Yersinia ironomics: Comparison of iron transporters among Yersinia pestis biotypes and its nearest neighbor, Yersinia pseudotuberculosis

BioMetals

Volumn 23, Issue 2, 2010, Pages 275-294

  Forman, Stanislav ^a,c   Paulley, James T ^a   Fetherston, Jacqueline D ^a   Cheng, Yi Qiang ^b   Perry, Robert D ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^c Zymo Research Corporation   (United States)

Author keywords

Heme transport; Iron transport; Plague; Siderophore; Yersinia pestis; Yersinia pseudotuberculosis; Yersiniabactin

Indexed keywords

ABC TRANSPORTER; AEROBACTIN; BACTERIAL PROTEIN; CARRIER PROTEIN; HEMIN; HMU ABC TRANSPORTER; IRON; PROTEIN EFEB; PROTEIN EFEO; PROTEIN EFEU; PROTEIN FEOA; PROTEIN FEOB; PROTEIN FEOC; PROTEIN FETM; PROTEIN FETP; PROTEIN FIEF; PROTEIN HASA; SIDEROPHORE; UNCLASSIFIED DRUG; YERSINIA NON RIBOSOMAL PEPTIDE; YERSINIABACTIN; MEMBRANE PROTEIN; TONB PROTEIN, BACTERIA;

ARTICLE; BACTERIAL GENOME; BACTERIAL VIRULENCE; BIOTYPE; GENE LOCUS; GENOME ANALYSIS; IRON TRANSPORT; NONHUMAN; OPEN READING FRAME; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PLAGUE;

YERSINIA; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; HEMIN; HUMANS; IRON; MEMBRANE PROTEINS; MOLECULAR STRUCTURE; PLAGUE; SIDEROPHORES; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

EID: 77952516373     PISSN: 09660844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10534-009-9286-4     Document Type: Article

References (89)

