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Metal acquisition and virulence in Brucella

Published online by Cambridge University Press:  28 May 2012

R. Martin Roop II
R. Martin Roop II*
Affiliation:
Department of Microbiology and Immunology, Brody School of Medicine, East Carolina University, 600 Moye Boulevard, Greenville, North Carolina 27834, USA
*
Corresponding author. E-mail: roopr@ecu.edu
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Abstract

Similar to other bacteria, Brucella strains require several biologically essential metals for their survival in vitro and in vivo. Acquiring sufficient levels of some of these metals, particularly iron, manganese and zinc, is especially challenging in the mammalian host, where sequestration of these micronutrients is a well-documented component of both the innate and acquired immune responses. This review describes the Brucella metal transporters that have been shown to play critical roles in the virulence of these bacteria in experimental and natural hosts.

Keywords

Brucellaironmanganesezincmagnesiumnickelbacterial iron acquisition
Type
Review Article
Information
Animal Health Research Reviews , Volume 13 , Issue 1 , June 2012 , pp. 10 - 20
Copyright
Copyright © Cambridge University Press 2012

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References

Alix, E and Blanc-Potard, JB (2007). MgtC: a key player in intramacrophage survival. Trends in Microbiology 15: 252–256.CrossRefGoogle ScholarPubMed
Almirón, M and Ugalde, RA (2010). Iron homeostasis in Brucella abortus: the role of bacterioferritin. Journal of Microbiology 48: 668–673.CrossRefGoogle ScholarPubMed
Anderson, ES, Paulley, JT, Gaines, JM, Valderas, MW, Martin, DW, Menscher, E, Brown, TD, Burns, CS and Roop, RM II (2009). The manganese transporter MntH is a critical virulence determinant for Brucella abortus 2308 in experimentally infected mice. Infection and Immunity 77: 3466–3474.CrossRefGoogle ScholarPubMed
Anderson, ES, Paulley, JT, Martinson, DA, Gaines, JM, Steele, KH and Roop, RM II (2011). The iron-responsive regulator Irr is required for the wild-type expression of the gene encoding the heme transporter BhuA in Brucella abortus 2308. Journal of Bacteriology 193: 5359–5364.CrossRefGoogle ScholarPubMed
Anderson, ES, Paulley, JT and 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. Journal of Bacteriology 190: 1838–1842.CrossRefGoogle ScholarPubMed
Anderson, GJ and Vulpe, CD (2009). Mammalian iron transport. Cellular and Molecular Life Sciences 66: 3241–3261.CrossRefGoogle ScholarPubMed
Anderson, JD and Smith, H (1965). The metabolism of erythritol by Brucella abortus. Journal of General Microbiology 38: 109–124.CrossRefGoogle Scholar
Anderson, TD, Cheville, NF and Meador, VP (1986). Pathogenesis of placentitis in the goat inoculated with Brucella abortus. II. Ultrastructural studies. Veterinary Pathology 23: 227–239.CrossRefGoogle ScholarPubMed
Andreini, C, Banci, L, Bertini, I and Rosato, A (2006). Zinc through the three domains of life. Journal of Proteome Research 5: 3173–3178.CrossRefGoogle ScholarPubMed
Anjem, A, Varghese, S and Imlay, JA (2009). Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Molecular Microbiology 72: 844–858.CrossRefGoogle ScholarPubMed
Archibald, F (1983). Lactobacillus plantarum, an organism not requiring iron. FEMS Microbiology Letters 19: 29–32.CrossRefGoogle Scholar
Ariza, J, Bosilkovski, M, Cascio, A, Colmenero, JD, Corbel, MJ, Falagas, ME, Memish, ZA, Roushan, MRH, Rubinstein, E, Sipsas, NV, Solera, J, Young, EJ and Pappas, G (2007). Perspectives for the treatment of brucellosis in the 21st century: the Ioannina recommendations. PLoS Medicine 4: e317.CrossRefGoogle ScholarPubMed
