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Iron

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Metals and the Biology and Virulence of Brucella

Abstract

Fe is an essential micronutrient for Brucella strains. Meeting their physiologic need for this metal is especially challenging for these bacteria because they live in close association with their mammalian hosts, and Fe-sequestration is a well-documented host defense against microbial pathogens. The following chapter will describe what is presently known about Fe homeostasis in Brucella strains, and how the individual cellular components involved in this process contribute to virulence.

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References

  • Almirón M, Link AJ, Furlong D, Kolter R (1992) A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Gens Dev 6:2646–2654

    Article  Google Scholar 

  • Almirón M, Martínez M, Sanjuan N, Ugalde RA (2001) Ferrochelatase is present in Brucella abortus and is critical for its intracellular survival and virulence. Infect Immun 69:6225–6230

    Article  Google Scholar 

  • Almirón MA, Ugalde RA (2010) Iron homeostasis in Brucella abortus: the role of bacterioferritin. J Microbiol 48:668–673

    Article  CAS  Google Scholar 

  • Anderson GJ, Vulpe CD (2009) Mammalian iron transport. Cell Mol Life Sci 66:3241–3261

    Article  CAS  Google Scholar 

  • Anderson JD, Smith H (1965) The metabolism of erythritol by Brucella abortus. J Gen Microbiol 38:109–124

    Article  CAS  Google Scholar 

  • Anderson ES, Paulley JT, Roop RM II (2008) The AraC-like transcriptional regulator DhbR is required for maximum expression of the 2,3-dihydroxybenzoic acid biosynthesis genes in Brucella abortus 2308 in response to iron deprivation. J Bacteriol 190:1838–1842

    Article  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

    Article  CAS  Google Scholar 

  • Andrews SC (2010) The ferritin-like superfamily: evolution of the biological storeman from a rubrerythrin-like ancestor. Biochim Biophys Acta 1800:691–705

    Article  CAS  Google Scholar 

  • Angerer A, Klupp B, Braun V (1992) Iron transport systems of Serratia marcescens. J Bacteriol 174:1378–1387

    Article  CAS  Google Scholar 

  • Archibald F (1983) Lactobacillus plantarum, an organism not requiring iron. FEMS Microbiol Lett 19:29–32

    Article  CAS  Google Scholar 

  • Atkinson XJ (2015) Determining the chemical structure of brucebactin, the sole complex siderophore utilized by the pathogenic bacterium Brucella abortus. Masters thesis. East Carolina University

    Google Scholar 

  • Baldwin CL, Goenka R (2006) Host immune responses to the intracellular bacterium Brucella: does the bacterium instruct the host to facilitate chronic infection? Crit Rev Immunol 26:407–442

    Article  CAS  Google Scholar 

  • Baldwin CL, Winter AJ (1994) Macrophages and Brucella. In: Zwilling BS, Eisenstein TK (eds) Macrophage-pathogen interactions. Marcel Dekker, New York, NY, pp 363–380

    Google Scholar 

  • Bellaire BH, Elzer PH, Baldwin CL, Roop RM II (1999) The siderophore 2,3-dihydoxybenzoic acid is not required for virulence of Brucella abortus in BALB/c mice. Infect Immun 67:2615–2618

    CAS  Google Scholar 

  • Bellaire BH (2001) Production of the siderophore 2,3-dihydroxybenzoic acid by Brucella abortus is regulated independent of Fur and is required for virulence in cattle. Doctoral dissertation. Louisiana State University Health Sciences Center-Shreveport

    Google Scholar 

  • Bellaire BH, Baldwin CL, Elzer PH, Roop RM II (2000) The siderophore 2,3-dihydroxybenzoic acid contributes to the virulence of Brucella abortus in ruminants. Abstr 100th Gen Meet Amer Soc Microbiol, Abstr B-17, p 44

    Google Scholar 

  • Bellaire BH, Elzer PH, Hagius S, Walker J, Baldwin CL, Roop RM II (2003a) Genetic organization and iron-responsive regulation of the Brucella abortus 2,3-dihydroxybenzoic acid biosynthesis operon, a cluster of genes required for wild-type virulence in pregnant cattle. Infect Immun 71:1794–1803

