The Yersinia pestis siderophore, yersiniabactin, and the ZnuABC system both contribute to zinc acquisition and the development of lethal septicaemic plague in mice

Molecular Microbiology

Volumn 93, Issue 4, 2014, Pages 759-775

  Bobrov, Alexander G ^a   Kirillina, Olga ^a   Fetherston, Jacqueline D ^a   Miller, M Clarke ^b,c   Burlison, Joseph A ^b   Perry, Robert D ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF LOUISVILLE   (United States)

^c UNIVERSITY OF NORTH GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; BETA GALACTOSIDASE; IRON; MEMBRANE PROTEIN; MEMBRANE RECEPTOR; PROTEIN HMWP2; PROTEIN PSN; PROTEIN TONB; PROTEIN YBTPQ; PROTEIN YBTX; PROTEIN ZNUA; PROTEIN ZNUABC; SIDEROPHORE; SYNTHETASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; YERSINIABACTIN; ZINC ION; PHENOL DERIVATIVE; THIAZOLE DERIVATIVE; VIRULENCE FACTOR; ZINC;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; FEMALE; GENETIC CODE; GRAM NEGATIVE SEPSIS; GROWTH STIMULATION; INNER MEMBRANE; ION TRANSPORT; IRON TRANSPORT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; REPORTER GENE; YERSINIA PESTIS; ANIMAL; DISEASE MODEL; METABOLISM; MICROBIOLOGY; PATHOLOGY; PLAGUE; SEPSIS; VIRULENCE;

BACTERIA (MICROORGANISMS); MUS; YERSINIA PESTIS;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; DISEASE MODELS, ANIMAL; MICE; PHENOLS; PLAGUE; SEPSIS; THIAZOLES; VIRULENCE; VIRULENCE FACTORS; YERSINIA PESTIS; ZINC;

EID: 84908546748     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12693     Document Type: Article

References (114)

1. Althaus, E.W., Outten, C.E., Olson, K.E., Cao, H., and O'Halloran, T.V. (1999) The ferric uptake regulation (Fur) repressor is a zinc metalloprotein. Biochemistry 38: 6559-6569.
2. 2+ uptake system ZnuABC is required for bacterial zinc homeostasis in intracellular environments and contributes to the virulence of Salmonella enterica. Infect Immun 75: 5867-5876.
3. Andreini, C., Banci, L., Bertini, I., and Rosato, A. (2006) Zinc through the three domains of life. J Proteome Res 5: 3173-3178.
4. Bayle, L., Chimalapati, S., Schoehn, G., Brown, J., Vernet, T., and Durmort, C. (2011) Zinc uptake by Streptococcus pneumoniae depends on both AdcA and AdcAII and is essential for normal bacterial morphology and virulence. Mol Microbiol 82: 904-916.
5. Bearden, S.W., and Perry, R.D. (1999) The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol Microbiol 32: 403-414.
6. Bearden, S.W., Fetherston, J.D., and Perry, R.D. (1997) Genetic organization of the yersiniabactin biosynthetic region and construction of avirulent mutants in Yersinia pestis. Infect Immun 65: 1659-1668.
7. Beesley, E.D., Brubaker, R.R., Janssen, W.A., and Surgalla, M.J. (1967) Pesticins. III. Expression of coagulase and mechanism of fibrinolysis. J Bacteriol 94: 19-26.
8. Brandel, J., Humbert, N., Elhabiri, M., Schalk, I.J., Mislin, G.L.A., and Albrecht-Gary, A.-M. (2012) Pyochelin, a siderophore of Pseudomonas aeruginosa: physicochemical characterization of the iron(III), copper(II) and zinc(II) complexes. Dalton Trans 41: 2820-2834.
9. Braud, A., Hannauer, M., Mislin, G.L.A., and Schalk, I.J. (2009a) The Pseudomonas aeruginosa pyochelin-iron uptake pathway and its metal specificity. J Bacteriol 191: 3517-3525.
10. Braud, A., Hoegy, F., Jezequel, K., Lebeau, T., and Schalk, I.J. (2009b) New insights into the metal specificity of the Pseudomonas aeruginosa pyoverdine-iron uptake pathway. Environ Microbiol 11: 1079-1091.