Bandara, AB, Contreras, A, Contreras-Rodriguez, A, Martins, AM, Dobrean, V, Poff-Reichow, S, Rajasekaran, P, Sriranganathan, N, Schurig, G and Boyle, SM (2007). Brucella suis urease encoded by ure1 but not ure2 is necessary for intestinal infection of mice. BMC Microbiology 7: 57.CrossRefGoogle ScholarPubMed
Batut, J, Andersson, SGE and O'Callaghan, D (2004). The evolution of chronic infection strategies in the α-proteobacteria. Nature Reviews Microbiology 2: 933–945.CrossRefGoogle ScholarPubMed
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,Louisiana, USAGoogle Scholar
Bellaire, BH, Baldwin, CL, Elzer, PH and Roop, RM II (2000). The siderophore 2,3-dihydroxybenzoic acid contributes to the virulence of Brucella abortus in ruminants. Abstracts of the 100th General Meeting of the American Society for Microbiology, Abstract B-17, page 44.Google Scholar
Bellaire, BH, Elzer, PH, Baldwin, CL and Roop, RM II (1999). The siderophore 2,3-dihydroxybenzoic acid is not required for virulence of Brucella abortus in BALB/c mice. Infection and Immunity 67: 2615–2618.CrossRefGoogle Scholar
Bellaire, BH, Elzer, PH, Baldwin, CL and 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. Infection and Immunity 71: 2927–2932.CrossRefGoogle ScholarPubMed
Bellaire, BH, Elzer, PH, Hagius, S, Walker, J, Baldwin, CL and 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. Infection and Immunity 71: 1794–1803.CrossRefGoogle ScholarPubMed
Blasco, JM (2003). Epididymite contagieuse du belier ou infection à Brucella ovis. In: Lefevre, PC, Blancou, J and Chermette, R (eds) Principales Maladies Infectieuses et Parasitaires du Bétail. Paris: Lavoiser, pp. 905–917.Google Scholar
Bratosin, D, Mazurier, J, Tissier, JP, Estaquier, J, Huart, JJ, Amiesen, JC, Aminoff, D and Montreuil, J (1998). Cellular and molecular mechanisms of senescent erythrocyte phagocytosis by macrophages. Biochimie 80: 173–195.CrossRefGoogle ScholarPubMed
Byrd, TF and Horwitz, MA (1989). Interferon gamma-activated human monocytes down-regulate transferrin receptors and inhibit intracellular multiplication of Legionella pneumophila by limiting the availability of iron. Journal of Clinical Investigation 83: 1457–1465.CrossRefGoogle Scholar
Celli, J, de Chastellier, C, Franchini, DM, Pizarro-Cerdá, J, Moreno, E and Gorvel, JP (2003). Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. Journal of Experimental Medicine 198: 545–556.CrossRefGoogle ScholarPubMed
Celli, J, Salcedo, SP and Gorvel, JP (2005). Brucella coopts the small GTPase Sar1 for intracellular replication. Proceedings of the National Academy of Sciences USA 102: 1673–1678.CrossRefGoogle ScholarPubMed
Cellier, MF, Courville, P and Campion, C (2007). Nramp1 phagocyte intracellular metal withdrawal defense. Microbes and Infection 9: 1662–1670.CrossRefGoogle ScholarPubMed
Corbel, MJ (1997). Brucellosis: an overview. Emerging Infectious Diseases 3: 213–221.CrossRefGoogle ScholarPubMed
Corbin, BD, Seeley, EH, Raab, A, Feldmann, J, Miller, MR, Torres, VJ, Anderson, KL, Dattilo, BM, Dunman, PM, Gerads, R, Caprioli, RM, Nacken, W, Chazin, WJ and Skaar, EP (2008). Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319: 962–965.CrossRefGoogle ScholarPubMed
Clapp, B, Skyberg, JA, Yang, X, Thornburg, T, Walters, N and Pascual, DW (2011). Protective live oral brucellosis vaccines stimulate Th1 and Th17 cell responses. Infection and Immunity 79: 4165–4174.CrossRefGoogle ScholarPubMed
Crichton, RR (2009). Iron Metabolism – from Molecular Mechanisms to Clinical Consequences. 3rd edn. West Sussex, UK: John Wiley & Sons.CrossRefGoogle Scholar