    Article  CAS  Google Scholar 

  • Bellaire BH, Elzer PH, Baldwin CL, Roop RM II (2003b) Production of the siderophore 2,3-dihydroxybenzoic acid is required for wild-type growth of Brucella abortus in the presence of erythritol under low-iron conditions in vitro. Infect Immun 71:2927–2932

    Article  CAS  Google Scholar 

  • Bhubhanil S, Chamsing J, Sittipo P, Chaoprasid P, Sukchawalit R, Mongkolsuk S (2014) Roles of Agrobacterium tumefaciens membrane-bound ferritin (MbfA) in iron transport and resistance to iron under acidic conditions. Microbiology 160:863–871

    Article  CAS  Google Scholar 

  • Boschiroli ML, Ouahrani-Bettache S, Foulongne V, Michaux-Charachon S, Bourg G, Allardet-Servent A, Cazevieille C, Liautard JP, Ramuz M, O’Callaghan D (2002) The Brucella suis virB operon is induced intracellularly in macrophages. Proc Natl Acad Sci USA 99:1544–1549

    Article  CAS  Google Scholar 

  • Brickman TJ, Armstrong SK (2009) Temporal signaling and differential expression of Bordetella iron transport systems: the role of ferrimones and positive regulators. Biometals 22:33–41

    Article  CAS  Google Scholar 

  • Brickman TJ, Armstrong SK (2012) Iron and pH-responsive FtrABCD ferrous iron utilization system of Bordetella species. Mol Microbiol 86:580–593

    Article  CAS  Google Scholar 

  • Brickman TJ, McIntosh MA (1992) Overexpression and purification of ferric enterobactin esterase from Escherichia coli. Demonstration of enzymatic hydrolysis of enterobactin and its iron complex. J Biol Chem 267:12350–12355

    CAS  Google Scholar 

  • Brickman TJ, Kang HY, Armstrong SK (2001) Transcriptional activation of Bordetella alcaligin siderophore genes requires the AlcR regulator with alcaligin as inducer. J Bacteriol 183:483–489

    Article  CAS  Google Scholar 

  • Byrd TF, Horwitz MA (1989) Interferon gamma-activated human monocytes downregulate transferrin receptors and inhibit the intracellular multiplication of Legionella pneumophila by limiting the availability of iron. J Exp Med 83:1457–1465

    CAS  Google Scholar 

  • Cairo G, Recalcati S, Mantovani A, Locati M (2011) Iron trafficking and metabolism in macrophages: contribution of the polarized phenotype. Trends Immunol 32:241–247

    Article  CAS  Google Scholar 

  • Celli J (2015) The changing nature of the Brucella-containing vacuole. Cell Microbiol 17:951–958

    Article  CAS  Google Scholar 

  • Cellier MF, Courville P, Campion C (2007) Nramp1 phagocyte intracellular metal withdrawal defense. Microbes Infect 9:1662–1670

    Article  CAS  Google Scholar 

  • Chan ACK, Doukov TI, Scofield M, Tom-Yew SAL, Ramin AB, MacKichan JK, Gaynor EC, Murphy MEP (2010) Structure and function of P19, a high-affinity iron transporter of the human pathogen Campylobacter jejuni. J Mol Biol 401:590–604

    Article  CAS  Google Scholar 

  • Chiancone E, Ceci P (2010) The multifaceted capacity of Dps proteins to combat bacterial stress conditions: detoxification of iron and hydrogen peroxide and DNA binding. Biochim Biophys Acta 1800:798–805

    Article  CAS  Google Scholar 

  • Chin N, Frey J, Chang CF, Chang YF (1996) Identification of a locus involved in the utilization of iron by Actinobacillus pleuropneumoniae. FEMS Microbiol Lett 143:1–6

    Article  CAS  Google Scholar 

  • Chipperfield JR, Ratledge C (2000) Salicylic acid is not a bacterial siderophore: a theoretical study. Biometals 13:165–168

