Skip to main content

Mechanisms and Regulation of Iron Homeostasis in the Rhizobia

  • Chapter
  • First Online:

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

Abstract

Rhizobia are soil bacteria belonging to different genera whose most conspicuous characteristic is the ability to establish a symbiotic association with legumes and carry out nitrogen fixation. The success of these organisms in the rhizosphere or within the host plant involves the ability to sense the environment to assess the availability of nutrients, and to optimize cellular systems for their acquisition. Iron in natural habitats is mostly inaccessible due to low solubility, and microorganisms must compete for this limited nutrient. In addition to their agricultural and economic importance, rhizobia are model organisms that have given new insights into related, but less tractable animal pathogens. In particular, genetic control of iron homeostasis in the rhizobia and other α-Proteobacteria has moved away from the Fur paradigm to an iron sensing mechanism responding to the metal indirectly. Moreover, utilization of heme as an iron source is not unique to animal pathogens, and the rhizobial strategy reveals some interesting novel features. This chapter reviews advances in our understanding of iron metabolism in rhizobia.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   34.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   49.95
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Ahn BE, Cha J, Lee EJ, Han AR, Thompson CJ, Roe JH (2006) Nur, a nickel-responsive regulator of the Fur family, regulates superoxide dismutases and nickel transport in Streptomyces coelicolor. Mol Microbiol 59:1848–1858

    CAS  Google Scholar 

  • Altuvia S, Almiron M, Huisman G, Kolter R, Storz G (1994) The dps promoter is activated by OxyR during growth and by IHF and sigma S in stationary phase. Mol Microbiol 13:265–272

    CAS  Google Scholar 

  • Altuvia S, Weinstein-Fischer D, Zhang A, Postow L, Storz G (1997) A small, stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell 90:43–53

    CAS  Google Scholar 

  • Amarelle V, Koziol U, Rosconi F, Noya F, O’Brian MR, Fabiano E (2010) A new small regulatory protein, HmuP, modulates haemin acquisition in Sinorhizobium meliloti. Microbiology 156:1873–1882

    CAS  Google Scholar 

  • Amarelle V, O’Brian MR, Fabiano E (2008) ShmR is essential for utilization of heme as a nutritional iron source in Sinorhizobium meliloti. Appl Environ Microbiol 74:6473–6475

    CAS  Google Scholar 

  • Anderson ES, Paulley JT, Gaines JM, Valderas MW, Martin DW, Menscher E, Brown TD, Burns CS, Roop RM 2nd (2009) The manganese transporter MntH is a critical virulence determinant for Brucella abortus 2308 in experimentally infected mice. Infect Immun 77:3466–3474

    CAS  Google Scholar 

  • Anderson ES, Paulley JT, Martinson DA, Gaines JM, Steele KH, Roop RM II (2011) The iron-responsive regulator Irr Is required for wild-type expression of the gene encoding the heme transporter BhuA in Brucella abortus 2308. J Bacteriol 193:5359–5364

    CAS  Google Scholar 

  • Anjem A, Imlay JA (2012) Mononuclear iron enzymes are primary targets of hydrogen peroxide stress. J Biol Chem 287:15544–15556

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Baginsky C, Brito B, Imperial J, Palacios JM, Ruiz-Argueso T (2002) Diversity and evolution of hydrogenase systems in rhizobia. Appl Environ Microbiol 68:4915–4924

    CAS  Google Scholar 

  • Baichoo N, Helmann JD (2002) Recognition of DNA by Fur: a reinterpretation of the Fur box consensus sequence. J Bacteriol 184:5826–5832

    CAS  Google Scholar 

  • Barnard A, Wolfe A, Busby S (2004) Regulation at complex bacterial promoters: how bacteria use different promoter organizations to produce different regulatory outcomes. Curr Opin Microbiol 7:102–108

    CAS  Google Scholar 

  • Barsomian GD, Urzainqui A, Lohman K, Walker GC (1992) Rhizobium meliloti mutants unable to synthesize anthranilate display a novel symbiotic phenotype. J Bacteriol 174:4416–4426

    CAS  Google Scholar 

  • Battisti JM, Smitherman LS, Sappington KN, Parrow NL, Raghavan R, Minnick MF (2007) Transcriptional regulation of the heme binding protein gene family of Bartonella quintana is accomplished by a novel promoter element and iron response regulator. Infect Immun 75:4373–4385

    CAS  Google Scholar 

  • Battistoni F, Platero R, Duran R, Cervenansky C, Battistoni J, Arias A, Fabiano E (2002a) Identification of an iron-regulated, hemin-binding outer membrane protein in Sinorhizobium meliloti. Appl Environ Microbiol 68:5877–5881

    CAS  Google Scholar 

  • Battistoni F, Platero R, Noya F, Arias A, Fabiano E (2002b) Intracellular Fe content influences nodulation competitiveness of Sinorhizobium meliloti strains as inocula of alfalfa. Soil Biol Biochem 34:593–597

    CAS  Google Scholar 

  • Bellini P, Hemmings AM (2006) In vitro characterization of a bacterial manganese uptake regulator of the Fur superfamily. Biochemistry 45:2686–2698

    CAS  Google Scholar 

  • Benson HP, Boncompagni E, Guerinot ML (2005) An iron uptake operon required for proper nodule development in the Bradyrhizobium japonicum-soybean symbiosis. Mol Plant Microbe Interact 18:950–959

    CAS  Google Scholar 

  • Benson HP, LeVier K, Guerinot ML (2004) A dominant-negative fur mutation in Bradyrhizobium japonicum. J Bacteriol 186:1409–1414

    CAS  Google Scholar 

  • Berlett BS, Stadtman ER (1997) Protein oxidation in aging, disease and oxidative stress. J Biol Chem 272:20313–20316

    CAS  Google Scholar 

  • Bsat N, Herbig A, Casillas-Martinez L, Setlow P, Helmann JD (1998) Bacillus subtilis contains multiple Fur homologs: identification of the iron uptake (Fur) and peroxide regulon (PerR) repressors. Mol Microbiol 29:189–198

    CAS  Google Scholar 

  • Burkhardt R, Braun V (1987) Nucleotide sequence of the fhuC and fhuD genes involved in iron (III) hydroxamate transport: domains in FhuC homologous to ATP-binding proteins. Mol Gen Genet 209:49–55

    CAS  Google Scholar 

  • Butcher BG, Bronstein PA, Myers CR, Stodghill PV, Bolton JJ, Markel EJ, Filiatrault MJ, Swingle B, Gaballa A, Helmann JD, Schneider DJ, Cartinhour SW (2011) Characterization of the fur regulon in Pseudomonas syringae pv. tomato DC3000. J Bacteriol 193:4598–4611

    CAS  Google Scholar 

  • Carlton TM, Sullivan JT, Stuart GS, Hutt K, Lamont IL, Ronson CW (2007) Ferrichrome utilization in a mesorhizobial population: microevolution of a three-locus system. Environ Microbiol 9:2923–2932

    CAS  Google Scholar 

  • Carson KC, Meyer J-M, Dilworth MJ (2000) Hydroxamate siderophores of root nodule bacteria. Soil Biol Biochem 32:11–21

