the peroral rabbit model. Int J Med Microbiol 294:383–393

    CrossRef  PubMed  Google Scholar 

  82. Oetjen J, Fives-Taylor P, Froeliger EH (2002) The divergently transcribed Streptococcus parasanguis virulence-associated fimA operon encoding an Mn2+-responsive metal transporter and pepO encoding a zinc metallopeptidase are not coordinately regulated. Infect Immun 70:5706–5714

    CrossRef  PubMed  CAS  Google Scholar 

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

    CrossRef  PubMed  CAS  Google Scholar 

  84. Paik S, Brown A, Munro CL, Cornelissen CN, Kitten T (2003) The sloABCR operon of Streptococcus mutans encodes an Mn and Fe transport system required for endocarditis virulence and its Mn-dependent repressor. J Bacteriol 185:5967–5975

    CrossRef  PubMed  CAS  Google Scholar 

  85. Patzer SI, Hantke K (2001) Dual repression by Fe2+-Fur and Mn2+-MntR of the mntH gene, encoding an NRAMP-like Mn2+transporter in Escherichia coli. J Bacteriol 183:4806–4813

    CrossRef  PubMed  CAS  Google Scholar 

  86. Plant J, Glynn AA (1974) Natural resistance to Salmonella infection, delayed hypersensitivity and Ir genes in different strains of mice. Nature 248:345–347

    CrossRef  PubMed  CAS  Google Scholar 

  87. Plant J, Glynn AA (1979) Locating Salmonella resistance gene on mouse chromosome 1. Clin Exp Immunol 37:1–6

    PubMed  CAS  Google Scholar 

  88. Plant JE, Blackwell JM, O'Brien AD, Bradley DJ, Glynn AA (1982) Are the Lsh and Ity disease resistance genes at one locus on mouse chromosome 1? Nature 297:510–511

    CrossRef  PubMed  CAS  Google Scholar 

  89. Platero R, Peixoto L, O'Brian MR, Fabiano E (2004) Fur is involved in manganese-dependent regulation of mntA (sitA) expression in Sinorhizobium meliloti. Appl Environ Microbiol 70:4349–4355

    CrossRef  PubMed  CAS  Google Scholar 

  90. Platero RA, Jaureguy M, Battistoni FJ, Fabiano ER (2003) Mutations in sitB and sitD genes affect manganese-growth requirements in Sinorhizobium meliloti. FEMS Microbiol Lett 218:65–70

    CrossRef  PubMed  CAS  Google Scholar 

  91. Polakis SE, Guchhait RB, Lane MD (1973) Stringent control of fatty acid synthesis in Escherichia coli. Possible regulation of acetyl coenzyme A carboxylase by ppGpp. J Biol Chem 248:7957–7966

    PubMed  CAS  Google Scholar 

  92. Qiu X, Pohl E, Holmes RK, Hol WG (1996) High-resolution structure of the diphtheria toxin repressor complexed with cobalt and manganese reveals an SH3-like third domain and suggests a possible role of phosphate as co-corepressor. Biochemistry 35:12292–12302

    CrossRef  PubMed  CAS  Google Scholar 

  93. 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 35:1454–1468

    CrossRef  PubMed  CAS  Google Scholar 

  94. Rajagopal L, Clancy A, Rubens CE (2003) A eukaryotic type serine/threonine kinase and phosphatase in Streptococcus agalactiae reversibly phosphorylate an inorganic pyrophosphatase and affect growth, cell segregation, and virulence. J Biol Chem 278:14429–14441

    CrossRef  PubMed  CAS  Google Scholar 

  95. Reeve I, Hummell D, Nelson N, Voss J (2002) Overexpression, purification, and site-directed spin labeling of the Nramp metal transporter from Mycobacterium leprae. Proc Natl Acad Sci USA 99:8608–8613

    CrossRef  PubMed  CAS  Google Scholar 

  96. Ricci S, Janulczyk R, Bjorck L (2002) The regulator PerR is involved in oxidative stress response and iron homeostasis and is necessary for full virulence of Streptococcus pyogenes. Infect Immun 70:4968–4976

    CrossRef  PubMed  CAS  Google Scholar 

  97. Richer E, Courville P, Bergevin I, Cellier MF (2003) Horizontal gene transfer of “prototype” Nramp in bacteria. J Mol Evol 57:363–376