    Article  CAS  Google Scholar 

  • Cooper SR, McArdle JV, Raymond KN (1978) Siderophore electrochemistry: relation to intracellular iron release mechanism. Proc Natl Acad Sci USA 75:3551–3554

    Article  CAS  Google Scholar 

  • Corbel MJ, Brinley-Morgan WJ (1984) Genus Brucella. In: Krieg NR, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 1. Williams & Wilkins, Baltimore, MD, pp 377–388

    Google Scholar 

  • Cornish AS, Page WJ (2000) Role of molybdate and other transition metals in the accumulation of protochelin by Azotobacter vinelandii. Appl Environ Microbiol 66:1580–1586

    Article  CAS  Google Scholar 

  • Crichton R (2009) Iron metabolism—from molecular mechanisms to clinical consequences, 3rd edn. Wiley, West Sussex, UK

    Google Scholar 

  • Crumbliss AL, Harrington JM (2009) Iron sequestration by small molecules: thermodynamic and kinetic studies of natural siderophores and synthetic model compounds. Adv Inorg Chem 61:179–251

    Article  CAS  Google Scholar 

  • Danese I, Haine V, Delrue R-M, Tibor A, Lestrate P, Stevaux O, Mertens P, Paquet J-Y, Godfroid J, De Bolle X, Letesson JJ (2004) The Ton system, an ABC transporter, and a universally conserved GTPase are involved in iron utilization by Brucella melitensis 16M. Infect Immun 72:5783–5790

    Article  CAS  Google Scholar 

  • de Barsy M, Jamet A, Filipon D, Nicolas C, Laloux G, Rual JF, Muller A, Twizere JC, Nkengfac B, Vandenhaute J, Hill DE, Salcedo SP, Gorvel JP, Letesson JJ, De Bolle X (2011) Identification of a Brucella spp. secreted effector specifically interacting with human small GTPase Rab2. Cell Microbiol 13:1044–1058

    Article  CAS  Google Scholar 

  • de Jong MF, Sun YH, den Hartigh AB, van Dijl JM, Tsolis RM (2008) Identification of VceA and VceC, two members of the VjbR regulon that are translocated into macrophages by the Brucella type IV secretion system. Mol Microbiol 70:1378–1396

    Article  CAS  Google Scholar 

  • de Silva DM, Askwith CC, Eide D, Kaplan J (1995) The FET3 gene product required for high affinity iron transport in yeast is a cell surface ferroxidase. J Biol Chem 270:1098–1101

    Article  Google Scholar 

  • Delpino MV, Cassataro J, Fossati CA, Goldbaum FA, Baldi PC (2006) Brucella outer membrane protein Omp31 is a haemin-binding protein. Microbes Infect 8:1203–1208

    Article  CAS  Google Scholar 

  • Denoel PA, Crawford RM, Zygmunt MS, Tibor A, Weynants AE, Godfroid F, Hoover DL, Letesson JJ (1997) Survival of a bacterioferritin deletion mutant of Brucella melitensis 16M in human monocyte-derived macrophages. Infect Immun 65:4337–4340

    CAS  Google Scholar 

  • Elhassanny AEM (2016) Characterization of FtrABCD: a ferrous iron-specific transporter that is required for the virulence of Brucella abortus 2308 in mice. Doctoral dissertation. East Carolina University

    Google Scholar 

  • Elhassanny AEM, Anderson ES, Menscher EA, Roop RM II (2013) The ferrous iron transporter FtrABCD is required for the virulence of Brucella abortus 2308 in mice. Mol Microbiol 88:1070–1082

    Article  CAS  Google Scholar 

  • Enright FM (1990) The pathogenesis and pathobiology of Brucella infections in domestic animals. In: Nielsen KH, Duncan JR (eds) Animal brucellosis. CRC Press, Boca Raton, FL, pp 201–320

    Google Scholar 

  • Evans RW, Kong X, Hider RC (2012) Iron mobilization from transferrin by therapeutic iron chelating agents. Biochim Biophys Acta 1820:282–290