1. Achtman M, Morelli G, Zhu P, Wirth T, Diehl I, Kusecek B, Vogler AJ, Wagner DM, Allender CJ, Easterday WR, Chenal-Francisque V, Worsham P, Thomson NR, Parkhill J, Lindler LE, Carniel E, Keim P (2004) Microevolution and history of the plague bacillus, Yersinia pestis. PNAS 101:17837-17842
2. Anisimov AP, Lindler LE, Pier GB (2004) Intraspecific diversity of Yersinia pestis. Clin Microbiol Rev 17:434-464
3. Ansari MZ, Yadav G, Gokhale RS, Mohanty D (2004) NRPSPKS: a knowledge-based resource for analysis of NRPS/ PKS megasynthases. Nucleic Acids Res 32:W405-W413
4. Bearden SW, Perry RD (1999) The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol Microbiol 32:403-414
5. Bearden SW, Fetherston JD, Perry RD (1997) Genetic organization of the yersiniabactin biosynthetic region and construction of avirulent mutants in Yersinia pestis. Infect Immun 65:1659-1668
6. Bearden SW, Staggs TM, Perry RD (1998) An ABC transporter system of Yersinia pestis allows utilization of chelated iron by Escherichia coli SAB11. J Bacteriol 180:1135-1147
7. Beesley ED, Brubaker RR, Janssen WA, Surgalla MJ (1967) Pesticins. III. Expression of coagulase and mechanism of fibrinolysis. J Bacteriol 94:19-26
8. Bobrov AG, Geoffroy VA, Perry RD (2002) Yersiniabactin production requires the thioesterase domain of HMWP2 and YbtD, a putative phosphopantetheinylate transferase. Infect Immun 70:4204-4214
9. Brubaker RR (1969) Mutation rate to nonpigmentation in Pasteurella pestis. J Bacteriol 98:1404-1406
10. Brubaker RR (2004) The recent emergence of plague: a process of felonious evolution. Microb Ecol 47:293-299
11. Buchrieser C, Prentice M, Carniel E (1998) The 102-kilobase unstable region of Yersinia pestis comprises a high-pathogenicity island linked to a pigmentation segment which undergoes internal rearrangement. J Bacteriol 180:2321-2329
12. Burrows TW, Bacon GA (1960) V and W antigens in strains of Pasteurella pseudotuberculosis. Br J Exp Pathol 41:38-44
13. Byers BR, Arceneaux EL (1998) Microbial iron transport: iron acquisition by pathogenic microorganisms. In: Sigel A, Sigel H (eds) Metal ions in biological systems: iron transport and storage in microorganisms, plants, and animals. Marcell Dekker, Inc., New York, pp 37-66
14. Cao J, Woodhall MR, Alvarez J, Cartron ML, Andrews SC (2007) EfeUOB (YcdNOB) is a tripartite, acid-induced and CpxAR-regulated, low-pH Fe2? transporter that is cryptic in Escherichia coli K-12 but functional in E. coli O157:H7. Mol Microbiol 65:857-875
15. Carniel E, Guiyoule A, Guilvout I, Mercereau-Puijalon O(1992) Molecular cloning, iron-regulation and mutagenesis of the irp2 gene encoding HMWP2, a protein specific for the highly pathogenic Yersinia. Mol Microbiol 6:379-388
16. Cartron ML, Maddocks S, Gillingham P, Craven CJ, Andrews SC (2006) Feo-transport of ferrous iron into bacteria. Biometals 19:143-157
17. Cescau S, Cwerman H, Létoffé S, Delepelaire P, Wandersman C, Biville F (2007) Heme acquisition by hemophores. Biometals 20:603-613
18. Chain PSG, Carniel E, Larimer FW, Lamerdin J, Stoutland PO, Regala WM, Georgescu AM, Vergez LM, Land ML, Motin VL, Brubaker RR, Fowler J, Hinnebusch J, Marceau M, Medigue C, Simonet M, Chenal-Francisque V, Souza B, Dacheux D, Elliott JM, Derbise A, Hauser LJ, Garcia E (2004) Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. PNAS 101:13826-13831
19. Chain PSG, Hu P, Malfatti SA, Radnedge L, Larimer F, Vergez LM, Worsham P, Chu MC, Andersen GL (2006) Complete genome sequence of Yersinia pestis strains Antiqua and Nepal516: evidence of gene reduction in an emerging pathogen. J Bacteriol 188:4453-4463
20. Challis GL (2005) A widely distributed bacterial pathway for siderophore biosynthesis independent of nonribosomal peptide synthetases. ChemBioChem 6:601-611
21. Crosa JH, Walsh CT (2002) Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol Mol Biol Rev 66:223-249
22. Crosa JH, Mey AR, Payne SM (2004) Iron transport in bacteria. ASM Press, Washington