Danese, I (2001). Contribution à l’étude de l'assimilation du fer chez Brucella melitensis 16M. Doctoral dissertation, Facultes Universitaires Notre-Dame de la Paix, Namur.Google Scholar
Dawson, CE, Stubblefield, EJ, Perrett, LL, King, AC, Whatmore, AM, Bashiruddin, JB, Stack, JA and MacMillan, AP (2008). Phenotypic and molecular characterization of Brucella isolates from marine mammals. BMC Microbiology 8: 224.CrossRefGoogle ScholarPubMed
Denoel, PA, Crawford, RM, Zygmunt, MS, Tibor, A, Weynants, VE, Godfroid, F, Hoover, DL and Letesson, JJ (1997). Survival of a bacterioferritin deletion mutant of Brucella melitensis 16M in human monocyte-derived macrophages. Infection and Immunity 65: 4337–4340.CrossRefGoogle ScholarPubMed
Denoel, PA, Zygmunt, MS, Weynants, V, Tibor, A, Lichtfouse, B, Briffeuil, P, Limet, JN and Letesson, JJ (1995). Cloning and sequencing of the bacterioferritin gene of Brucella melitensis 16M strain. FEBS Letters 361: 238–242.CrossRefGoogle ScholarPubMed
Detilleux, PG, Deyoe, BL and Cheville, NF (1990). Entry and intracellular localization of Brucella spp. in Vero cells: fluorescence and electron microscopy. Veterinary Pathology 27: 317–328.CrossRefGoogle ScholarPubMed
Dozot, M, Boigegrain, RA, Delrue, RM, Hallez, R, Ouahrani-Bettache, S, Danese, I, Letesson, JJ, De Bolle, X and Köhler, S (2006). The stringent response mediator Rsh is required for Brucella melitensis and Brucella suis virulence, and for expression of the type IV secretion system virB. Cellular Microbiology 8: 1791–1802.CrossRefGoogle ScholarPubMed
Enright, FM (1990). The pathogenesis and pathobiology of Brucella infections in domestic animals. In: Nielsen, KH and Duncan, JR (eds) Animal Brucellosis. Boca Raton, FL: CRC Press, pp. 301–320.Google Scholar
Evenson, MA and Gerhardt, P (1955). Nutrition of brucellae: utilization of iron, magnesium and manganese for growth. Proceedings of the Society for Experimental Biology and Medicine 89: 678–680.CrossRefGoogle ScholarPubMed
Franz, DR, Jahrling, PB, Friedlander, AM, McClain, DJ, Hoover, DL, Bryne, WR, Pavlin, JA, Christopher, GW and Eitzen, EM (1997). Clinical recognition and management of patients exposed to biological warfare agents. Journal of the American Medical Association 278: 399–411.CrossRefGoogle ScholarPubMed
Gary, ND, Kupferberg, LL and Graf, LH (1955). Demonstration of an iron-activated aldolase in sonic extracts of Brucella suis. Journal of Bacteriology 69: 478–479.CrossRefGoogle ScholarPubMed
Gee, JM, Valderas, MW, Kovach, ME, Grippe, VL, Robertson, GT, Ng, W-L, Richardson, JM, Winkler, ME and Roop, RM II (2005). The Brucella abortus Cu,Zn superoxide dismutase is required for optimal resistance to oxidative killing by murine macrophages and wild-type virulence in experimentally infected mice. Infection and Immunity 73: 2873–2880.CrossRefGoogle ScholarPubMed
Gerhardt, P (1958). The nutrition of brucellae. Bacteriological Reviews 22: 81–98.CrossRefGoogle ScholarPubMed
González-Carreró, MI, Sangari, FJ, Agüero, J and García-Lobo, JM (2002). Brucella abortus 2308 produces brucebactin, a highly efficient catecholic siderophore. Microbiology 148: 353–360.CrossRefGoogle ScholarPubMed
Griffiths, E (1999). Iron in biological systems. In: Bullen, JJ and Griffiths, E (eds) Iron and Infection. Molecular, Physiological and Clinical Aspects, 2nd edn. New York: John Wiley & Sons, pp. 1–25.Google Scholar
Günzel, D, Kucharski, LM, Kehres, DG, Romero, MF and Maguire, ME (2006). The MgtC virulence factor of Salmonella enterica serovar Typhimurium activates Na+,K+-ATPase. Journal of Bacteriology 188: 5586–5594.CrossRefGoogle ScholarPubMed