    Article  CAS  Google Scholar 

  • Fillat MF (2014) The FUR (ferric uptake regulator) superfamily: diversity and versatility of key transcriptional regulators. Arch Biochem Biophys 546:41–52

    Article  CAS  Google Scholar 

  • Frankenberg-Dinkel N (2004) Bacterial heme oxygenases. Antioxid Redox Signal 6:825–834

    Article  CAS  Google Scholar 

  • Goetz DH, Holmes MA, Borregaard N, Bluhm ME, Raymond KN, Strong RK (2002) The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol Cell 10:1033–1043

    Article  CAS  Google Scholar 

  • Gong S, Bearden SW, Geoffroy VA, Fetherston JD, Perry RD (2001) Characterization of the Yersinia pestis Yfu ABC inorganic iron transport system. Infect Immun 67:2829–2837

    Article  CAS  Google Scholar 

  • González-Carreró MI, Sangari FJ, Agüero J, García-Lobo JM (2002) Brucella abortus 2308 produces brucebactin, a highly efficient catecholic siderophore. Microbiology 148:353–360

    Article  Google Scholar 

  • Grilló MJ, Blasco JM, Gorvel JP, Moriyón I, Moreno E (2012) What have we learned from brucellosis in the mouse model? Vet Res 43:e29

    Article  CAS  Google Scholar 

  • Hancock REW, Hantke K, Braun V (1977) Iron transport in Escherichia coli K-12—2,3-dihydroxybenzoate-promoted iron uptake. Arch Microbiol 114:231–239

    Article  CAS  Google Scholar 

  • Hantke K (1990) Dihydroxybenzoylserine—a siderophore for E. coli. FEMS Microbiol Lett 67:5–8

    CAS  Google Scholar 

  • Harrington JM, Crumbliss AL (2009) The redox hypothesis in siderophore-mediated iron uptake. Biometals 22:679–689

    Article  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

    Article  CAS  Google Scholar 

  • Hider RC, Kong X (2013) Iron speciation in the cytosol: an overview. Dalton Trans 42:3220–3229

    Article  CAS  Google Scholar 

  • Hood MI, Skaar EP (2012) Nutritional immunity: transition metals at the pathogen-host interface. Nature Rev Microbiol 10:525–537

    Article  CAS  Google Scholar 

  • Jain N, Rodriguez AC, Kimsawatde G, Seleem MN, Boyle SM, Sriranganathan N (2011) Effect of entF deletion on iron acquisition and erythritol metabolism by Brucella abortus 2308. FEMS Microbiol Lett 316:1–6

    Article  CAS  Google Scholar 

  • Jenner DC, Dassa E, Whatmore AM, Atkins HS (2009) ABC-binding cassette systems of Brucella. Comp Funct Genom 2009:e354649

    Article  CAS  Google Scholar 

  • Johnston AWB, Todd JD, Curson AR, Lei S, Nikolaidou-Katsaridou N, Gelfand MS, Rodionov DA (2007) Living without Fur: the sublety and complexity of iron-responsive gene regulation in the symbiotic bacterium Rhizobium and other α-proteobacteria. Biometals 20:501–511

    Article  CAS  Google Scholar 

  • Kadner RJ (1990) Vitamin B12 transport in Escherichia coli: energy coupling between membranes. Mol Microbiol 4:2027–2033

    Article  CAS  Google Scholar 

  • Keating TA, Marshall CG, Walsh CT, Keating AE (2002) The structure of VibH represents nonribosomal peptide synthetase condensation, cyclization and epimerization domains. Nat Struct Biol 9:522–526

    CAS  Google Scholar 

  • Kern J, Simon J (2008) Characterization of the NapGH quinol dehydrogenase complex involved in Wolinella succinogens nitrate respiration. Mol Microbiol 69:1137–1152

    Article  CAS  Google Scholar 

  • Kim H-S, Willett JW, Jain-Gupta N, Fiebig A, Crosson S (2014) The Brucella abortus virulence regulator, LovhK, is a sensor kinase in the general stress response signalling pathway. Mol Microbiol 94:913–925