    CAS  Google Scholar 

  • Carter RA, Worsley PS, Sawers G, Challis GL, Dilworth MJ, Carson KC, Lawrence JA, Wexler M, Johnston AW, Yeoman KH (2002) The vbs genes that direct synthesis of the siderophore vicibactin in Rhizobium leguminosarum: their expression in other genera requires ECF sigma factor RpoI. Mol Microbiol 44:1153–1166

    CAS  Google Scholar 

  • Cescau S, Cwerman H, Letoffe S, Delepelaire P, Wandersman C, Biville F (2007) Heme acquisition by hemophores. Biometals 20:603–613

    CAS  Google Scholar 

  • Challis GL (2005) A widely distributed bacterial pathway for siderophore biosynthesis independent of nonribosomal peptide synthetases. ChemBioChem 6:601–611

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Chao TC, Buhrmester J, Hansmeier N, Puhler A, Weidner S (2005) Role of the regulatory gene rirA in the transcriptional response of Sinorhizobium meliloti to iron limitation. Appl Environ Microbiol 71:5969–5982

    CAS  Google Scholar 

  • Chauhan S, Titus DE, O’Brian MR (1997) Metals control activity and expression of the heme biosynthesis enzyme δ-aminolevulinic acid dehydratase in Bradyrhizobium japonicum. J Bacteriol 179:5516–5520

    CAS  Google Scholar 

  • Chen L, Keramati L, Helmann JD (1995) Coordinate regulation of Bacillus subtilis peroxide stress genes by hydrogen peroxide and metal ions. Proc Natl Acad Sci U S A 92:8190–8194

    CAS  Google Scholar 

  • Chen WM, Moulin L, Bontemps C, Vandamme P, Bena G, Boivin-Masson C (2003) Legume symbiotic nitrogen fixation by beta-proteobacteria is widespread in nature. J Bacteriol 185:7266–7272

    CAS  Google Scholar 

  • Christman MF, Storz G, Ames BN (1989) OxyR, a positive regulator of hydrogen peroxide-inducible genes in Escherichia coli and Salmonella typhimurium, is homologous to a family of bacterial regulatory proteins. Proc Natl Acad Sci U S A 86:3484–3488

    CAS  Google Scholar 

  • Claverys JP (2001) A new family of high-affinity ABC manganese and zinc permeases. Res Microbiol 152:231–243

    CAS  Google Scholar 

  • Cornelis P, Matthijs S, Van Oeffelen L (2009) Iron uptake regulation in Pseudomonas aeruginosa. Biometals 22:15–22

    CAS  Google Scholar 

  • Coulton JW, Mason P, Allatt DD (1987) fhuC and fhuD genes for iron (III)-ferrichrome transport into Escherichia coli K-12. J Bacteriol 169:3844–3849

    CAS  Google Scholar 

  • Cuiv PO, Clarke P, Lynch D, O’Connell M (2004) Identification of rhtX and fptX, novel genes encoding proteins that show homology and function in the utilization of the siderophores rhizobactin 1021 by Sinorhizobium meliloti and pyochelin by Pseudomonas aeruginosa, respectively. J Bacteriol 186:2996–3005

    CAS  Google Scholar 

  • Cuiv PO, Keogh D, Clarke P, O’Connell M (2008) The hmuUV genes of Sinorhizobium meliloti 2011 encode the permease and ATPase components of an ABC transport system for the utilization of both haem and the hydroxamate siderophores, ferrichrome and ferrioxamine B. Mol Microbiol 70:1261–1273

    CAS  Google Scholar 

  • Dancis A, Klausner RD, Hinnebusch AG, Barriocanal JG (1990) Genetic evidence that ferric reductase is required for iron uptake in Saccharomyces cerevisiae. Mol Cell Biol 10:2294–2301

    CAS  Google Scholar 

  • Danielli A, Roncarati D, Delany I, Chiarini V, Rappuoli R, Scarlato V (2006) In vivo dissection of the Helicobacter pylori Fur regulatory circuit by genome-wide location analysis. J Bacteriol 188:4654–4662

    CAS  Google Scholar 

  • Davies BW, Walker GC (2007) Disruption of sitA compromises Sinorhizobium meliloti for manganese uptake required for protection against oxidative stress. J Bacteriol 189:2101–2109

    CAS  Google Scholar 

  • Degen O, Eitinger T (2002) Substrate specificity of nickel/cobalt permeases: insights from mutants altered in transmembrane domains I and II. J Bacteriol 184:3569–3577

    CAS  Google Scholar 

  • Delany I, Rappuoli R, Scarlato V (2004) Fur functions as an activator and as a repressor of putative virulence genes in Neisseria meningitidis. Mol Microbiol 52:1081–1090

    CAS  Google Scholar 

  • Delany I, Spohn G, Rappuoli R, Scarlato V (2001) The Fur repressor controls transcription of iron-activated and -repressed genes in Helicobacter pylori. Mol Microbiol 42:1297–1309

    CAS  Google Scholar 

  • Delany I, Spohn G, Rappuoli R, Scarlato V (2003) An anti-repression Fur operator upstream of the promoter is required for iron-mediated transcriptional autoregulation in Helicobacter pylori. Mol Microbiol 50:1329–1338

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Dilworth MJ (1980) [74] Leghemoglobins. In: Methods in enzymology, Vol 69. Academic Press, Salt Lake City, pp 812–823

    Google Scholar 

  • Dilworth MJ, Carson KC, Giles RGF, Byrne LT, Glenn AR (1998) Rhizobium leguminosarum bv. viciae produces a novel cyclic trihydroxamate siderophore, vicibactin. Microbiology 144:781–791

    CAS  Google Scholar 

  • Domenech P, Pym AS, Cellier M, Barry CE 3rd, Cole ST (2002) Inactivation of the Mycobacterium tuberculosis Nramp orthologue (mntH) does not affect virulence in a mouse model of tuberculosis. FEMS Microbiol Lett 207:81–86

    CAS  Google Scholar 

  • Donadio S, Monciardini P, Sosio M (2007) Polyketide synthases and nonribosomal peptide synthetases: the emerging view from bacterial genomics. Nat Prod Rep 24:1073–1109

    CAS  Google Scholar 

  • Downie JA, Walker SA (1999) Plant responses to nodulation factors. Curr Opin Plant Biol 2:483–489

    CAS  Google Scholar 

  • Elgrably-Weiss M, Park S, Schlosser-Silverman E, Rosenshine I, Imlay J, Altuvia S (2002) A Salmonella enterica serovar typhimuriumhemA mutant is highly susceptible to oxidative DNA damage. J Bacteriol 184:3774–3784

    CAS  Google Scholar 

  • Enz S, Mahren S, Stroeher UH, Braun V (2000) Surface signaling in ferric citrate transport gene induction: interaction of the FecA, FecR, and FecI regulatory proteins. J Bacteriol 182:637–646

    CAS  Google Scholar 

  • Ernst FD, Bereswill S, Waidner B, Stoof J, Mäder U, Kusters JG, Kuipers EJ, Kist M, van Vliet AHM, Homuth G (2005a) Transcriptional profiling of Helicobacter pylori Fur- and iron-regulated gene expression. Microbiology 151:533–546