Jain, N, Rodriquez, AC, Kimsawatde, G, Seleem, MN, Boyle, SM and Sriranganathan, N (2011). Effect of entF deletion on iron acquisition and erythritol metabolism by Brucella abortus 2308. FEMS Microbiology Letters 316: 1–6.CrossRefGoogle ScholarPubMed
Jubier-Maurin, V, Rodrique, A, Ouahrani-Bettache, S, Layssac, M, Mandrand-Berthelos, MA, Köhler, S and Liautard, JP (2001). Identification of the nik gene cluster of Brucella suis: regulation and contribution to urease activity. Journal of Bacteriology 183: 426–434.CrossRefGoogle ScholarPubMed
Kehl-Fie, TE and Skaar, EP (2010). Nutritional immunity beyond iron: a role for manganese and zinc. Current Opinion in Chemical Biology 14: 218–224.CrossRefGoogle Scholar
Kim, S, Watanabe, K, Shirahata, T and Watarai, M (2004). Zinc uptake system (znuA locus) of Brucella abortus is essential for intracellular survival and virulence in mice. Journal of Veterinary Medical Science 66: 1059–1063.CrossRefGoogle ScholarPubMed
Lavigne, JP, O'Callaghan, D and Blanc-Potard, AB (2005). Requirement of MgtC for Brucella suis intramacrophagic growth: a potential mechanism shared by Salmonella enterica and Mycobacterium tuberculosis for adaptation to a low-Mg2+ environment. Infection and Immunity 73: 3160–3163.CrossRefGoogle ScholarPubMed
Lestrate, P, Delrue, RM, Danese, I, Didembourg, C, Taminiau, B, Mertens, P, De Bolle, X, Tibor, A, Tang, CM and Letesson, JJ (2000). Identification and characterization of in vivo attenuated mutants of Brucella melitensis. Molecular Microbiology 38: 543–551.CrossRefGoogle ScholarPubMed
LeVier, K, Phillips, RW, Grippe, VK, Roop, RM II and Walker, GC (2000). Similar requirements of a plant symbiont and a mammalian pathogen for prolonged intracellular survival. Science 287: 2492–2493.CrossRefGoogle Scholar
Li, Y and Zamble, DR (2009). Nickel homeostasis and nickel regulation: an overview. Chemical Reviews 109: 4617–4643.CrossRefGoogle ScholarPubMed
Lopez, M, Köhler, S and Winum, JY (2012). Zinc metalloenzymes as new targets against the bacterial pathogen Brucella. Journal of Inorganic Biochemistry (in press).CrossRefGoogle ScholarPubMed
López-Goñi, I and Moriyón, I (1995). Production of 2,3-dihydroxybenzoic acid by Brucella species. Current Microbiology 31: 291–293.CrossRefGoogle Scholar
López-Goñi, I, Moriyón, I and Neilands, JB (1992). Identification of 2,3-dihydrobenzoic acid as a Brucella abortus siderophore. Infection and Immunity 60: 4496–4503.CrossRefGoogle Scholar
Lucero, NE, Corazza, R, Almuzara, MN, Reynes, E, Escobar, GI, Boeri, E and Ayala, SM (2010). Human Brucella canis outbreak linked to infection in dogs. Epidemiology and Infection 138: 280–285.CrossRefGoogle ScholarPubMed
Martin, DW, Baumgartner, JE, Gee, JM, Anderson, ES and Roop, RM II (2012). SodA is a major metabolic antioxidant in Brucella abortus 2308 that plays a significant, but limited, role in the virulence of this strain in the mouse model. Microbiology, published online May 3, 2012, doi:10.1099/mic.0.059584-0.CrossRefGoogle Scholar
Martínez, J, Ugalde, RA and Almirón, M (2005). Dimeric Brucella abortus Irr protein controls its own expression and binds heme. Microbiology 151: 3427–3433.CrossRefGoogle Scholar
Martínez, J, Ugalde, RA and 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.CrossRefGoogle ScholarPubMed
McCullough, WG, Mills, RC, Herbst, EJ, Roessler, WG and Brewer, CR (1947). Studies on the nutritional requirements of Brucella suis. Journal of Bacteriology 53: 5–15.CrossRefGoogle ScholarPubMed
Menscher, EA, Caswell, CC, Anderson, ES and Roop, RM II (2012). Mur regulates the gene encoding the manganese transporter MntH in Brucella abortus 2308. Journal of Bacteriology 194: 561–566.CrossRefGoogle ScholarPubMed