    Article  CAS  Google Scholar 

  • Koch D, Chan ACK, Murphy MEP, Lilie H, Grass G, Nies DH (2011) Characterization of a dipartite iron uptake system from uropathogenic Escherichia coli strain F11. J Biol Chem 286:25317–25330

    Article  CAS  Google Scholar 

  • Korolnek T, Hamza I (2014) Like iron in the blood of the people: the requirement for heme trafficking in iron metabolism. Front Pharmacol 5:e126

    Article  CAS  Google Scholar 

  • Kosman DJ (2003) Molecular mechanisms of iron uptake in fungi. Mol Microbiol 47:1185–1197

    Article  CAS  Google Scholar 

  • Kosman DJ (2010) Redox cycling in iron uptake, efflux and trafficking. J Biol Chem 285:26729–26735

    Article  CAS  Google Scholar 

  • Kosman DJ (2013) Iron metabolism in aerobes: managing ferric iron hydrolysis and ferrous iron autoxidation. Coord Chem Rev 257:210–217

    Article  CAS  Google Scholar 

  • Köster WL, Actis LA, Waldbeser LS, Tolmasky ME, Crosa JH (1991) Molecular characterization of the iron transport system mediated by the pJM1 plasmid in Vibrio anguillarum 775. J Biol Chem 266:23829–23833

    Google Scholar 

  • Kwok EY, Severance S, Kosman DJ (2006) Evidence for iron channeling in the Fet3p-Ftr1p high-affinity iron uptake complex in the yeast plasma membrane. Biochemistry 45:6317–6327

    Article  CAS  Google Scholar 

  • Lengeler JW, Drews G, Schlegel HG (1999) Biology of the prokaryotes. Georg Thieme Verlag, Stuttgart, Germany

    Google Scholar 

  • López-Goñi I, Moriyón I (1995) Production of 2,3-dihydroxybenzoic acid by Brucella species. Curr Microbiol 31:291–293

    Article  Google Scholar 

  • López-Goñi I, Moriyón I, Neilands JB (1992) Identification of 2,3-dihydroxybenzoic acid as a Brucella abortus siderophore. Infect Immun 60:4496–4503

    Google Scholar 

  • Luke RKJ, Gibson F (1971) Location of three genes concerned with the conversion of 2,3-dihydroxybenzoate into enterochelin in Escherichia coli K-12. J Bacteriol 107:557–562

    CAS  Google Scholar 

  • Marchesini MI, Herrmann CK, Salcedo SP, Gorvel JP, Comerci DJ (2011) In search of Brucella abortus type IV secretion substrates: screening and identification of four proteins translocated into host cells through VirB system. Cell Microbiol 13:1261–1274

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Martínez M, Ugalde RA, Almirón 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

    Article  CAS  Google Scholar 

  • Martinson DA (2014) The iron response regulator controls iron homeostasis in Brucella. Doctoral dissertation. East Carolina University

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Massé E, Salvail H, Desnoyers G, Arguin M (2007) Small RNAs controlling iron metabolism. Curr Opin Microbiol 10:140–145

    Article  CAS  Google Scholar 

  • May JJ, Wendrich MT, Marahiel MA (2001) The dhb operon of Bacillus subtilis encodes the biosynthetic template for the catecholic siderophore 2,3-dihydroxybenzoate-glycine-threonine trimeric ester bacillibactin. J Biol Chem 276:7209–7217

    Article  CAS  Google Scholar 

  • Michels K, Nemeth E, Ganz T, Mehrad B (2015) Hepcidin and host defense against infectious diseases. PLoS Pathog 11:e1004998

    Article  CAS  Google Scholar 

  • Minnick MF, Sappington KN, Smitherman LS, Andersson SG, Karlberg O, Carroll JA (2003) Five-member gene family of Bartonella quintana. Infect Immun 71:814–821

    Article  CAS  Google Scholar 

  • Myeni S, Child R, Ng TW, Kupko JJ III, Wehrly TD, Porcella SF, Knodler LA, Celli J (2013) Brucella modulates secretory trafficking via multiple Type IV secretion effector proteins. PLoS Pathog 9:e1003556