11. Braud, A., Geoffroy, V., Hoegy, F., Mislin, G.L.A., and Schalk, I.J. (2010) Presence of the siderophores pyoverdine and pyochelin in the extracellular medium reduces toxic metal accumulation in Pseudomonas aeruginosa and increases bacterial metal tolerance. Environ Microbiol Rep 2: 419-425.
12. Brubaker, R.R. (1969) Mutation rate to nonpigmentation in Pasteurella pestis. J Bacteriol 98: 1404-1406.
13. Campoy, S., Jara, M., Busquets, N., Pérez de Rozas, A.M., Badiola, I., and Barbé, J. (2002) Role of the high-affinity zinc uptake znuABC system in Salmonella enterica serovar typhimurium virulence. Infect Immun 70: 4721-4725.
14. Cerasi, M., Ammendola, S., and Battistoni, A. (2013) Competition for zinc binding in the host-pathogen interaction. Front Cell Infect Microbiol 3: 108.
15. Cerasi, M., Liu, J.Z., Ammendola, S., Poe, A.J., Petrarca, P., Pesciaroli, M., etal. (2014) The ZupT transporter plays an important role in zinc homeostasis and contributes to Salmonella enterica virulence. Metallomics 6: 845-853.
16. Cescau, S., Cwerman, H., Létoffé, S., Delepelaire, P., Wandersman, C., and Biville, F. (2007) Heme acquisition by hemophores. Biometals 20: 603-613.
17. Chatfield, C.H., Mulhern, B.J., Burnside, D.M., and Cianciotto, N.P. (2011) Legionella pneumophila LbtU acts as a novel, TonB-independent receptor for the legiobactin siderophore. J Bacteriol 193: 1563-1575.
18. Chatfield, C.H., Mulhern, B.J., Viswanathan, V.K., and Cianciotto, N.P. (2012) The major facilitator superfamily-type protein LbtC promotes the utilization of the legiobactin siderophore by Legionella pneumophila. Microbiology 158: 721-735.
19. Chaturvedi, K.S., Hung, C.S., Crowley, J.R., Stapleton, A.E., and Henderson, J.P. (2012) The siderophore yersiniabactin binds copper to protect pathogens during infection. Nat Chem Biol 8: 731-736.
20. Citiulo, F., Jacobsen, I.D., Miramón, P., Schild, L., Brunke, S., Zipfel, P., etal. (2012) Candida albicans scavenges host zinc via Pra1 during endothelial invasion. PLoS Pathog 8: e1002777.
21. Corbett, D., Wang, J., Schuler, S., Lopez-Castejon, G., Glenn, S., Brough, D., etal. (2012) Two zinc uptake systems contribute to the full virulence of Listeria monocytogenes during growth in vitro and in vivo. Infect Immun 80: 14-21.
22. Corbin, B.D., Seeley, E.H., Raab, A., Feldmann, J., Miller, M.R., Torres, V.J., etal. (2008) Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319: 962-965.
23. Cortese, M.S., Paszczynski, A., Lewis, T.A., Sebat, J.L., Borek, V., and Crawford, R.L. (2002) Metal chelating properties of pyridine-2, 6-bis(thiocarboxylic acid) produced by Pseudomonas spp. and the biological activities of the formed complexes. Biometals 15: 103-120.
24. Crouch, M.-L.V., Castor, M., Karlinsey, J.E., Kalhorn, T., and Fang, F.C. (2008) Biosynthesis and IroC-dependent export of the siderophore salmochelin are essential for virulence of Salmonella enterica serovar Typhimurium. Mol Microbiol 67: 971-983.
25. Dahiya, I., and Stevenson, R.M.W. (2010) The ZnuABC operon is important for Yersinia ruckeri infections of rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 33: 331-340.
26. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
27. Davis, L.M., Kakuda, T., and DiRita, V.J. (2009) A Campylobacter jejuni znuA orthologue is essential for growth in low-zinc environments and chick colonization. J Bacteriol 191: 1631-1640.