    CAS  Google Scholar 

  • Ernst FD, Homuth G, Stoof J, Mäder U, Waidner B, Kuipers EJ, Kist M, Kusters JG, Bereswill S, van Vliet AHM (2005b) Iron-responsive regulation of the Helicobacter pylori iron-cofactored superoxide dismutase SodB Is mediated by Fur. J Bacteriol 187:3687–3692

    CAS  Google Scholar 

  • Escamilla-Hernandez R, O’Brian MR (2012) HmuP is a co-activator of Irr-dependent expression of heme utilization genes in Bradyrhizobium japonicum. J Bacteriol 194:3137–3143

    CAS  Google Scholar 

  • Escolar L, Perez-Martin J, de Lorenzo V (1998) Binding of the fur (ferric uptake regulator) repressor of Escherichia coli to arrays of the GATAAT sequence. J Mol Biol 283:537–547

    CAS  Google Scholar 

  • Escolar L, Perez-Martin J, de Lorenzo V (1999) Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181:6223–6229

    CAS  Google Scholar 

  • Ettema TJG, Andersson SGE (2009) The α-proteobacteria: the Darwin finches of the bacterial world. Biol Lett 5:429–432

    Google Scholar 

  • Expert D, Gill PRJ (1992) Iron: a modulator in bacterial virulence and symbiotic nitrogen-fixation. CRC Press, Boca Raton

    Google Scholar 

  • Fabiano E, Gill PR Jr, Noya F, Bagnasco P, De La Fuente L, Arias A (1995) Siderophore-mediated iron acquisition mutants in Rhizobium meliloti 242 and its effect on the nodulation kinetic of alfalfa nodules. Symbiosis 19:197–211

    CAS  Google Scholar 

  • Finking R, Marahiel MA (2004) Biosynthesis of nonribosomal peptides1. Annu Rev Microbiol 58:453–488

    CAS  Google Scholar 

  • Friedman DB, Stauff DL, Pishchany G, Whitwell CW, Torres VJ, Skaar EP (2006) Staphylococcus aureus redirects central metabolism to increase iron availability. PLoS Pathog 2:e87

    Google Scholar 

  • Friedman YE, O’Brian MR (2003) A novel DNA-binding site for the ferric uptake regulator (Fur) protein from Bradyrhizobium japonicum. J Biol Chem 278:38395–38401

    CAS  Google Scholar 

  • Friedman YE, O’Brian MR (2004) The ferric uptake regulator (Fur) protein from Bradyrhizobium japonicum is an iron-responsive transcriptional repressor in vitro. J Biol Chem 279:32100–32105

    CAS  Google Scholar 

  • Gaballa A, Antelmann H, Aguilar C, Khakh SK, Song K-B, Smaldone GT, Helmann JD (2008) The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small, basic proteins. Proc Natl Acad Sci U S A 105:11927–11932

    CAS  Google Scholar 

  • Gaballa A, Helmann JD (1998) Identification of a zinc-specific metalloregulatory protein, Zur, controlling zinc transport operons in Bacillus subtilis. J Bacteriol 180:5815–5821

    CAS  Google Scholar 

  • Gao H, Zhou D, Li Y, Guo Z, Han Y, Song Y, Zhai J, Du Z, Wang X, Lu J, Yang R (2008) The iron-responsive Fur regulon in Yersinia pestis. J Bacteriol 190:3063–3075

    CAS  Google Scholar 

  • Genco CA, Dixon DW (2001) Emerging strategies in microbial haem capture. Mol Microbiol 39:1–11

    CAS  Google Scholar 

  • Georgiadis MM, Komiya H, Chakrabarti P, Woo D, Kornuc JJ, Rees DC (1992) Crystallographic structure of the nitrogenase iron protein from Azotobacter vinelandii. Science 257:1653–1659

    CAS  Google Scholar 

  • Gibson KE, Kobayashi H, Walker GC (2008) Molecular determinants of a symbiotic chronic infection. Annu Rev Genet 42:413–441

    CAS  Google Scholar 

  • Giel JL, Rodionov D, Liu M, Blattner FR, Kiley PJ (2006) IscR-dependent gene expression links iron-sulphur cluster assembly to the control of O2-regulated genes in Escherichia coli. Mol Microbiol 60:1058–1075

    CAS  Google Scholar 

  • Gill PR Jr, Neilands JB (1989) Cloning a genomic region required for a high-affinity iron-uptake system in Rhizobium meliloti 1021. Mol Microbiol 3:1183–1189

    CAS  Google Scholar 

  • Giraud E, Fardoux J, Fourrier N, Hannibal L, Genty B, Bouyer P, Dreyfus B, Vermeglio A (2002) Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria. Nature 417:202–205

    CAS  Google Scholar 

  • Giraud E, Hannibal L, Fardoux J, Vermeglio A, Dreyfus B (2000) Effect of Bradyrhizobium photosynthesis on stem nodulation of Aeschynomene sensitiva. Proc Natl Acad Sci U S A 97:14795–14800

    CAS  Google Scholar 

  • Grifantini R, Frigimelica E, Delany I, Bartolini E, Giovinazzi S, Balloni S, Agarwal S, Galli G, Genco C, Grandi G (2004) Characterization of a novel Neisseria meningitidis Fur and iron-regulated operon required for protection from oxidative stress: utility of DNA microarray in the assignment of the biological role of hypothetical genes. Mol Microbiol 54:962–979

    CAS  Google Scholar 

  • Gruber N, Galloway JN (2008) An earth-system perspective of the global nitrogen cycle. Nature 451:293–296

    CAS  Google Scholar 

  • Guerinot ML, Meidl EJ, Plessner O (1990) Citrate as a siderophore in Bradyrhizobium japonicum. J Bacteriol 172:3298–3303

    CAS  Google Scholar 

  • Gyaneshwar P, Paliy O, McAuliffe J, Popham DL, Jordan MI, Kustu S (2005) Sulfur and nitrogen limitation in Escherichia coli K-12: specific homeostatic responses. J Bacteriol 187:1074–1090

    CAS  Google Scholar 

  • Hall HK, Foster JW (1996) The role of fur in the acid tolerance response of Salmonella typhimurium is physiologically and genetically separable from its role in iron acquisition. J Bacteriol 178:5683–5691

    CAS  Google Scholar 

  • Hamza I, Chauhan S, Hassett R, O’Brian MR (1998) The bacterial Irr protein is required for coordination of heme biosynthesis with iron availability. J Biol Chem 273:21669–21674

    CAS  Google Scholar 

  • Hamza I, Hassett R, O’Brian MR (1999) Identification of a functional fur gene in Bradyrhizobium japonicum. J Bacteriol 181:5843–5846

    CAS  Google Scholar 

  • Hamza I, Qi Z, King ND, O’Brian MR (2000) Fur-independent regulation of iron metabolism by Irr in Bradyrhizobium japonicum. Microbiol. 146:669–676

    CAS  Google Scholar 

  • Hantke K (2003) Is the bacterial ferrous iron transporter FeoB a living fossil? Trends Microbiol 11:192–195