    Article  CAS  Google Scholar 

  • Nairz M, Fritsche G, Brunner P, Talasz H, Hantke K, Weiss G (2008) Interferon-γ limits the availability of iron for intramacrophage Salmonella typhimurium. Eur J Immunol 38:1923–1936

    Article  CAS  Google Scholar 

  • Nairz M, Schleicher U, Schroll A, Sonnweber T, Theurl I, Ludwiczek S, Talasz H, Brandacher G, Moser PL, Muckenthaler MU, Fang FC, Bogdan C, Weiss G (2013) Nitric oxide-mediated regulation of ferroportin-1 controls macrophage iron homeostasis and immune function in Salmonella infection. J Exp Med 210:855–873

    Article  CAS  Google Scholar 

  • Nairz M, Haschka D, Demetz E, Weiss G (2014) Iron at the interface of immunity and infection. Front Pharmacol 5:e152

    Article  CAS  Google Scholar 

  • Nakashige TG, Zhang B, Krebs C, Nolan EM (2015) Human calprotectin is an iron-sequestering host-defense protein. Nature Chem Biol 11:765–771

    Article  CAS  Google Scholar 

  • Nikaido H, Rosenberg EY (1990) Cir and Fiu proteins in the outer membrane of Escherichia coli catalyze transport of monomeric catechols: study with & β-lactam antibiotics containing catechol and analogous groups. J Bacteriol 172:1361–1367

    Article  CAS  Google Scholar 

  • Noinaj N, Guillier M, Barnard TJ, Buchanan SK (2010) TonB-dependent transporters: regulation, structure and function. Ann Rev Microbiol 64:43–60

    Article  CAS  Google Scholar 

  • O’Brian MR (2015) Perception and homeostatic control of iron in the rhizobia and related bacteria. Annu Rev Microbiol 69:229–245

    Article  CAS  Google Scholar 

  • Ojeda JF (2012) The bhuTUV and bhuO genes play vital roles in the ability of Brucella abortus to use heme as an iron source and are regulated in an iron-responsive manner by RirA and Irr. Doctoral dissertation. East Carolina University

    Google Scholar 

  • Ojeda JF, Martinson DA, Menscher EA, Roop RM II (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 194:4052–4058

    Article  CAS  Google Scholar 

  • Ollinger J, Song KB, Antelmann H, Hecker M, Helmann JD (2006) Role of the Fur regulon in iron transport in Bacillus subtilis. J Bacteriol 188:3664–3673

    Article  CAS  Google Scholar 

  • Parent MA, Bellaire BH, Murphy EA, Roop RM II, Elzer PH, Baldwin CL (2002) Brucella abortus siderophore 2,3-dihydroxybenzoic acid (DHBA) facilitates intracellular survival of the bacteria. Microb Pathogen 32:239–248

    Article  CAS  Google Scholar 

  • Paulley JT (2007) Production of BhuA by B. abortus is required for hemin utilization and virulence and is dependent on the transcriptional regulators RirA and ChrA. Doctoral dissertation. East Carolina University

    Google Scholar 

  • Paulley JT, Anderson ES, Roop RM II (2007) Brucella abortus requires the heme transporter BhuA for maintenance of chronic infection in BALB/c mice. Infect Immun 75:5248–5254

    Article  CAS  Google Scholar 

  • Peng X, Dong H, Wu Q (2015) A new cis-encoded sRNA, BsrH, regulating the expression of hemH gene in Brucella abortus 2308. FEMS Microbiol Lett 362:1–7

    Article  Google Scholar 

  • Persmark MD, Expert D, Neilands JB (1992) Ferric iron uptake in Erwinia chrysanthemi mediated by chrysobactin and related catechol-type compounds. J Bacteriol 174:4783–4789

    Article  CAS  Google Scholar 

  • Peuser V, Remes B, Klug G (2012) Role of the Irr protein in the regulation of iron metabolism in Rhodobacter sphaeroides. PLoS One 7:e42231