28. Desrosiers, D.C., Bearden, S.W., Mier, I., Jr, Abney, J., Paulley, J.T., Fetherston, J.D., etal. (2010) Znu is the predominant zinc importer in Yersinia pestis during in vitro growth but is not essential for virulence. Infect Immun 78: 5163-5177.
29. Fetherston, J.D., and Perry, R.D. (1994) The pigmentation locus of Yersinia pestis KIM6+ is flanked by an insertion sequence and includes the structural genes for pesticin sensitivity and HMWP2. Mol Microbiol 13: 697-708.
30. Fetherston, J.D., Lillard, J.W., Jr, and Perry, R.D. (1995) Analysis of the pesticin receptor from Yersinia pestis: role in iron-deficient growth and possible regulation by its siderophore. J Bacteriol 177: 1824-1833.
31. Fetherston, J.D., Bertolino, V.J., and Perry, R.D. (1999) YbtP and YbtQ: two ABC transporters required for iron uptake in Yersinia pestis. Mol Microbiol 32: 289-299.
32. Fetherston, J.D., Kirillina, O., Bobrov, A.G., Paulley, J.T., and Perry, R.D. (2010) The yersiniabactin transport system is critical for the pathogenesis of bubonic and pneumonic plague. Infect Immun 78: 2045-2052.
33. 2-macroglobulin bound zinc concentrations in the sera of healthy adults. J Clin Pathol 37: 1050-1054.
34. Forman, S., Paulley, J.T., Fetherston, J.D., Cheng, Y.-Q., and Perry, R.D. (2010) Yersinia ironomics: comparison of iron transporters among Yersinia pestis biotypes and its nearest neighbor, Yersinia pseudotuberculosis. Biometals 23: 275-294.
35. Furrer, J.L., Sanders, D.N., Hook-Barnard, I.G., and McIntosh, M.A. (2002) Export of the siderophore enterobactin in Escherichia coli: involvement of a 43kDa membrane exporter. Mol Microbiol 44: 1225-1234.
36. Gabbianelli, R., Scotti, R., Ammendola, S., Petrarca, P., Nicolini, L., and Battistoni, A. (2011) Role of ZnuABC and ZinT in Escherichia coli O157:H7 zinc acquisition and interaction with epithelial cells. BMC Microbiol 11: 36.
37. Garrido, M.E., Bosch, M., Medina, R., Llagostera, M., Pérez de Rozas, A.M., Badiola, I., and Barbé, J. (2003) The high-affinity zinc-uptake system znuACB is under control of the iron-uptake regulator (fur) gene in the animal pathogen Pasteurella multocida. FEMS Microbiol Lett 221: 31-37.
38. Gong, S., Bearden, S.W., Geoffroy, V.A., Fetherston, J.D., and Perry, R.D. (2001) Characterization of the Yersinia pestis Yfu ABC iron transport system. Infect Immun 67: 2829-2837.
39. Graham, A.I., Hunt, S., Stokes, S.L., Bramall, N., Bunch, J., Cox, A.G., etal. (2009) Severe zinc depletion of Escherichia coli: roles for high-affinity zinc binding by ZinT, zinc transport and zinc-independent proteins. J Biol Chem 284: 18377-18389.
40. Grass, G., Wong, M.D., Rosen, B.P., Smith, R.L., and Rensing, C. (2002) ZupT Is a Zn(II) uptake system in Escherichia coli. J Bacteriol 184: 864-866.
41. Hannauer, M., Braud, A., Hoegy, F., Ronot, P., Boos, A., and Schalk, I.J. (2012) The PvdRT-OpmQ efflux pump controls the metal selectivity of the iron uptake pathway mediated by the siderophore pyoverdine in Pseudomonas aeruginosa. Environ Microbiol 14: 1696-1708.
42. Hantke, K. (2005) Bacterial zinc uptake and regulators. Curr Opin Microbiol 8: 196-202.
43. Hesketh, A., Kock, H., Mootien, S., and Bibb, M. (2009) The role of absC, a novel regulatory gene for secondary metabolism, in zinc-dependent antibiotic production in Streptomyces coelicolor A3(2). Mol Microbiol 74: 1427-1444.