    CAS  Google Scholar 

  • Hennecke H (1992) The role of respiration in symbiotic nitrogen fixation. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Herbig AF, Helmann JD (2001) Roles of metal ions and hydrogen peroxide in modulating the interaction of the Bacillus subtilis PerR peroxide regulon repressor with operator DNA. Mol Microbiol 41:849–859

    CAS  Google Scholar 

  • Herrada G, Puppo A, Moreau S, Day DA, Rigaud J (1993) How is leghemoglobin involved in peribacteroid membrane degradation during nodule senescence? FEBS Lett 326:33–38

    CAS  Google Scholar 

  • Hibbing ME, Fuqua C (2011) Antiparallel and interlinked control of cellular iron levels by the Irr and RirA regulators of Agrobacterium tumefaciens. J Bacteriol 193:3461–3472

    CAS  Google Scholar 

  • Hirotsu S, Chu GC, Unno M, Lee DS, Yoshida T, Park SY, Shiro Y, Ikeda-Saito M (2004) The crystal structures of the ferric and ferrous forms of the heme complex of HmuO, a heme oxygenase of Corynebacterium diphtheriae. J Biol Chem 279:11937–11947

    CAS  Google Scholar 

  • Hohle TH, Franck WL, Stacey G, O’Brian MR (2011) Bacterial outer membrane channel for divalent metal ion acquisition. Proc Natl Acad Sci U S A 108:15390–15395

    CAS  Google Scholar 

  • Hohle TH, O’Brian MR (2009) The mntH gene encodes the major Mn2+ transporter in Bradyrhizobium japonicum and is regulated by manganese via the Fur protein. Mol Microbiol 72:399–409

    CAS  Google Scholar 

  • Hohle TH, O’Brian MR (2010) Transcriptional control of the Bradyrhizobium japonicum irr gene requires repression by Fur and antirepression by Irr. J Biol Chem 285:26074–26080

    CAS  Google Scholar 

  • Hohle TH, O’Brian MR (2012) Manganese is required for oxidative metabolism in unstressed Bradyrhizobium japonicum cells. Mol Microbiol 84:766–777

    CAS  Google Scholar 

  • Hu RG, Wang H, Xia Z, Varshavsky A (2008) The N-end rule pathway is a sensor of heme. Proc Natl Acad Sci U S A 105:76–81

    CAS  Google Scholar 

  • Hu X, Boyer GL (1995) Isolation and characterization of the siderophore N-deoxyschizokinen from Bacillus megaterium ATCC 19213. Biometals 8(357):364

    Google Scholar 

  • Ishikawa H, Kato M, Hori H, Ishimori K, Kirisako T, Tokunaga F, Iwai K (2005) Involvement of heme regulatory motif in heme-mediated ubiquitination and degradation of IRP2. Mol Cell 19:171–181

    CAS  Google Scholar 

  • Ishikawa H, Nakagaki M, Bamba A, Uchida T, Hori H, O’Brian MR, Iwai K, Ishimori K (2011) Unusual heme binding in the bacterial iron response regulator protein: spectral characterization of heme binding to the heme regulatory motif. Biochemistry 50:1016–1022

    CAS  Google Scholar 

  • Jeong J, Rouault TA, Levine RL (2004) Identification of a heme-sensing domain in iron regulatory protein 2. J Biol Chem 279:45450–45454

    CAS  Google Scholar 

  • Kaiser BN, Moreau S, Castelli J, Thomson R, Lambert A, Bogliolo S, Puppo A, Day DA (2003) The soybean NRAMP homologue, GmDMT1, is a symbiotic divalent metal transporter capable of ferrous iron transport. Plant J 35:295–304

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Kitphati W, Ngok-Ngam P, Suwanmaneerat S, Sukchawalit R, Mongkolsuk S (2007) Agrobacterium tumefaciens fur has important physiological roles in iron and manganese homeostasis, the oxidative stress response, and full virulence. Appl Environ Microbiol 73:4760–4768

    CAS  Google Scholar 

  • Koster W, Braun V (1990) Iron (III) hydroxamate transport into Escherichia coli. Substrate binding to the periplasmic FhuD protein. J Biol Chem 265:21407–21410

    CAS  Google Scholar 

  • Kunze B, Trowitzsch-Kienast W, Hofle G, Reichenbach H (1992) Nannochelins A, B and C, new iron-chelating compounds from Nannocystis exedens (myxobacteria). Production, isolation, physico-chemical and biological properties. J Antibiot (Tokyo) 45:147–150

    CAS  Google Scholar 

  • Kurokawa H, Lee DS, Watanabe M, Sagami I, Mikami B, Raman CS, Shimizu T (2004) A redox-controlled molecular switch revealed by the crystal structure of a bacterial heme PAS sensor. J Biol Chem 279:20186–20193

    CAS  Google Scholar 

  • Lankford CE (1973) Bacterial assimilation of iron. Crit Rev Microbiol 2:273–331

    CAS  Google Scholar 

  • Lensbouer JJ, Patel A, Sirianni JP, Doyle RP (2008) Functional characterization and metal ion specificity of the metal-citrate complex transporter from Streptomyces coelicolor. J Bacteriol 190:5616–5623

    CAS  Google Scholar 

  • Letoffe S, Delepelaire P, Wandersman C (2006) The housekeeping dipeptide permease is the Escherichia coli heme transporter and functions with two optional peptide binding proteins. Proc Natl Acad Sci U S A 103:12891–12896

    CAS  Google Scholar 

  • Letoffe S, Delepelaire P, Wandersman C (2008) Functional differences between heme permeases: Serratia marcescens HemTUV permease exhibits a narrower substrate specificity (restricted to heme) than the Escherichia coli DppABCDF peptide-heme permease. J Bacteriol 190:1866–1870

    CAS  Google Scholar 

  • LeVier K, Day DA, Guerinot ML (1996) Iron uptake by symbiosomes from soybean root nodules. Plant Physiol 111:893–900

    CAS  Google Scholar 

  • Litwin CM, Calderwood SB (1993) Role of iron in regulation of virulence genes. Clin Microbiol Rev 6:137–149

    CAS  Google Scholar 

  • Lynch D, O’Brien J, Welch T, Clarke P, Cuiv PO, Crosa JH, O’Connell M (2001) Genetic organization of the region encoding regulation, biosynthesis, and transport of rhizobactin 1021, a siderophore produced by Sinorhizobium meliloti. J Bacteriol 183:2576–2585

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Martinez M, Ugalde RA, Almiron M (2005) Dimeric Brucella abortus Irr protein controls its own expression and binds haem. Microbiology 151:3427–3433

    CAS  Google Scholar 

  • Martinez M, Ugalde RA, Almiron M (2006) Irr regulates brucebactin and 2,3-dihydroxybenzoic acid biosynthesis, and is implicated in the oxidative stress resistance and intracellular survival of Brucella abortus. Microbiology 152:2591–2598

    CAS  Google Scholar 

  • Masse E, Gottesman S (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci U S A 99:4620–4625