23. Deng W, Burland V, Plunkett G III, Boutin A, Mayhew GF, Liss P, Perna NT, Rose DJ, Mau B, Zhou S, Schwartz DC, Fetherston JD, Lindler LE, Brubaker RR, Plano GV, Straley SC, McDonough KA, Nilles ML, Matson JS, Blattner FR, Perry RD (2002) Genome sequence of Yersinia pestis KIM. J Bacteriol 184:4601-4611
24. Di Lorenzo M, Stork M, Alice AF, López CS, Crosa JH (2004) Vibrio. In: Crosa JH, Mey AR, Payne SM (eds) Iron transport in bacteria. ASM Press, Washington, pp 241-255
25. Dubbels BL, DiSpirito AA, Morton JD, Semrau JD, Neto JNE, Bazylinski DA (2004) Evidence for a copper-dependent iron transport system in the marine, magnetotactic bacterium strain MV-1. Microbiology 150:2931-2945
26. Fetherston JD, Perry RD (1994) The pigmentation locus of Yersinia pestis KIM6 ? is flanked by an ins Perry, et al. 1990rtion sequence and includes the structural genes for pesticin sensitivity andHMWP2.Mol Microbiol 13:697-708
27. Fetherston JD, Schuetze P, Perry RD (1992) Loss of the pigmentation phenotype in Yersinia pestis is due to the spontaneous deletion of 102 kb of chromosomal DNA which is flanked by a repetitive element. Mol Microbiol 6:2693-2704
28. Fetherston JD, Lillard JW Jr, Perry RD (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
29. Fetherston JD, Bertolino VJ, Perry RD (1999) YbtP and YbtQ: two ABC transporters required for iron uptake in Yersinia pestis. Mol Microbiol 32:289-299
30. Forman S, Nagiec MJ, Abney J, Perry RD, Fetherston JD (2007) Analysis of the aerobactin and ferric hydroxamate uptake systems of Yersinia pestis. Microbiology 153:2332-2341
31. Forman S, Wulff CR, Myers-Morales T, Cowan C, Perry RD, Straley SC (2008) yadBC of Yersinia pestis, a new virulence determinant for bubonic plague. Infect Immun 76:578-587
32. 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
33. Gong S, Bearden SW, Geoffroy VA, Fetherston JD, Perry RD (2001) Characterization of the Yersinia pestis Yfu ABC iron transport system. Infect Immun 67:2829-2837
34. Grass G, Otto M, Fricke B, Haney CJ, Rensing C, Nies DH, Munkelt D (2005) FieF (YiiP) from Escherichia coli mediates decreased cellular accumulation of iron and relieves iron stress. Archives Microbiol 183:9-18
35. Große C, Scherer J, Koch D, Otto M, Taudte N, Grass G (2006) A new ferrous iron-uptake transporter, EfeU (YcdN), from Escherichia coli. Mol Microbiol 62:120-131
36. Guerinot ML (1994) Microbial iron transport. Annu Rev Microbiol 48:743-772
37. Hantke K (2004) Ferrous iron transport. In: Crosa JH, Mey AR, Payne SM (eds) Iron Transport in Bacteria. ASM Press, Washington, pp 178-184
38. Hare JM, McDonough KA (1999) High-frequency RecAdependent and -independent mechanisms of Congo red binding mutations in Yersinia pestis. J Bacteriol 181:4896-4904
39. Higuchi K, Smith JL (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
40. Hinchliffe SJ, Isherwood KE, Stabler RA, Prentice MB, Rakin A, Nichols RA, Oyston PCF, Hinds J, Titball RW, Wren BW (2003) Application of DNA microarrays to study the evolutionary genomics of Yersinia pestis and Yersinia pseudotuberculosis. Genome Res 13:2018-2029
41. Hinnebusch BJ (2004) The evolution of flea-borne transmission of Yersinia pestis. In: Carniel E, Hinnebusch BJ (eds) Yersinia molecular and cellular biology. Horizon Bioscience, Norfolk, pp 49-73
42. Hornung JM, Jones HA, Perry RD (1996) The hmu locus of Yersinia pestis is essential for utilization of free haemin and haem-protein complexes as iron sources. Mol Microbiol 20:725-739
43. Hu P, Elliott J, McCready P, Skowronski E, Garnes J, Kobayashi A, Brubaker RR, Garcia E (1998) Structural organization of virulence-associated plasmids of Yersinia pestis. J Bacteriol 180:5192-5202
44. Karlyshev AV, Oyston PCF, Williams K, Clark GC, Titball RW, Winzeler EA, Wren BW (2001) Application of highdensity array-based signature-tagged mutagenesis to discover novel Yersinia virulence-associated genes. Infect Immun 69:7810-7819
45. Kirillina O, Bobrov AG, Fetherston JD, Perry RD (2006) A hierarchy of iron uptake systems: Yfu and Yiu are functional in Yersinia pestis. Infect Immun 74:6171-6178