44. Higuchi, K., and Smith, J.L. (1961) Studies on the nutrition and physiology of Pasteurella pestis. VI. A differential plating medium for the estimation of the mutation rate to avirulence. J Bacteriol 81: 605-608.
45. Hood, M.I., and Skaar, E.P. (2012) Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 10: 525-537.
46. Hood, M.I., Mortensen, B.L., Moore, J.L., Zhang, Y., Kehl-Fie, T.E., Sugitani, N., etal. (2012) Identification of an Acinetobacter baumannii zinc acquisition system that facilitates resistance to calprotectin-mediated zinc sequestration. PLoS Pathog 8: e1003068.
47. Jackson, S., and Burrows, T.W. (1956) The virulence-enhancing effect of iron on non-pigmented mutants of virulent strains of Pasteurella pestis. Br J Exp Pathol 37: 577-583.
48. Karlinsey, J.E., Maguire, M.E., Becker, L.A., Crouch, M.-L.V., and Fang, F.C. (2010) The phage shock protein PspA facilitates divalent metal transport and is required for virulence of Salmonella enterica sv. Typhimurium. Mol Microbiol 78: 669-685.
49. Katayama, A., Tsujii, A., Wada, A., Nishino, T., and Ishihama, A. (2002) Systematic search for zinc-binding proteins in Escherichia coli. Eur J Biochem 269: 2403-2413.
50. Kehl-Fie, T.E., and Skaar, E.P. (2010) Nutritional immunity beyond iron: a role for manganese and zinc. Curr Opin Chem Biol 14: 218-224.
51. 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. J Vet Med Sci 66: 1059-1063.
52. Kingsley, R.A., Reissbrodt, R., Rabsch, W., Ketley, J.M., Tsolis, R.M., Everest, P., etal. (1999) Ferrioxamine-mediated iron(III) utilization by Salmonella enterica. Appl Environ Microbiol 65: 1610-1618.
53. Kobayashi, S., Hidaka, S., Kawamura, Y., Ozaki, M., and Hayase, Y. (1998a) Micacocidin A, B and C, novel antimycoplasma agents from Pseudomonas sp. I. taxonomy, fermentation, isolation, physico-chemical properties and biological activities. J Antibiot (Tokyo) 51: 323-327.
54. Kobayashi, S., Nakai, H., Ikenishi, Y., Sun, W.-Y., Ozaki, M., Hayase, Y., and Takeda, R. (1998b) Micacocidin A, B and C, novel antimycoplasma agents from Pseudomonas sp. II. Structure elucidation. J Antibiot (Tokyo) 51: 328-332.
55. Kobayashi, S., Ikenishi, Y., Takinami, Y., Takema, M., Sun, W.Y., Ino, A., and Hayase, Y. (2000) Preparation and antimicrobial activity of micacocidin. J Antibiot (Tokyo) 53: 532-539.
56. Kreutzer, M.F., Kage, H., Gebhardt, P., Wackler, B., Saluz, H.P., Hoffmeister, D., and Nett, M. (2011) Biosynthesis of a complex yersiniabactin-like natural product via the mic locus in phytopathogen Ralstonia solanacearum. Appl Environ Microbiol 77: 6117-6124.
57. Kumar, P., Sannigrahi, S., and Tzeng, Y.-L. (2012) The Neisseria meningitidis ZnuD zinc receptor contributes to interactions with epithelial cells and supports heme utilization when expressed in Escherichia coli. Infect Immun 80: 657-667.
58. Lathem, W.W., Price, P.A., Miller, V.L., and Goldman, W.E. (2007) A plasminogen-activating protease specifically controls the development of primary pneumonic plague. Science 315: 509-513.
59. Leach, L.H., Morris, J.C., and Lewis, T.A. (2007) The role of the siderophore pyridine-2, 6-bis (thiocarboxylic acid) (PDTC) in zinc utilization by Pseudomonas putida DSM 3601. Biometals 20: 717-726.
60. Lewis, D.A., Klesney-Tait, J., Lumbley, S.R., Ward, C.K., Latimer, J.L., Ison, C.A., and Hansen, E.J. (1999) Identification of the znuA-encoded periplasmic zinc transport protein of Haemophilus ducreyi. Infect Immun 67: 5060-5068.