    CAS  Google Scholar 

  • Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol 17:458–466

    CAS  Google Scholar 

  • Matzanke BF, Anemuller S, Schunemann V, Trautwein AX, Hantke K (2004) FhuF, part of a siderophore-reductase system. Biochemistry 43:1386–1392

    CAS  Google Scholar 

  • McKie AT (2008) The role of Dcytb in iron metabolism: an update. Biochem Soc Trans 36:1239–1241

    CAS  Google Scholar 

  • Mellin JR, Goswami S, Grogan S, Tjaden B, Genco CA (2007) A novel Fur- and iron-regulated small RNA, NrrF, is required for indirect Fur-mediated regulation of the sdhA and sdhC Genes in Neisseria meningitidis. J Bacteriol 189:3686–3694

    CAS  Google Scholar 

  • Mellin JR, McClure R, Lopez D, Green O, Reinhard B, Genco C (2010) Role of Hfq in iron-dependent and -independent gene regulation in Neisseria meningitidis. Microbiology 156:2316–2326

    CAS  Google Scholar 

  • Menscher EA, Caswell CC, Anderson ES, Roop RM (2012) Mur regulates the gene encoding the manganese transporter MntH in Brucella abortus 2308. J Bacteriol 194:561–566

    CAS  Google Scholar 

  • Modi M, Shah KS, Modi VV (1985) Isolation and characterisation of catechol-like siderophore from cowpea Rhizobium RA-1. Arch Microbiol 141:156–158

    CAS  Google Scholar 

  • Mongkolsuk S, Helmann JD (2002) Regulation of inducible peroxide stress responses. Mol Microbiol 45:9–15

    CAS  Google Scholar 

  • Mongkolsuk S, Praituan W, Loprasert S, Fuangthong M, Chamnongpol S (1998) Identification and characterization of a new organic hydroperoxide resistance (ohr) gene with a novel pattern of oxidative stress regulation from Xanthomonas campestris pv. phaseoli. J Bacteriol 180:2636–2643

    CAS  Google Scholar 

  • Moreau S, Day DA, Puppo A (1998) Ferrous iron is transported across the peribacteroid membrane of soybean nodules. Planta 207:83–87

    CAS  Google Scholar 

  • Moreau S, Meyer JM, Puppo A (1995) Uptake of iron by symbiosomes and bacteroids from soybean nodules. FEBS Lett 361:225–228

    CAS  Google Scholar 

  • Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 411:948–950

    CAS  Google Scholar 

  • Nandal A, Huggins CC, Woodhall MR, McHugh J, Rodriguez-Quinones F, Quail MA, Guest JR, Andrews SC (2009) Induction of the ferritin gene (ftnA) of Escherichia coli by Fe2+-Fur is mediated by reversal of H-NS silencing and is RyhB independent. Mol Microbiol 75(3): 637–657

    Google Scholar 

  • Neilands JB (1973) Microbial iron transport compounds (siderochromes). Elsevier, Amsterdam

    Google Scholar 

  • Neilands JB (1981) Microbial iron compounds. Annu Rev Biochem 50:715–731

    CAS  Google Scholar 

  • Neilands JB, Leong SA (1986) Siderophores in relation to plant growth and disease. Annu Rev Plant Physiol 37:187–208

    CAS  Google Scholar 

  • Ngok-Ngam P, Ruangkiattikul N, Mahavihakanont A, Virgem SS, Sukchawalit R, Mongkolsuk S (2009) Roles of Agrobacterium tumefaciens RirA in iron regulation, oxidative stress response, and virulence. J Bacteriol 191:2083–2090

    CAS  Google Scholar 

  • Nienaber A, Hennecke H, Fischer HM (2001) Discovery of a haem uptake system in the soil bacterium Bradyrhizobium japonicum. Mol Microbiol 41:787–800

    CAS  Google Scholar 

  • Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67:593–656

    CAS  Google Scholar 

  • Noya F, Arias A, Fabiano E (1997) Heme compounds as iron sources for nonpathogenic rhizobium bacteria. J Bacteriol 179:3076–3078

    CAS  Google Scholar 

  • O’Brian MR, Thony-Meyer L (2002) Biochemistry, regulation and genomics of haem biosynthesis in prokaryotes. Adv Microb Physiol 46:257–318

    Google Scholar 

  • O’Hara GW, Dilworth MJ, Boonkerd JN, Parkpian P (1988) Iron-deficiency specifically limits nodule development in peanut inoculated with Bradyrhizobium sp. New Phytol 108:51–57

    Google Scholar 

  • Ojeda JF, Martinson D, Menscher E, Roop RM 2nd (2012) The bhuQ gene encodes a heme oxygenase that contributes to the ability of Brucella abortus 2308 to use heme as an iron source and is regulated by Irr. J Bacteriol (in press)

    Google Scholar 

  • Oke V, Long SR (1999) Bacteroid formation in the Rhizobium-legume symbiosis. Curr Opin Microbiol 2:641–646

    CAS  Google Scholar 

  • Okujo N, Sakakibara Y, Yoshida T, Yamamoto S (1994) Structure of acinetoferrin, a new citrate-based dihydroxamate siderophore from Acinetobacter haemolyticus. Biometals 7:170–176

    CAS  Google Scholar 

  • Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546

    CAS  Google Scholar 

  • Outten FW, Djaman O, Storz G (2004) A suf operon requirement for Fe-S cluster assembly during iron starvation in Escherichia coli. Mol Microbiol 52:861–872

    CAS  Google Scholar 

  • Panek HR, O’Brian MR (2004) KatG is the primary detoxifier of hydrogen peroxide produced by aerobic metabolism in Bradyrhizobium japonicum. J Bacteriol 186:7874–7880

    CAS  Google Scholar 

  • Parrow NL, Abbott J, Lockwood AR, Battisti JM, Minnick MF (2009) Function, regulation, and transcriptional organization of the hemin utilization locus of Bartonella quintana. Infect Immun 77:307–316

    CAS  Google Scholar 

  • Patel HN, Chakraborty RN, Desai SB (1988) Isolation and partial characterization of phenolate siderophore from Rhizobium leguminosarum IARI 102. FEMS Microbiol Lett 56:131–134

    CAS  Google Scholar 

  • Patzer SI, Hantke K (1998) The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol Microbiol 28:1199–1210

    CAS  Google Scholar 

  • Persmark M, Pittman P, Buyer JS, Schwyn B, Gill PR Jr, Neilands JB (1993) Isolation and structure of rhizobactin 1021, a siderophore from the alfalfa symbiont Rhizobium meliloti 1021. J Am Chem Soc 115:3950–3956

    CAS  Google Scholar 

  • Platero R, de Lorenzo V, Garat B, Fabiano E (2007) Sinorhizobium meliloti fur-like (Mur) protein binds a fur box-like sequence present in the mntA promoter in a manganese-responsive manner. Appl Environ Microbiol 73:4832–4838

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Plessner O, Klapatch T, Guerinot ML (1993) Siderophore utilization by Bradyrhizobium japonicum. Appl Environ Microbiol 59:1688–1690

    CAS  Google Scholar 

  • Pohl E, Holmes RK, Hol WG (1999a) Crystal structure of a cobalt-activated diphtheria toxin repressor-DNA complex reveals a metal-binding SH3-like domain. J Mol Biol 292:653–667