Meyer, ME (1967). Metabolic characterization of the genus Brucella. VI. Growth stimulation by i-erythritol compared with strain virulence for guinea pigs. Journal of Bacteriology 93: 996–1000.CrossRefGoogle ScholarPubMed
Moomaw, AS and Maguire, ME (2008). The unique nature of Mg2+ channels. Physiology (Bethesda) 23: 275–285.Google ScholarPubMed
Moreno, E, Stackenbrandt, E, Dorsch, M, Wolters, J, Busch, M and Mayer, H (1990). Brucella abortus 16S rRNA and lipid A reveal a phylogenetic relationship with members of the alpha-2 subdivision of the class Proteobacteria. Journal of Bacteriology 172: 3569–3576.CrossRefGoogle ScholarPubMed
Nairz, M, Schroll, A, Sonnweber, T and Weiss, G (2010). The struggle for iron – a metal at the host-pathogen interface. Cellular Microbiology 12: 1691–1702.CrossRefGoogle Scholar
Nairz, M, Theurl, I, Ludwiczek, S, Theurl, M, Mair, SM, Fritsche, G and Weiss, G (2007). The co-ordinated regulation of iron homeostasis in murine macrophages limits the availability of iron for intracellular Salmonella Typhimurium. Cellular Microbiology 9: 2126–2140.CrossRefGoogle ScholarPubMed
Nemeth, E, Tuttle, MS, Powelson, J, Vaughn, MB, Donovan, A, Ward, DM, Ganz, T and Kaplan, J (2004). Hepcidin regulates iron efflux by binding to ferroportin and inducing its internalization. Science 306: 2090–2093.CrossRefGoogle ScholarPubMed
Nicoletti, P, Lenk, RP, Popescu, MC and Swenson, CE (1989). Efficacy of various treatment regimens, using liposomal streptomycin in cows with brucellosis. American Journal of Veterinary Research 50: 1004–1007.Google ScholarPubMed
Nymo, IH, Tryland, N and Godfroid, J (2011). A review of Brucella infection in marine mammals, with special emphasis on Brucella pinnipedialis in the hooded seal (Cystophora cristata). Veterinary Research 42: 93.CrossRefGoogle ScholarPubMed
O'Callaghan, D, Cazevieille, C, Allardet-Servent, A, Boschiroli, ML, Bourg, G, Foulongne, V, Frutos, P, Kulakov, Y and Ramuz, M (1999). A homologue of the Agrobacterium tumefaciens VirB and Bordetella Ptl type IV secretion systems is essential for intracellular survival of Brucella suis. Molecular Microbiology 33: 2110–1220.CrossRefGoogle ScholarPubMed
O'Callaghan, D and Whatmore, AM (2011). Brucella genomics as we enter the multi-genomeera. Briefings in Functional Genomics 10: 334–341.CrossRefGoogle Scholar
Papp-Wallace, KM and Maguire, ME (2006). Manganese transport and the role of manganese in virulence. Annual Review of Microbiology 60: 187–209.CrossRefGoogle ScholarPubMed
Pappas, G, Panagopoulou, P, Christou, L and Tsianos, EV (2006). The new global map of human brucellosis. Lancet Infectious Diseases 6: 91–99.CrossRefGoogle ScholarPubMed
Parent, MA, Bellaire, BH, Murphy, EA, Roop, RM II, Elzer, PH and Baldwin, CL (2002). Brucella abortus siderophore 2,3-dihydroxybenzoic acid (2,3-DHBA) facilitates intracellular survival of the bacteria. Microbial Pathogenesis 32: 239–248.Google Scholar
Paulley, JT, Anderson, ES and Roop, RM II (2007). Brucella abortus requires the heme transporter BhuA for maintenance of chronic infection in BALB/c mice. Infection and Immunity 75: 5248–5254.CrossRefGoogle ScholarPubMed
Pizzaro-Cerdá, J, Méresse, S, Parton, RG, van der Goot, G, Sola-Landa, A, López-Goñi, I, Moreno, E and Gorvel, JP (1998). Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infection and Immunity 66: 5711–5724.CrossRefGoogle Scholar
Posey, JE and Gherardini, FC (2000). Lack of a role for iron in the Lyme disease pathogen. Science 288: 1651–1653.CrossRefGoogle ScholarPubMed
Puri, S and O'Brian, MR (2008). The hmuQ and hmuD genes from Bradyrhizobium japonicum encode heme-degrading enzymes. Journal of Bacteriology 188: 6476–6482.CrossRefGoogle Scholar