61. Li, Y., Qiu, Y., Gao, H., Guo, Z., Han, Y., Song, Y., etal. (2009) Characterization of Zur-dependent genes and direct Zur targets in Yersinia pestis. BMC Microbiol 9: 128.
62. Lim, K.H.L., Jones, C.E., vanden Hoven, R.N., Edwards, J.L., Falsetta, M.L., Apicella, M.A., etal. (2008) Metal binding specificity of the MntABC permease of Neisseria gonorrhoeae and its influence on bacterial growth and interaction with cervical epithelial cells. Infect Immun 76: 3569-3576.
63. Liu, J.Z., Jellbauer, S., Poe, A.J., Ton, V., Pesciaroli, M., Kehl-Fie, T.E., etal. (2012) Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11: 227-239.
64. Liu, M., Yan, M., Liu, L., and Chen, S. (2013) Characterization of a novel zinc transporter ZnuA acquired by Vibrio parahaemolyticus through horizontal gene transfer. Front Cell Infect Microbiol 3: 61.
65. Liuzzi, J.P., Lichten, L.A., Rivera, S., Blanchard, R.K., Aydemir, T.B., Knutson, M.D., etal. (2005) Interleukin-6 regulates the zinc transporter Zip14 in liver and contributes to the hypozincemia of the acute-phase response. Proc Natl Acad Sci USA 102: 6843-6848.
66. Lloubès, R., Goemaere, E., Zhang, X., Cascales, E., and Duché, D. (2012) Energetics of colicin import revealed by genetic cross-complementation between the Tol and Ton systems. Biochem Soc Trans 40: 1480-1485.
67. Ma, Z., Faulkner, M.J., and Helmann, J.D. (2012) Origins of specificity and cross-talk in metal ion sensing by Bacillus subtilis Fur. Mol Microbiol 86: 1144-1155.
68. Michel, L., Bachelard, A., and Reimmann, C. (2007) Ferripyochelin uptake genes are involved in pyochelin-mediated signalling in Pseudomonas aeruginosa. Microbiology 153: 1508-1518.
69. Miethke, M., and Marahiel, M.A. (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71: 413-451.
70. Miller, D.A., Luo, L., Hillson, N., Keating, T.A., and Walsh, C.T. (2002) Yersiniabactin synthetase: a four-protein assembly line producing the nonribosomal peptide/polyketide hybrid siderophore of Yersinia pestis. Chem Biol 9: 333-449.
71. Miller, J.H. (1992) A Short Course in Bacterial Genetics. A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
72. Miller, M.C., and DeMoll, E. (2011) Extraction, purification, and identification of Yersiniabactin, the siderophore of Yersinia pestis. Curr Protoc Microbiol 23: 5B.3.1-5B.3.22.
73. Miller, M.C., Fetherston, J.D., Pickett, C.L., Bobrov, A.G., Weaver, R.H., DeMoll, E., and Perry, R.D. (2010) Reduced synthesis of the Ybt siderophore or production of aberrant Ybt-like molecules activates transcription of yersiniabactin genes in Yersinia pestis. Microbiology 156: 2226-2238.
74. Mills, S.A., and Marletta, M.A. (2005) Metal binding characteristics and role of iron oxidation in the ferric uptake regulator from Escherichia coli. Biochemistry 44: 13553-13559.
75. Murphy, T.F., Brauer, A.L., Kirkham, C., Johnson, A., Koszelak-Rosenblum, M., and Malkowski, M.G. (2013) Role of the zinc uptake ABC transporter of Moraxella catarrhalis in persistence in the respiratory tract. Infect Immun 81: 3406-3413.
76. Nakai, H., Kobayashi, S., Ozaki, M., Hayase, Y., and Takeda, R. (1999) Micacocidin A. Acta Crystallogr C55: 54-56.
77. Napolitano, M., Rubio, M.Á., Santamaría-Gómez, J., Olmedo-Verd, E., Robinson, N.J., and Luque, I. (2012) Characterization of the response to zinc deficiency in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 194: 2426-2436.