    CAS  Google Scholar 

  • Pohl E, Holmes RK, Hol WG (1999b) Crystal structure of the iron-dependent regulator (IdeR) from Mycobacterium tuberculosis shows both metal binding sites fully occupied. J Mol Biol 285:1145–1156

    CAS  Google Scholar 

  • Poole K (2004) Iron transport systems in pathogenic bacteria: pseudomonas. ASM Press, Washington

    Google Scholar 

  • Postle K, Kadner RJ (2003) Touch and go: tying TonB to transport. Mol Microbiol 49:869–882

    CAS  Google Scholar 

  • Postle K, Larsen R (2007) TonB-dependent energy transduction between outer and cytoplasmic membranes. Biometals 20:453–465

    CAS  Google Scholar 

  • Prieto-Alamo MJ, Jurado J, Gallardo-Madueno R, Monje-Casas F, Holmgren A, Pueyo C (2000) Transcriptional regulation of glutaredoxin and thioredoxin pathways and related enzymes in response to oxidative stress. J Biol Chem 275:13398–13405

    CAS  Google Scholar 

  • Puri S, Hohle TH, O’Brian MR (2010) Control of bacterial iron homeostasis by manganese. Proc Natl Acad Sci U S A 107:10691–10695

    CAS  Google Scholar 

  • Puri S, O’Brian MR (2006) The hmuQ and hmuD genes from Bradyrhizobium japonicum encode heme-degrading enzymes. J Bacteriol 188:6476–6482

    CAS  Google Scholar 

  • Qi Z, Hamza I, O’Brian MR (1999) Heme is an effector molecule for iron-dependent degradation of the bacterial iron response regulator (Irr) protein. Proc Natl Acad Sci U S A 96:13056–13061

    CAS  Google Scholar 

  • Qi Z, O’Brian MR (2002) Interaction between the bacterial iron response regulator and ferrochelatase mediates genetic control of heme biosynthesis. Mol Cell 9:155–162

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Ratledge C, Dover LG (2000) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54:881–941

    CAS  Google Scholar 

  • Ratliff M, Zhu W, Deshmukh R, Wilks A, Stojiljkovic I (2001) Homologues of neisserial heme oxygenase in gram-negative bacteria: degradation of heme by the product of the pigA gene of Pseudomonas aeruginosa. J Bacteriol 183:6394–6403

    CAS  Google Scholar 

  • Raymond KN, Dertz EA (2004) Biochemical and physical properties of siderophores. ASM Press, Washington

    Google Scholar 

  • Rees DC, Howard JB (2000) Nitrogenase: standing at the crossroads. Curr Opin Chem Biol 4:559–566

    CAS  Google Scholar 

  • Reigh G, O’Connell M (1993) Siderophore-mediated iron transport correlates with the presence of specific iron-regulated proteins in the outer membrane of Rhizobium meliloti. J Bacteriol 175:94–102

    CAS  Google Scholar 

  • Reniere ML, Ukpabi GN, Harry SR, Stec DF, Krull R, Wright DW, Bachmann BO, Murphy ME, Skaar EP (2010) The IsdG-family of haem oxygenases degrades haem to a novel chromophore. Mol Microbiol 75:1529−1538

    CAS  Google Scholar 

  • Rioux CR, Jordan DC, Rattray JB (1986) Iron requirement of Rhizobium leguminosarum and secretion of anthranilic acid during growth on an iron-deficient medium. Arch Biochem Biophys 248:175–182

    CAS  Google Scholar 

  • Ritz D, Patel H, Doan B, Zheng M, Aslund F, Storz G, Beckwith J (2000) Thioredoxin 2 is involved in the oxidative stress response in Escherichia coli. J Biol Chem 275:2505–2512

    CAS  Google Scholar 

  • Roberts GP, Youn H, Kerby RL (2004) CO-sensing mechanisms. Microbiol Mol Biol Rev 68:453–473

    CAS  Google Scholar 

  • Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697

    CAS  Google Scholar 

  • Rodionov DA, Gelfand MS, Todd JD, Curson AR, Johnston AW (2006) Computational reconstruction of iron- and manganese-responsive transcriptional networks in alpha-Proteobacteria. PLoS Comput Biol 2:e163

    Google Scholar 

  • Ruangkiattikul N, Bhubhanil S, Chamsing J, Niamyim P, Sukchawalit R, Mongkolsuk S (2012) Agrobacterium tumefaciens membrane-bound ferritin plays a role in protection against hydrogen peroxide toxicity and is negatively regulated by the iron response regulator. FEMS Microbiol Lett 329:87–92

    CAS  Google Scholar 

  • Rudolph G, Hennecke H, Fischer HM (2006a) Beyond the Fur paradigm: iron-controlled gene expression in rhizobia. FEMS Microbiol Rev 30:631–648

    CAS  Google Scholar 

  • Rudolph G, Semini G, Hauser F, Lindemann A, Friberg M, Hennecke H, Fischer HM (2006b) The Iron control element, acting in positive and negative control of iron-regulated Bradyrhizobium japonicum genes, is a target for the Irr protein. J Bacteriol 188:733–744

    CAS  Google Scholar 

  • Salahudeen AA, Thompson JW, Ruiz JC, Ma HW, Kinch LN, Li Q, Grishin NV, Bruick RK (2009) An E3 ligase possessing an iron-responsive hemerythrin domain is a regulator of iron homeostasis. Science 326:722–726

    CAS  Google Scholar 

  • Sangwan I, O’Brian MR (1992) Characterization of δ-aminolevulinic acid formation in soybean root nodules. Plant Physiol 98:1074–1079

    CAS  Google Scholar 

  • Sangwan I, Small SK, O’Brian MR (2008) The Bradyrhizobium japonicum Irr protein is a transcriptional repressor with high-affinity DNA-binding activity. J Bacteriol 190:5172–5177

    CAS  Google Scholar 

  • Santos R, Bocquet S, Puppo A, Touati D (1999) Characterization of an atypical superoxide dismutase from Sinorhizobium meliloti. J Bacteriol 181:4509–4516

    CAS  Google Scholar 

  • Schauer K, Rodionov DA, de Reuse H (2008) New substrates for TonB-dependent transport: do we only see the ‘tip of the iceberg’? Trends Biochem Sci 33:330–338

    CAS  Google Scholar 

  • Schmitt MP (1997) Utilization of host iron sources by Corynebacterium diphtheriae: identification of a gene whose product is homologous to eukaryotic heme oxygenases and is required for acquisition of iron from heme and hemoglobin. J Bacteriol 179:838–845

    CAS  Google Scholar 

  • Schuller DJ, Wilks A, Ortiz de Montellano PR, Poulos TL (1999) Crystal structure of human heme oxygenase-1. Nat Struct Biol 6:860–867

    CAS  Google Scholar 

  • Schuller DJ, Zhu W, Stojiljkovic I, Wilks A, Poulos TL (2001) Crystal structure of heme oxygenase from the gram-negative pathogen Neisseria meningitidis and a comparison with mammalian heme oxygenase-1. Biochemistry 40:11552–11558