Raymond, KN and Dertz, EA (2004). Biochemical and physical properties of siderophores. In: Crosa, JH, Mey, AR and Payne, SM (eds) Iron Transport in Bacteria. Washington: ASM Press, pp. 3–17.Google Scholar
Rodionov, DA, Gelfand, MS, Todd, JD, Curson, ARJ and Johnston, AWB (2006). Computational reconstruction of iron- and manganese-responsive transcriptional networks in α- proteobacteria. PLoS Computational Biology 2: 1568–1585.CrossRefGoogle ScholarPubMed
Roop, RM II, Anderson, E, Ojeda, J, Martinson, D, Menscher, E and Martin, DW (2011). Metal acquisition by Brucella strains. In: López-Goñi, I and O'Callaghan, D (eds) Brucella: Molecular Microbiology and Genetics. Norfolk: Caister Academic Press, pp. 179–199.Google Scholar
Roop, RM II, Gaines, JM, Anderson, ES, Caswell, CC and Martin, DW (2009). Survival of the fittest: how Brucella strains adapt to their intracellular niche in the host. Medical Microbiology and Immunology 198: 221–238.CrossRefGoogle ScholarPubMed
Sanders, TH, Higuchi, K and Brewer, CR (1953). Studies on the nutrition of Brucella melitensis. Journal of Bacteriology 66: 294–299.CrossRefGoogle ScholarPubMed
Sangari, FJ, Cayón, AM, Seoane, A and García-Lobo, JM (2010). Brucella abortus ure2 region contains an acid-activated urea transporter and a nickel transport system. BMC Microbiology 10: 107.CrossRefGoogle Scholar
Sangari, FJ, Seoane, A, Rodríguez, MC, Agüero, J and García-Lobo, JM (2007). Characterization of the urease operon of Brucella abortus and assessment of its role in virulence of the bacterium. Infection and Immunity 75: 774–780.CrossRefGoogle ScholarPubMed
Scholz, HC, Hubalek, Z, Sedláček, I, Vergnaud, G, Tomaso, H, Al Dahouk, S, Melzer, F, Kämpfer, P, Nuebauer, H, Cloeckaert, A, Marquart, M, Zygmunt, MS, Whatmore, AM, Falsen, E, Bahn, P, Göllner, C, Pfeffer, M, Huber, B, Busse, HJ and Knöckler, K (2008). Brucella microti sp. nov., isolated from the common vole Microtus arvalis. International Journal of Systematic and Evolutionary Microbiology 58: 375–382.CrossRefGoogle ScholarPubMed
Scholz, HC, Knöckler, K, Göllner, C, Bahn, P, Vergnaud, G, Tomaso, H, Al Dahouk, S, Kämpfer, P, Cloeckaert, A, Marquart, M, Zygmunt, MS, Whatmore, AM, Pfeffer, M, Huber, B, Busse, HJ and De, BK (2010). Brucella inopinata sp. nov., isolated from a breast implant infection. International Journal of Systematic and Evolutionary Microbiology 60: 801–808.CrossRefGoogle ScholarPubMed
Schroeder, S, Lawrence, AD, Biedendieck, R, Rose, RS, Deery, E, Graham, RM, McLean, KJ, Munro, AW, Rigby, SE and Warren, MJ (2009). Demonstration that CobG, the monooxygenase associated with the ring contraction process of the aerobic cobalamin (vitamin B12) biosynthetic pathway, contains an Fe-S center and a mononuclear non-heme iron center. Journal of Biological Chemistry 284: 4796–4805.CrossRefGoogle Scholar
Sieira, R, Comerci, DJ, Sánchez, DO and Ugalde, RA (2000). A homologue of an operon required for DNA transfer in Agrobacterium is required in Brucella abortus for virulence and intracellular replication. Journal of Bacteriology 182: 4849–4855.CrossRefGoogle Scholar
Sobota, J and 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. Proceedings of the National Academy of Sciences USA. 108: 5402–5407.CrossRefGoogle ScholarPubMed
Sola-Landa, A, Pizarro-Cerdá, J, Grilló, MJ, Moriyón, I, Blasco, JM, Gorvel, JP and López-Goñi, I (1998). A two-component regulatory system playing a critical role in plant pathogens and endosymbionts is present in Brucella abortus and controls cell invasion and virulence. Molecular Microbiology 29: 125–138.CrossRefGoogle ScholarPubMed