78. Nielubowicz, G.R., Smith, S.N., and Mobley, H.L.T. (2010) Zinc uptake contributes to motility and provides a competitive advantage to Proteus mirabilis during experimental urinary tract infection. Infect Immun 78: 2823-2833.
79. Ó Cuív, P., Clarke, P., Lynch, D., and 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.
80. Perry, R.D., and Fetherston, J.D. (1997) Yersinia pestis - etiologic agent of plague. Clin Microbiol Rev 10: 35-66.
81. Perry, R.D., and Fetherston, J.D. (2004) Iron and heme uptake systems. In Yersinia Molecular and Cellular Biology. Carniel, E., and Hinnebusch, B.J. (eds). Norfolk, UK: Horizon Bioscience, pp. 257-283.
82. Perry, R.D., and Fetherston, J.D. (2011) Yersiniabactin iron uptake: mechanisms and role in Yersinia pestis pathogenesis. Microbes Infect 13: 808-817.
83. 2+-response plasmid pCD1 of Yersinia pestis KIM5. Infect Immun 66: 4611-4623.
84. Perry, R.D., Balbo, P.B., Jones, H.A., Fetherston, J.D., and DeMoll, E. (1999) Yersiniabactin from Yersinia pestis: biochemical characterization of the siderophore and its role in iron transport and regulation. Microbiology 145: 1181-1190.
85. Perry, R.D., Abney, J., Mier, I., Jr, Lee, Y., Bearden, S.W., and Fetherston, J.D. (2003a) Regulation of the Yersinia pestis Yfe and Ybt iron transport systems. Adv Exp Med Biol 529: 275-283.
86. Perry, R.D., Shah, J., Bearden, S.W., Thompson, J.M., and Fetherston, J.D. (2003b) Yersinia pestis TonB: role in iron, heme and hemoprotein utilization. Infect Immun 71: 4159-4162.
87. Perry, R.D., Bobrov, A.G., Kirillina, O., Rhodes, E.R., Actis, L.A., and Fetherston, J.D. (2012) Yersinia pestis transition metal divalent cation transporters. Adv Exp Med Biol 954: 267-279.
88. Petrarca, P., Ammendola, S., Pasquali, P., and Battistoni, A. (2010) The Zur-regulated ZinT protein is an auxiliary component of the high-affinity ZnuABC zinc transporter that facilitates metal recruitment during severe zinc shortage. J Bacteriol 192: 1553-1564.
89. Plumptre, C.D., Eijkelkamp, B.A., Morey, J.R., Behr, F., Couñago, R.M., Ogunniyi, A.D., etal. (2014) AdcA and AdcAII employ distinct zinc acquisition mechanisms and contribute additively to zinc homeostasis in Streptococcus pneumoniae. Mol Microbiol 91: 834-851.
90. Rahuel-Claremont, S., and Dunn, M.F. (1998) The biological chemistry of zinc. In Copper and Zinc in Inflammatory and Degenerative Diseases. Rainsford, K.D., Milanino, R., Sorenson, R.J., and Velo, G.P. (eds). Dordrecht, the Netherlands: Kluwer Academic Publisher, pp. 47-59.
91. Ramakrishnan, G., Meeker, A., and Dragulev, B. (2008) fslE is necessary for siderophore-mediated iron acquisition in Francisella tularensis Schu S4. J Bacteriol 190: 5353-5361.
92. Ramakrishnan, G., Sen, B., and Johnson, R. (2012) Paralogous outer membrane proteins mediate uptake of different forms of iron and synergistically govern virulence in Francisella tularensis tularensis. J Biol Chem 287: 25191-25202.
93. Reed, L.J., and Muench, H. (1938) A simple method for estimating fifty percent endpoints. Am J Hyg 27: 493-497.
94. Rink, L., and Haase, H. (2007) Zinc homeostasis and immunity. Trends Immunol 28: 1-4.
95. Rosadini, C.V., Gawronski, J.D., Raimunda, D., Argüello, J.M., and Akerley, B.J. (2011) A novel zinc binding system, ZevAB, is critical for survival of nontypeable Haemophilus influenzae in a murine lung infection model. Infect Immun 79: 3366-3376.