    CAS  Google Scholar 

  • Schwartz CJ, Giel JL, Patschkowski T, Luther C, Ruzicka FJ, Beinert H, Kiley PJ (2001) IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins. Proc Natl Acad Sci U S A 98:14895–14900

    CAS  Google Scholar 

  • Sedlacek V, van Spanning RJ, Kucera I (2009) Ferric reductase A is essential for effective iron acquisition in Paracoccus denitrificans. Microbiology 155:1294–1301

    CAS  Google Scholar 

  • Silhavy TJ, Kahne D, Walker S (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2:a000414

    Google Scholar 

  • Singleton C, White GF, Todd JD, Marritt SJ, Cheesman MR, Johnston AW, Le Brun NE (2010) Heme-responsive DNA binding by the global iron regulator Irr from Rhizobium leguminosarum. J Biol Chem 285:16023–16031

    CAS  Google Scholar 

  • Skaar EP, Gaspar AH, Schneewind O (2004) IsdG and IsdI, heme-degrading enzymes in the cytoplasm of Staphylococcus aureus. J Biol Chem 279:436–443

    CAS  Google Scholar 

  • Skaar EP, Gaspar AH, Schneewind O (2006) Bacillus anthracis IsdG, a heme-degrading monooxygenase. J Bacteriol 188:1071–1080

    CAS  Google Scholar 

  • Skorupska A, Deryło M, Lorkiewicz Z (1989) Siderophore production and utilization by Rhizobium trifolii. Biometals 2:45–49

    CAS  Google Scholar 

  • Small SK, O’Brian MR (2011) The Bradyrhizobium japonicum frcB gene encodes a diheme ferric reductase. J Bacteriol 193:4088–4094

    CAS  Google Scholar 

  • Small SK, Puri S, O’Brian MR (2009a) Heme-dependent metalloregulation by the iron response regulator (Irr) protein in Rhizobium and other Alpha-proteobacteria. Biometals 22:89–97

    CAS  Google Scholar 

  • Small SK, Puri S, Sangwan I, O’Brian MR (2009b) Positive control of ferric siderophore receptor gene expression by the Irr protein in Bradyrhizobium japonicum. J Bacteriol 191:1361–1368

    CAS  Google Scholar 

  • Smith MJ, Neilands JB (1984) Rhizobactin, a siderophore from Rhizobium meliloti. J Plant Nutr 7:449–458

    CAS  Google Scholar 

  • Smith MJ, Shoolery JN, Schwyn B, Holden I, Neilands JB (1985) Rhizobactin, a structurally novel siderophore from Rhizobium meliloti. J Am Chem Soc 107:1739–1743

    CAS  Google Scholar 

  • Sobota JM, Imlay JA (2011) Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese. Proc Natl Acad Sci U S A 108:5402–5407

    CAS  Google Scholar 

  • Spaink HP (2000) Root nodulation and infection factors produced by rhizobial bacteria. Annu Rev Microbiol 54:257–288

    CAS  Google Scholar 

  • Stevens JB, Carter RA, Hussain H, Carson KC, Dilworth MJ, Johnston AW (1999) The fhu genes of Rhizobium leguminosarum, specifying siderophore uptake proteins: fhuDCB are adjacent to a pseudogene version of fhuA. Microbiology 145(Pt 3):593–601

    CAS  Google Scholar 

  • Stojiljkovic I, Baumler AJ, Hantke K (1994) Fur regulon in gram-negative bacteria. Identification and characterization of new iron-regulated Escherichia coli genes by a fur titration assay (published erratum appears in J Mol Biol 1994 Jul 15; 240(3):271). J Mol Biol 236:531–545

    CAS  Google Scholar 

  • Stojiljkovic I, Hantke K (1992) Hemin uptake system of Yersinia enterocolitica: similarities with other TonB-dependent systems in gram-negative bacteria. EMBO J 11:4359–4367

    CAS  Google Scholar 

  • Tang C, Robson AD, Dilworth MJ (1990) The role of iron in nodulation and nitrogen fixation in Lupinus angustifolius L. New Phytol 114:173–182

    CAS  Google Scholar 

  • Tao K, Makino K, Yonei S, Nakata A, Shinagawa H (1989) Molecular cloning and nucleotide sequencing of oxyR, the positive regulatory gene of a regulon for an adaptive response to oxidative stress in Escherichia coli: homologies between OxyR protein and a family of bacterial activator proteins. Mol Gen Genet 218:371–376

    CAS  Google Scholar 

  • Taulé C, Zabaleta M, Mareque C, Platero R, Sanjurjo L, Sicardi M, Frioni L, Battistoni F, Fabiano E (2012) New Betaproteobacterial Rhizobium strains able To efficiently nodulate Parapiptadenia rigida (Benth.) Brenan. Appl Environ Microbiol 78:1692–1700

    Google Scholar 

  • Tartaglia LA, Storz G, Ames BN (1989) Identification and molecular analysis of oxyR-regulated promoters important for the bacterial adaptation to oxidative stress. J Mol Biol 210:709–719

    CAS  Google Scholar 

  • Todd JD, Sawers G, Johnston AW (2005) Proteomic analysis reveals the wide-ranging effects of the novel, iron-responsive regulator RirA in Rhizobium leguminosarum bv. viciae. Mol Genet Genomics 273:197–206

    CAS  Google Scholar 

  • Todd JD, Sawers G, Rodionov DA, Johnston AW (2006) The Rhizobium leguminosarum regulator IrrA affects the transcription of a wide range of genes in response to Fe availability. Mol Genet Genomics 275:564–577

    CAS  Google Scholar 

  • Todd JD, Wexler M, Sawers G, Yeoman KH, Poole PS, Johnston AW (2002) RirA, an iron-responsive regulator in the symbiotic bacterium Rhizobium leguminosarum. Microbiology 148:4059–4071

    CAS  Google Scholar 

  • Tottey S, Rich PR, Rondet SAM, Robinson NJ (2001) Two menkes-type ATPases supply copper for photosynthesis in Synechocystis PCC 6803. J Biol Chem 276:19999–20004

    CAS  Google Scholar 

  • Turner SL, Young JP (2000) The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications. Mol Biol Evol 17:309–319

    CAS  Google Scholar 

  • Vashisht AA, Zumbrennen KB, Huang X, Powers DN, Durazo A, Sun D, Bhaskaran N, Persson A, Uhlen M, Sangfelt O, Spruck C, Leibold EA, Wohlschlegel JA (2009) Control of iron homeostasis by an iron-regulated ubiquitin ligase. Science 326:718–721

    CAS  Google Scholar 

  • Verma DPS, Nadler KD (1984) The Rhizobium-legume symbiosis: the host’s point of view. Springer-Verlag, New York

    Google Scholar 

  • Viguier C, Cuiv PO, Clarke P, O’Connell M (2005) RirA is the iron response regulator of the rhizobactin 1021 biosynthesis and transport genes in Sinorhizobium meliloti 2011. FEMS Microbiol Lett 246:235–242

    CAS  Google Scholar 

  • Wandersman C, Delepelaire P (2004) Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611–647