    CrossRef  PubMed  CAS  Google Scholar 

  98. Roggenkamp A, Bittner T, Leitritz L, Sing A, Heesemann J (1997) Contribution of the Mn-cofactored superoxide dismutase (SodA) to the virulence of Yersinia enterocolitica serotype O8. Infect Immun 65:4705–4710

    PubMed  CAS  Google Scholar 

  99. Runyen-Janecky LJ, Payne SM (2002) Identification of chromosomal Shigella flexneri genes induced by the eukaryotic intracellular environment. Infect Immun 70:4379–4388

    CrossRef  PubMed  CAS  Google Scholar 

  100. Runyen-Janecky LJ, Reeves SA, Gonzales EG, Payne SM (2003) Contribution of the Shigella flexneri Sit, Iuc, and Feo iron acquisition systems to iron acquisition in vitro and in cultured cells. Infect Immun 71:1919–1928

    CrossRef  PubMed  CAS  Google Scholar 

  101. Runyen-Janecky L, Dazenski E, Hawkins S, Warner L (2006) Role and Regulation of the Shigella flexneri Sit and MntH Systems. Infect Immun 74:4666–4672

    CrossRef  PubMed  CAS  Google Scholar 

  102. Sacher A, Cohen A, Nelson N (2001) Properties of the mammalian and yeast metal-ion transporters DCT1 and Smf1p expressed in Xenopus laevis oocytes. J Exp Biol 204:1053–1061

    PubMed  CAS  Google Scholar 

  103. Sarubbi E, Rudd KE, Xiao H, Ikehara K, Kalman M, Cashel M (1989) Characterization of the spoT gene of Escherichia coli. J Biol Chem 264:15074–15082

    PubMed  CAS  Google Scholar 

  104. Schmidt AJ, Ryjenkov DA, Gomelsky M (2005) The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J Bacteriol 187:4774–4781

    CrossRef  PubMed  CAS  Google Scholar 

  105. Schmitt MP (2002) Analysis of a DtxR-like metalloregulatory protein, MntR, from Corynebacterium diphtheriae that controls expression of an ABC metal transporter by an Mn2+-dependent mechanism. J Bacteriol 184:6882–6892

    CrossRef  PubMed  CAS  Google Scholar 

  106. Sen KI, Sienkiewicz A, Love JF, vanderSpek JC, Fajer PG, Logan TM (2006) Mn(II) binding by the anthracis repressor from Bacillus anthracis. Biochemistry 45:4295–4303

    CrossRef  PubMed  CAS  Google Scholar 

  107. Shi L (2004) Manganese-dependent protein O-phosphatases in prokaryotes and their biological functions. Front Biosci 9:1382–1397

    CrossRef  PubMed  CAS  Google Scholar 

  108. Shi L, Carmichael WW, Kennelly PJ (1999) Cyanobacterial PPP family protein phosphatases possess multifunctional capabilities and are resistant to microcystin-LR. J Biol Chem 274:10039–10046

    CrossRef  PubMed  CAS  Google Scholar 

  109. 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

    CrossRef  PubMed  CAS  Google Scholar 

  110. Simm R, Fetherston JD, Kader A, Romling U, Perry RD (2005) Phenotypic convergence mediated by GGDEF-domain-containing proteins. J Bacteriol 187:6816–6823

    CrossRef  PubMed  CAS  Google Scholar 

  111. Singh KV, Coque TM, Weinstock GM, Murray BE (1998) In vivo testing of an Enterococcus faecalis efaA mutant and use of efaA homologs for species identification. FEMS Immunol Med Microbiol 21:323–331

    PubMed  CAS  Google Scholar 

  112. Sy J (1977) In vitro degradation of guanosine 5′-diphosphate, 3′-diphosphate. Proc Natl Acad Sci USA 74:5529–5533

    CrossRef  PubMed  CAS  Google Scholar 

  113. Tamayo R, Tischler AD, Camilli A (2005) The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J Biol Chem 280:33324–33330

    CrossRef  PubMed  CAS  Google Scholar 

  114. Tao X, Zeng HY, Murphy JR (1995) Transition metal ion activation of DNA binding by the diphtheria tox repressor requires the formation of stable homodimers. Proc Natl Acad Sci USA 92:6803–6807