96. Sabri, M., Houle, S., and Dozois, C.M. (2009) Roles of the extraintestinal pathogenic Escherichia coli ZnuACB and ZupT zinc transporters during urinary tract infection. Infect Immun 77: 1155-1164.
97. Schaible, U.E., and Kaufmann, S.H.E. (2004) Iron and microbial infection. Nat Rev Microbiol 2: 946-953.
98. Schalk, I.J., and Guillon, L. (2013) Pyoverdine biosynthesis and secretion in Pseudomonas aeruginosa: implications for metal homeostasis. Environ Microbiol 15: 1661-1673.
99. Schalk, I.J., Hannauer, M., and Braud, A. (2011) New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13: 2844-2854.
100. Sebbane, F., Mandrand-Berthelot, M.-A., and Simonet, M. (2002) Genes encoding specific nickel transport systems flank the chromosomal urease locus of pathogenic Yersiniae. J Bacteriol 184: 5706-5713.
101. Sebbane, F., Jarrett, C.O., Gardner, D., Long, D., and Hinnebusch, B.J. (2006) Role of the Yersinia pestis plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea-borne plague. Proc Natl Acad Sci USA 103: 5526-5530.
102. Sebbane, F., Jarrett, C., Gardner, D., Long, D., and Hinnebusch, B.J. (2010) Role of the Yersinia pestis yersiniabactin iron acquisition system in the incidence of flea-borne plague. PLoS ONE 5: e14379.
103. Sheikh, M.A., and Taylor, G.L. (2009) Crystal structure of the Vibrio cholerae ferric uptake regulator (Fur) reveals insights into metal co-ordination. Mol Microbiol 72: 1208-1220.
104. Sohnle, P.G., Hunter, M.J., Hahn, B., and Chazin, W.J. (2000) Zinc reversible antimicrobial activity of recombinant calprotectin (migration inhibitory factor-related proteins 8 and 14). J Infect Dis 182: 1272-1275.
105. Stork, M., Bos, M.P., Jongerius, I., de Kok, N., Schilders, I., Weynants, V.E., etal. (2010) An outer membrane receptor of Neisseria meningitidis involved in zinc acquisition with vaccine potential. PLoS Pathog 6: e1000969.
106. Stork, M., Grijpstra, J., Bos, M.P., Mañas Torres, C., Devos, N., Poolman, J.T., etal. (2013) Zinc piracy as a mechanism of Neisseria meningitidis for evasion of nutritional immunity. PLoS Pathog 9: e1003733.
107. Surgalla, M.J., and Beesley, E.D. (1969) Congo red-agar plating medium for detecting pigmentation in Pasteurella pestis. Appl Microbiol 18: 834-837.
108. r phenotypes of yersiniae. Infect Immun 43: 895-900.
109. Vallee, B.L., and Falchuk, K.H. (1993) The biochemical basis of zinc physiology. Physiol Rev 73: 79-118.
110. Weinberg, E.D. (1972) Infectious diseases influenced by trace element environment. Ann N Y Acad Sci 199: 274-284.
111. Weston, B.F., Brenot, A., and Caparon, M.G. (2009) The metal homeostasis protein, Lsp, of Streptococcus pyogenes is necessary for acquisition of zinc and virulence. Infect Immun 77: 2840-2848.
112. Yang, X., Becker, T., Walters, N., and Pascual, D.W. (2006) Deletion of znuA virulence factor attenuates Brucella abortus and confers protection against wild-type challenge. Infect Immun 74: 3874-3879.
113. Youard, Z., Wenner, N., and Reimmann, C. (2011) Iron acquisition with the natural siderophore enantiomers pyochelin and enantio-pyochelin in Pseudomonas species. Biometals 24: 513-522.
114. Zhao, B., Moody, S.C., Hider, R.C., Lei, L., Kelly, S.L., Waterman, M.R., and Lamb, D.C. (2012) Structural analysis of cytochrome P450 105N1 involved in the biosynthesis of the zincophore, coelibactin. Int J Mol Sci 13: 8500-8513.