    CAS  Google Scholar 

  • Wandersman C, Stojiljkovic I (2000) Bacterial heme sources: the role of heme, hemoprotein receptors and hemophores. Curr Opin Microbiol 3:215–220

    CAS  Google Scholar 

  • Wang S, Wu Y, Outten FW (2011) Fur and the novel regulator YqjI control transcription of the ferric reductase gene yqjH in Escherichia coli. J Bacteriol 193:563–574

    CAS  Google Scholar 

  • Wexler M, Todd JD, Kolade O, Bellini D, Hemmings AM, Sawers G, Johnston AW (2003) Fur is not the global regulator of iron uptake genes in Rhizobium leguminosarum. Microbiology 149:1357–1365

    CAS  Google Scholar 

  • Wexler M, Yeoman KH, Stevens JB, de Luca NG, Sawers G, Johnston AW (2001) The Rhizobium leguminosarum tonB gene is required for the uptake of siderophore and haem as sources of iron. Mol Microbiol 41:801–816

    CAS  Google Scholar 

  • Wilderman PJ, Sowa NA, FitzGerald DJ, FitzGerald PC, Gottesman S, Ochsner UA, Vasil ML (2004) Identification of tandem duplicate regulatory small RNAs in Pseudomonas aeruginosa involved in iron homeostasis. Proc Natl Acad Sci U S A 101:9792–9797

    CAS  Google Scholar 

  • Wilhelm SW, Trick CG (1994) Iron-limited growth of cyanobacteria: multiple siderophore production is a common response. Limnol Oceanogr 39:1979–1984

    CAS  Google Scholar 

  • Wilks A, Schmitt MP (1998) Expression and characterization of a heme oxygenase (Hmu O) from Corynebacterium diphtheriae. Iron acquisition requires oxidative cleavage of the heme macrocycle. J Biol Chem 273:837–841

    CAS  Google Scholar 

  • Williams PH (1979) Novel iron uptake system specified by ColV plasmids: an important component in the virulence of invasive strains of Escherichia coli. Infect Immun 26:925–932

    CAS  Google Scholar 

  • Winkelmann G (2007) Ecology of siderophores with special reference to the fungi. Biometals 20:379–392

    CAS  Google Scholar 

  • Wu R, Skaar EP, Zhang R, Joachimiak G, Gornicki P, Schneewind O, Joachimiak A (2005) Staphylococcus aureus IsdG and IsdI, heme-degrading enzymes with structural similarity to monooxygenases. J Biol Chem 280:2840–2846

    CAS  Google Scholar 

  • Yamanaka K, Ishikawa H, Megumi Y, Tokunaga F, Kanie M, Rouault TA, Morishima I, Minato N, Ishimori K, Iwai K (2003) Identification of the ubiquitin-protein ligase that recognizes oxidized IRP2. Nat Cell Biol 5:336–340

    CAS  Google Scholar 

  • Yang J, Ishimori K, O’Brian MR (2005) Two heme binding sites are involved in the regulated degradation of the bacterial iron response regulator (Irr) protein. J Biol Chem 280:7671–7676

    CAS  Google Scholar 

  • Yang J, Kim KD, Lucas A, Drahos KE, Santos CS, Mury SP, Capelluto DG, Finkielstein CV (2008) A novel heme-regulatory motif mediates heme-dependent degradation of the circadian factor period 2. Mol Cell Biol 28:4697–4711

    CAS  Google Scholar 

  • Yang J, Panek HR, O’Brian MR (2006a) Oxidative stress promotes degradation of the Irr protein to regulate haem biosynthesis in Bradyrhizobium japonicum. Mol Microbiol 60:209–218

    CAS  Google Scholar 

  • Yang J, Sangwan I, Lindemann A, Hauser F, Hennecke H, Fischer HM, O’Brian MR (2006b) Bradyrhizobium japonicum senses iron through the status of haem to regulate iron homeostasis and metabolism. Mol Microbiol 60:427–437

    Google Scholar 

  • Yang J, Sangwan I, O’Brian MR (2006c) The Bradyrhizobium japonicum Fur protein is an iron-responsive regulator in vivo. Mol Genet Genomics 276:555–564

    CAS  Google Scholar 

  • Yeo WS, Lee JH, Lee KC, Roe JH (2006) IscR acts as an activator in response to oxidative stress for the suf operon encoding Fe-S assembly proteins. Mol Microbiol 61:206–218

    CAS  Google Scholar 

  • Yeoman KH, Curson AR, Todd JD, Sawers G, Johnston AW (2004) Evidence that the Rhizobium regulatory protein RirA binds to cis-acting iron-responsive operators (IROs) at promoters of some Fe-regulated genes. Microbiology 150:4065–4074

    CAS  Google Scholar 

  • Yeoman KH, Wisniewski-Dye F, Timony C, Stevens JB, deLuca NG, Downie JA, Johnston AW (2000) Analysis of the Rhizobium leguminosarum siderophore-uptake gene fhuA: differential expression in free-living bacteria and nitrogen-fixing bacteroids and distribution of an fhuA pseudogene in different strains. Microbiology 146(Pt 4):829–837

    CAS  Google Scholar 

  • Yu C, Genco CA (2012) Fur-mediated activation of gene transcription in the human pathogen Neisseria gonorrhoeae. J Bacteriol 194:1730–1742

    CAS  Google Scholar 

  • Zenke-Kawasaki Y, Dohi Y, Katoh Y, Ikura T, Ikura M, Asahara T, Tokunaga F, Iwai K, Igarashi K (2007) Heme induces ubiquitination and degradation of the transcription factor Bach1. Mol Cell Biol 27:6962–6971

    CAS  Google Scholar 

  • Zheng M, Aslund F, Storz G (1998) Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279:1718–1721

    CAS  Google Scholar 

  • Zheng M, Doan B, Schneider TD, Storz G (1999) OxyR and SoxRS regulation of fur. J Bacteriol 181:4639–4643

    CAS  Google Scholar 

  • Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA, Storz G (2001) DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183:4562–4570

    CAS  Google Scholar 

  • Zhu W, Hunt DJ, Richardson AR, Stojiljkovic I (2000a) Use of heme compounds as iron sources by pathogenic neisseriae requires the product of the hemO gene. J Bacteriol 182:439–447

    CAS  Google Scholar 

  • Zhu W, Wilks A, Stojiljkovic I (2000b) Degradation of heme in gram-negative bacteria: the product of the hemO gene of Neisseriae is a heme oxygenase. J Bacteriol 182:6783–6790

    CAS  Google Scholar 

Download references

Acknowledgments

Research from the authors’ laboratories was supported by a grant from PEDECIBA-Uruguay to E.F., NIH grants GM067966 and GM099667 to M.R.O’B.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Elena Fabiano or Mark R. O’Brian .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 The Author(s)

About this chapter

Cite this chapter

Fabiano, E., O’Brian, M.R. (2012). Mechanisms and Regulation of Iron Homeostasis in the Rhizobia. In: Expert, D., O'Brian, M. (eds) Molecular Aspects of Iron Metabolism in Pathogenic and Symbiotic Plant-Microbe Associations. SpringerBriefs in Molecular Science(). Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5267-2_3

Download citation

Publish with us

Policies and ethics