46. Koch D, Nies DH, Grass G (2008) Characterization of a novel iron uptake system from uropathogenic Escherichia coli strain F11. In: BioMetals 2008 (6th Intl Biometals Symp), Santiago de Compostela, Spain, 14-18 July 2008, p 102
47. Lathem WW, Crosby SD, Miller VL, Goldman WE (2005) Progression of primary pneumonic plague: a mouse model of infection, pathology, and bacterial transcriptional activity. PNAS 102:17786-17791
48. Lesic B, Carniel E (2004) The high pathogenicity island: a broad-host-range pathogenicity island. In: Carniel E, Hinnebusch BJ (eds) Yersinia molecular and cellular biology. Horizon Bioscience, Norfolk, pp 285-306
49. Lindler LE, Plano GV, Burland V, Mayhew GF, Blattner FR (1998) Complete DNA sequence and detailed analysis of the Yersinia pestis KIM5 plasmid encoding murine toxin and capsular antigen. Infect Immun 66:5731-5742
50. Lorange EA, Race BL, Sebbane F, Hinnebusch JB (2005) Poor vector competence of fleas and the evolution of hypervirulence in Yersinia pestis. J Infect Dis 191:1907-1912
51. Lucier TS, Brubaker RR (1992) Determination of genome size, macrorestriction pattern polymorphism, and nonpigmentation- specific deletion in Yersinia pestis by pulsed-field gel electrophoresis. J Bacteriol 174:2078-2086
52. Mey AR, Wyckoff EE, Oglesby AG, Rab E, Taylor RK, Payne SM (2002) Identification of the Vibrio cholerae enterobactin receptors VctA and IrgA: IrgA is not required for virulence. Infect Immun 70:3419-3426
53. Mietzner TA, Morse SA (1994) The role of iron-binding proteins in the survival of pathogenic bacteria. Annu Rev Nutr 14:471-493
54. Miller MC, Parkin S, Fetherston JD, Perry RD, DeMoll E (2006) Crystal structure of ferric-yersiniabactin, a virulence factor of Yersinia pestis. J Inorg Biochm 100:1495-1500
55. Ollinger J, Song K-B, Antelmann H, Hecker M, Helmann JD (2006) Role of the Fur regulon in iron transport in Bacillus subtilis. J Bacteriol 188:3664-3673
56. Papp-Wallace KM, Maguire ME (2006) Manganese transport and the role of manganese in virulence. Annu Rev Microbiol 60:187-209
57. Parkhill J, Wren BW, Thomson NR, Titball RW, Holden MT, Prentice MB, Sebaihia M, James KD, Churcher C, Mungall KL, Baker S, Basham D, Bentley SD, Brooks K, Cerdeno-Tarraga AM, Chillingworth T, Cronin A, Davies RM, Davis P, Dougan G, Feltwell T, Hamlin N, Holroyd S, Jagels K, Karlyshev AV, Leather S, Moule S, Oyston PC, Quail M, Rutherford K, Simmonds M, Skelton J, Stevens K, Whitehead S, Barrell BG (2001) Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413:523-527
58. Payne SM, Mey AR (2004) Pathogenic Escherichia coli, Shigella. In: Crosa JH, Mey AR, Payne SM (eds) Iron transport in bacteria. ASM Press, Washington, pp 199-218
59. Pérez-Miranda S, Cabirol N, George-Téllez R, Zamudio-Rivera LS, Fernández FJ (2007) O-CAS, a fast and universal method for siderophore detection. J Microbiol Meth 70:127-131
60. Perkins-Balding D, Rasmussen A, Stojiljkovic I (2004) Bacterial heme and hemoprotein receptors. In: Crosa JH, Mey AR, Payne SM (eds) Iron transport in bacteria. ASM Press, Washington, pp 66-85
61. Perry RD (2004) Yersinia. In: Crosa JH, Mey AR, Payne SM (eds) Iron transport in bacteria. ASM Press, Washington, pp 219-240
62. + phenotype of Yersinia enterocolitica. Infect Immun 40:166-171
63. Perry RD, Fetherston JD (1997) Yersinia pestis-etiologic agent of plague. Clin Microbiol Rev 10:35-66
64. Perry RD, Fetherston JD (2004) Iron and heme uptake systems. In: Carniel E, Hinnebusch BJ (eds) Yersinia molecular and cellular biology. Horizon Bioscience, Norfolk, pp 257-283
65. Perry RD, Pendrak ML, Schuetze P (1990) Identification and cloning of a hemin storage locus involved in the pigmentation phenotype of Yersinia pestis. J Bacteriol 172:5929-5937
66. 2+-response plasmid pCD1 of Yersinia pestis KIM5. Infect Immun 66:4611-4623
67. Perry RD, Balbo PB, Jones HA, Fetherston JD, DeMoll E (1999) Yersiniabactin from Yersinia pestis: biochemical characterization of the siderophore and its role in iron transport and regulation. Microbiology 145:1181-1190