    CrossRef  PubMed  CAS  Google Scholar 

  115. Tischler AD, Camilli A (2004) Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53:857–869

    CrossRef  PubMed  CAS  Google Scholar 

  116. Tischler AD, Camilli A (2005) Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect Immun 73:5873–5882

    CrossRef  PubMed  CAS  Google Scholar 

  117. Tsolis RM, Baumler AJ, Heffron F (1995) Role of Salmonella typhimurium Mn-superoxide dismutase (SodA) in protection against early killing by J774 macrophages. Infect Immun 63:1739–1744

    PubMed  CAS  Google Scholar 

  118. Udo H, Inouye M, Inouye S (1997) Biochemical characterization of Pkn2, a protein Ser/Thr kinase from Myxococcus xanthus, a Gram-negative developmental bacterium. FEBS Lett 400:188–192

    CrossRef  PubMed  CAS  Google Scholar 

  119. Vidal S, Belouchi AM, Cellier M, Beatty B, Gros P (1995a) Cloning and characterization of a second human NRAMP gene on chromosome 12q13. Mamm Genome 6:224–230

    CrossRef  PubMed  CAS  Google Scholar 

  120. Vidal S, Gros P, Skamene E (1995b) Natural resistance to infection with intracellular parasites: molecular genetics identifies Nramp1 as the Bcg/Ity/Lsh locus. J Leukoc Biol 58:382–390

    PubMed  CAS  Google Scholar 

  121. Vidal SM, Malo D, Vogan K, Skamene E, Gros P (1993) Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg. Cell 73:469–485

    CrossRef  PubMed  CAS  Google Scholar 

  122. Wu HJ, Seib KL, Srikhanta YN, Kidd SP, Edwards JL, Maguire TL, Grimmond SM, Apicella MA, McEwan AG, Jennings MP (2006) PerR controls Mn-dependent resistance to oxidative stress in Neisseria gonorrhoeae. Mol Microbiol 60:401–416

    CrossRef  PubMed  CAS  Google Scholar 

  123. Zaharik ML (2003) Host-Pathogen Interactions: The Impact of Nramp1 on Salmonella Enterica Serovar Typhimurium Virulence Gene Expression, Ph.D. Thesis, Univ. British Columbia

    Google Scholar 

  124. Zaharik ML, Finlay BB (2004) Mn2+and bacterial pathogenesis. Front Biosci 9:1035–1042

    CrossRef  PubMed  CAS  Google Scholar 

  125. Zaharik ML, Gruenheid S, Perrin AJ, Finlay BB (2002a) Delivery of dangerous goods: type III secretion in enteric pathogens. Int J Med Microbiol 291:593–603

    CrossRef  PubMed  CAS  Google Scholar 

  126. Zaharik ML, Vallance BA, Puente JL, Gros P, Finlay BB (2002b) Host-pathogen interactions: Host resistance factor Nramp1 up-regulates the expression of Salmonella pathogenicity island-2 virulence genes. Proc Natl Acad Sci USA 99:15705–15710

    CrossRef  PubMed  CAS  Google Scholar 

  127. Zaharik ML, Cullen VL, Fung AM, Libby SJ, Kujat Choy SL, Coburn B, Kehres DG, Maguire ME, Fang FC, Finlay BB (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

    CrossRef  PubMed  CAS  Google Scholar 

  128. Zwilling BS, Hilburger ME (1994) Macrophage resistance genes: Bcg/Ity/Lsh. Immunol Ser 60:233–245

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pharmacology, Case School of Medicine,Case Western Reserve University, 10900 Euclid Avenue, OH 44106-4965, Cleveland, USA

    Krisztina M. Papp-Wallace, Andrea S. Moomaw & Michael E. Maguire

Authors
  1. Krisztina M. Papp-Wallace
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea S. Moomaw
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael E. Maguire
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael E. Maguire .

Editor information

Dietrich H. Nies Simon Silver

Rights and permissions

Reprints and permissions

Copyright information

© 2007 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Papp-Wallace, K.M., Moomaw, A.S., Maguire, M.E. (2007). Manganese: Uptake, Biological Function, and Role in Virulence. In: Nies, D.H., Silver, S. (eds) Molecular Microbiology of Heavy Metals. Microbiology Monographs, vol 6. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7171_2006_080

Download citation

Publish with us

Policies and ethics

search

Navigation