Smith, DL, Tao, T and Maguire, ME (1993). Membrane topology of a P-type ATPase. The MgtB magnesium transport protein of Salmonella typhimurium. Journal of Biological Chemistry 268: 22469–22479.CrossRefGoogle ScholarPubMed
Smith, H, Williams, AE, Pearce, JH, Keppie, J, Harris-Smith, PW, Fitzgeorge, RB and Witt, K (1962). Foetal erythritol: a cause of the localization of Brucella abortus in bovine contagious abortion. Nature 193: 47–49.CrossRefGoogle ScholarPubMed
Sohn, AH, Probert, WS, Glaser, CA, Gupta, N, Bollen, AW, Wong, JD, Grace, EM and McDonald, WC (2003). Human neurobrucellosis with intracebral granuloma caused by a marine mammal Brucella spp. Emerging Infectious Diseases 9: 485–488.CrossRefGoogle Scholar
Sperry, JF and Robertson, DC (1975). Erythritol catabolism by Brucella abortus. Journal of Bacteriology 121: 619–630.CrossRefGoogle ScholarPubMed
Stoenner, HG and Lackman, DB (1957). A new species of Brucella isolated from the desert wood rat, Neotoma lepida Thomas. American Journal of Veterinary Research 18: 947–951.Google ScholarPubMed
Summers, AO (2009). Damage control: defenses against toxic metals and metalloids. Current Opinion in Microbiology 12: 138–144.CrossRefGoogle ScholarPubMed
Taga, ME and Walker, GC (2010). Sinorhizobium meliloti requires a cobalamin-dependent ribonucleotide reductase for symbiosis with its plant host. Molecular Plant-Microbe Interactions 23: 1643–1654.CrossRefGoogle ScholarPubMed
Taketani, S (2005). Acquisition, mobilization and utilization of cellular iron and heme; endless findings and growing evidence of tight regulation. Tohoku Journal of Experimental Medicine 205: 297–318.CrossRefGoogle Scholar
Tatum, FM, Detilleux, PG, Sacks, JM and Halling, SM (1992). Construction of Cu-Zn superoxide dismutase deletions mutants of Brucella abortus: analysis of survival in vitro in epithelial and phagocytic cells and in vivo in mice. Infection and Immunity 60: 2863–2869.CrossRefGoogle ScholarPubMed
Valderas, MW and Roop, RM II (2006). Brucella and bioterrorism. In: Anderson, B, Friedman, H and Bendinelli, M (eds) Microorganisms and Bioterrorism. New York: Springer, pp. 139–153.CrossRefGoogle Scholar
Waldron, KJ and Robinson, NJ (2009). How do bacterial cells ensure that metalloproteins get the correct metal? Nature Reviews Microbiology 6: 25–35.CrossRefGoogle Scholar
Wanke, MM (2004). Canine brucellosis. Animal Reproduction Science 82–83: 195–207.CrossRefGoogle ScholarPubMed
Waring, WS, Elberg, SS, Schneider, P and Green, W (1953). The role of iron in the biology of Brucella suis. I. Growth and nutrition. Journal of Bacteriology 66: 82–91.CrossRefGoogle Scholar
Weinberg, ED (1995). Acquisition of iron and other nutrients in vivo. In: Roth, JA, Bolin, CA, Brogden, KA, Minion, FC and Wannemuehler, MJ (eds) Virulence Mechanisms of Bacterial Pathogens, 2nd edn. Washington: ASM Press, pp. 79–93.Google Scholar
Weiss, G (2005). Modification of iron regulation by the inflammatory response. Best Practices in Research in Clinical Haematology 18: 183–201.CrossRefGoogle ScholarPubMed
Yang, X, Becker, T, Walters, N and Pascual, DW (2006). Deletion of znuA virulence factor attenuates Brucella abortus and confers protection against wild-type challenge. Infection and Immunity 74: 3874–3879.CrossRefGoogle ScholarPubMed
Zaharik, ML, Cullen, VL, Fung, AM, Libby, SJ, Kujat Choy, SL, Coburn, B, Kehres, DG, Maguire, ME, Fang, FC and 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. Infection and Immunity 72: 5522–5525.CrossRefGoogle Scholar
ZoBell, CE and Meyer, KF (1932). Metabolism studies on the Brucella group. VIII. Nutrient requirements in synthetic mediums. Journal of Infectious Diseases 51: 344–360.CrossRefGoogle Scholar