68. Perry RD, Abney J, Mier I Jr, Lee Y, Bearden SW, Fetherston JD (2003a) Regulation of the Yersinia pestis Yfe and Ybt iron transport systems. Adv Exp Med Biol 529:275-283
69. Perry RD, Shah J, Bearden SW, Thompson JM, Fetherston JD (2003b) Yersinia pestis TonB: role in iron, heme and hemoprotein utilization. Infect Immun 71:4159-4162
70. Perry RD, Bobrov AG, Kirillina O, Jones HA, Pedersen LL, Abney J, Fetherston JD (2004) Temperature regulation of the hemin storage (Hms?) phenotype of Yersinia pestis is posttranscriptional. J Bacteriol 186:1638-1647
71. Perry RD, Mier I Jr, Fetherston JD (2007) Roles of the Yfe and Feo transporters of Yersinia pestis in iron uptake and intracellular growth. Biometals 20:699-703
72. Reed LJ, Muench H (1938) A simple method for estimating fifty percent endpoints. Am J Hyg 27:493-497
73. Rossi M-S, Fetherston JD, Létoffé S, Carniel E, Perry RD, Ghigo J-M (2001) Identification and characterization of the hemophore-dependent heme acquisition system of Yersinia pestis. Infect Immun 69:6707-6717
74. Rossi M-S, Paquelin A, Ghigo JM, Wandersman C (2003) Haemophore-mediated signal transduction across the bacterial cell envelope in Serratia marcescens: the inducer and the transported substrate are different molecules. Mol Microbiol 48:1467-1489
75. Runyen-Janecky LJ, Reeves SA, Gonzales EG, Payne SM (2003) Contribution of the Shigella flexneri Sit, Iuc, and Feo iron acquisition systems to iron acquisition in vitro and in cultured cells. Infect Immun 71:1919-1928
76. Schaible UE, Kaufmann SHE (2004) Iron and microbial infection. Nat Rev Microbiol 2:946-953
77. Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47-56
78. Song Y, Tong Z, Wang J, Wang L, Guo Z, Han Y, Zhang J, Pei D, Zhou D, Qin H, Pang X, Han Y, Zhai J, Li M, Cui B, Qi Z, Jin L, Dai R, Chen F, Li S, Ye C, Du Z, Lin W, Wang J, Yu J, Yang H, Wang J, Huang P, Yang R (2004) Complete genome sequence of Yersinia pestis strain 91001, an isolate avirulent to humans. DNA Res 11:179-197
79. Straley SC, Starnbach MN (2000) Yersinia: strategies that thwart immune defenses. In: Cunningham MW, Fujinami RS (eds) Effects of microbes on the immune system. Lippincott Williams & Wilkins, Philadelphia, pp 71-92
80. Surgalla MJ, Beesley ED (1969) Congo red-agar plating medium for detecting pigmentation in Pasteurella pestis. Appl Microbiol 18:834-837
81. Thompson JM, Jones HA, Perry RD (1999) Molecular characterization of the hemin uptake locus (hmu) from Yersinia pestis and analysis of hmu mutants for hemin and hemoprotein utilization. Infect Immun 67:3879-3892
82. Thomson NR, Howard S, Wren BW, Holden MTG, Crossman L, Challis GL, Churcher C, Mungall K, Brooks K, Chillingworth T, Feltwell T, Abdellah Z, Hauser H, Jagels K, Maddison M, Moule S, Sanders M, Whitehead S, Quail MA, Dougan G, Parkhill J, Prentice MB (2006) The complete genome sequence and comparative genome analysis of the high pathogenicity Yersinia enterocolitica strain 8081. PLoS Genet 2:e206
83. Une T, Brubaker RR (1984) In vivo comparison of avirulent Vwa- and Pgm- or Pstr phenotypes of yersiniae. Infect Immun 43:895-900
84. Walsh CT, Marshall CG (2004) Siderophore biosynthesis in bacteria. In: Crosa JH, Mey AR, Payne SM (eds) Iron transport in bacteria. ASM Press, Washington, pp 18-37
85. Weinberg ED, Weinberg GA (1995) The role of iron in infection. Curr Opin Infect Dis 8:164-169
86. Wren BW (2003) The Yersiniae-a model genus to study the rapid evolution of bacterial pathogens. Nature Rev 1:55-64
87. Wyckoff EE, Schmitt M, Wilks A, Payne SM (2004) HutZ is required for efficient heme utilization in Vibrio cholerae. J Bacteriol 186:4142-4151
88. Zhou D, Han Y, Song Y, Huang P, Yang R (2004a) Comparative and evolutionary genomics of Yersinia pestis. Microbes Infect 6:1226-1234
89. Zhou D, Tong Z, Song Y, Han Y, Pei D, Pang X, Zhai J, Li M, Cui B, Qi Z, Jin L, Dai R, Du Z, Wang J, Guo Z, Wang J, Huang P, Yang R (2004b) Genetics of metabolic variations between Yersinia pestis biovars and the proposal of a new biovar, microtus. J Bacteriol 186:5147-5152