    Article  CAS  Google Scholar 

  • Pittman M (1984). Genus Bordetella. In: Krieg NR, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 1. Williams & Wilkins, Baltimore, MD, pp 388–393

    Google Scholar 

  • Posey JE, Gherardini FC (2000) Lack of a role for iron in the Lyme disease pathogen. Science 288:1651–1653

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Rajasekaran MB, Nilapwar S, Andrews SC, Watson KA (2010) EfeO-cupredoxins: major new members of the cupredoxin superfamily with roles in bacterial iron transport. Biometals 23:1–17

    Article  CAS  Google Scholar 

  • Raymond KN, Dertz EA (2004) Biochemical and physical properties of siderophores. In: Crosa JH, Mey AR, Payne SM (eds) Iron transport in bacteria. ASM Press, Washington, DC, pp 3–17

    Chapter  Google Scholar 

  • Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS (2003) Comparative genomics of the vitamin B12 metabolism and regulation in prokaryotes. J Biol Chem 278:41148–41159

    Article  CAS  Google Scholar 

  • Rodionov DA, Gelfand MS, Todd JD, Curson ARJ, Johnston AWB (2006) Computational reconstruction of iron—and manganese-responsive transcriptional networks in α-proteobacteria. PLOS Comput Biol 2:e163

    Article  CAS  Google Scholar 

  • Roop RM II, Bellaire BH, Valderas MW, Cardelli JA (2004) Adaptation of the brucellae to their intracellular niche. Mol Microbiol 52:621–630

    Article  CAS  Google Scholar 

  • Roop RM II, Gaines JM, Anderson ES, Caswell CC, Martin DW (2009) Survival of the fittest: how Brucella strains adapt to their intracellular niche in the host. Med Microbiol Immunol 198:221–238

    Article  Google Scholar 

  • Roop RM II, Anderson E, Ojeda J, Martinson D, Menscher E, Martin DW (2012) Metal acquisition by Brucella strains. In: López-Goñi I, O’Callaghan D (eds) Brucella—molecular microbiology and genomics. Caister Academic Press, Norfolk, UK, pp 179–199

    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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Salcedo SP, Marchesini MI, Degos C, Terwagne M, von Bargen K, Lepidi H, Herrmann CK, Santos Lacerda TL, Imbert PRC, Pierre P, Alexopoulo L, Letesson JJ, Comerci DJ, Gorvel JP (2013) BtpB, a novel TIR-containing effector protein with immune modulatory functions. Front Cell Infect Microbiol 3:e28

    Article  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

    Article  CAS  Google Scholar 

  • Sankari S, O’Brian MR (2014) A bacterial iron exporter for maintenance of iron homeostasis. J Biol Chem 289:16498–16507

    Article  CAS  Google Scholar 

  • Shi X, Stoj C, Romeo A, Kosman DJ, Zhu Z (2003) Fre1p Cu2+ reduction and Fet3p Cu1+ oxidation modulate copper toxicity in Saccharomyces cerevisiae. J Biol Chem 278:50309–50315

    Article  CAS  Google Scholar 

  • Sia AK, Allred BE, Raymond KN (2013) Siderocalins: siderophore binding proteins evolved for primary pathogen host defense. Curr Opin Chem Biol 17:150–157

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Smith AW, Freeman S, Minnett WG, Lambert PA (1990) Characterisation of a siderophore from Acinetobacter calcoaceticus. FEMS Microbiol Lett 70:29–32

    Article  CAS  Google Scholar 

  • Smith H, Williams AE, Pearce JH, Keppie J, Harris-Smith PW, Fitz-George RB, Witt K (1962) Foetal erythritol: a cause of the localization of Brucella abortus in bovine contagious abortion. Nature 193:47–49

    Article  CAS  Google Scholar 

  • Starr T, Child R, Wehrly TD, Hansen B, Hwang S, López-Otin C, Virgin HW, Celli J (2012) Selective subversion of autophagy complexes facilitates completion of the Brucella intracellular cycle. Cell Host Microbe 11:33–45

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Vizcaíno N, Cloeckaert A (2012) Biology and genetics of the Brucella outer membrane. In: López-Goñi I, O’Callaghan D (eds) Brucella—molecular microbiology and genomics. Caister Academic Press, Norfolk, UK, pp 133–161

    Google Scholar 

  • Vogel HJ (2012) Lactoferrin, a bird’s eye view. Biochem Cell Biol 90:233–244

    Article  CAS  Google Scholar 

  • Walsh CT, Marshall CG (2004) Siderophore biosynthesis in bacteria. In: Crosa JH, Mey AR, Payne SM (eds) Iron transport in bacteria. ASM Press, Washington, DC, pp 18–37

    Chapter  Google Scholar 

  • Waring WS, Elberg SS, Schneider P, Green W (1953) The role of iron in the biology of Brucella suis I. Growth and nutrition. J Bacteriol 66:82–91

    CAS  Google Scholar 

  • Waters LS, Storz G (2009) Regulatory RNAs in bacteria. Cell 136:615–628

    Article  CAS  Google Scholar 

  • Xavier MN, Winter MG, Spees AM, den Hartigh AB, Nguyen K, Roux CM, Silva TMA, Atluri VL, Kerrinnes T, Keestra AM, Monack DM, Luciw PA, Eigenheer RA, Bäumler AJ, Santos RL, Tsolis RM (2013) PPARγ-mediated increase in glucose availability sustains chronic Brucella abortus infection in alternatively activated macrophages. Cell Host Microbe 14:159–170

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Young IG, Langman L, Luke RKJ, Gibson F (1971) Biosynthesis of the iron-transport compound enterochelin: mutants of Escherichia coli unable to synthesize 2,3-dihydroxybenzoate. J Bacteriol 106:51–57

    CAS  Google Scholar 

  • Zhan Y, Cheers C (1993) Endogenous gamma interferon mediates resistance to Brucella abortus infection. Infect Immun 61:4899–4901

    CAS  Google Scholar 

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Acknowledgements

The authors thank present and former members of the Roop and Almirón laboratories for their contributions to the body of work that provided the basis for preparation of this chapter. We also thank Claire Parker Siburt for preparing the siderophore biosynthesis pathways shown in Fig. 2.4. Work on Brucella Fe metabolism in the Roop lab has been supported by grants from the National Institute of Allergy and Infectious Disease (AI-63516) and the United States Department of Agriculture Competitive Research Grants Program (95-01995; 98-02620 and 35204-12218). Work in the Almiron lab has been supported by the Agencia Nacional de Promoción Científica y Tecnológica de la República Argentina (01-6580 and 06-00651) and the Consejo Nacional de Investigaciones Científicas y Tecnológicas de la Argentina-CONICET (PIP 5463).

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Authors and Affiliations

  1. Department of Microbiology and Immunology, Brody School of Medicine, East Carolina University, Greenville, NC, 27834, USA

    R. Martin Roop II & Ahmed E. Elhassanny

  2. Instituto de Investigaciones Biotecnológicas–Instituto Tecnólogico de Chascomús, Universidad Nacional de San Martín–Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina

    Marta A. Almirón

  3. Department of Biology, East Carolina University, Greenville, 27834, USA

    Eric S. Anderson & Xavier J. Atkinson

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  1. R. Martin Roop II
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  2. Ahmed E. Elhassanny
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  5. Xavier J. Atkinson
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Correspondence to R. Martin Roop II .

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  1. Department of Microbiology and Immunology, Brody School of Medicine, East Carolina University, Greenville, North Carolina, USA

    R. Martin Roop II

  2. Department of Biomedical Sciences and Pathobiology, Virginia–Maryland College of Veterinary Medicine, Virginia Tech, Blacksburg, Virginia, USA

    Clayton C. Caswell

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Roop II, R.M., Elhassanny, A.E., Almirón, M.A., Anderson, E.S., Atkinson, X.J. (2017). Iron. In: Roop II, R., Caswell, C. (eds) Metals and the Biology and Virulence of Brucella. Springer, Cham. https://doi.org/10.1007/978-3-319-53622-4_2

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