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Chapter 15 : Yersinia

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Yersinia, Page 1 of 2

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Abstract:

The genus is part of the family and consists of environmental species (, , , , , , and ), a primary fish pathogen (), two enteropathogenic species ( and ), and the plague bacillus (). The virulence properties of the human pathogenic species include iron acquisition systems. The genome encodes three potential siderophore biosynthesis systems, two of which are nonribosomal peptide synthetase (NRPS) systems. Only one of these has been demonstrated to produce a siderophore, yersiniabactin (Ybt). Genes through , which are required for non-NRPS-mediated synthesis of the hydroxamate siderophore aerobactin, are also present in the genome. The genome encodes a number of ABC transport systems with significant similarities to iron or siderophore transport systems. Since none of these systems is associated with genes encoding biosynthetic enzymes for siderophores and since the ligands for most of these systems have not been experimentally determined, they are included in the topic on siderophore-independent iron transport systems. Heme transport systems, including the Hmu/Hem heme uptake system, and the Has hemophore system, and iron regulation and storage are discussed in this chapter.

Citation: Perry R. 2004. Yersinia, p 219-240. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch15

Key Concept Ranking

Type I Secretion System
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Figures

Image of FIGURE 1
FIGURE 1

Genetic organization of the locus and the HPI pathogenicity island of . IS elements (black boxes) define the ends of the locus. Numbering of the locus within the HPI corresponds to nucleotide numbers for the start codons of , , , , , , and and for the stop codons of (start of locus), , , , and (end of the locus). The HPIs are extremely similar in the core region (tRNA to ), with two differences in the HPI: an ERIC (enterobacterial repetitive intergenic consensus) sequence in the promoter region and an inactive putative integrase gene. Genes of the locus encoding transport proteins (cross-hatched boxes), biosynthetic enzymes (boxes with diagonal lines), the regulatory protein YbtA (box with horizontal lines), and (unknown function [open box]) are shown with arrows indicating promoter regions and the direction of transcription. Each promoter has proven Fur and YbtA binding sites (not shown). Molecular masses of Ybt proteins are indicated in kilodaltons. The unprocessed and processed masses of Psn are shown. High-molecular-weight proteins 1 and 2 (HMWP1 and HMWP2) are encoded by and , respectively.

Citation: Perry R. 2004. Yersinia, p 219-240. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch15
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Image of FIGURE 2
FIGURE 2

Structure of yersiniabactin. Asterisks indicate the predicted ferric iron binding sites. Three cysteine residues are precursors for the thiazoline ring and the two thiazolidine rings, while the phenolate moiety is derived from salicylate.

Citation: Perry R. 2004. Yersinia, p 219-240. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch15
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Image of FIGURE 3
FIGURE 3

Model of the Ybt system. Dashed arrows designate predicted mechanisms, steps, or substrate transported that have not been experimentally demonstrated. It is uncertain whether a PBP is required for uptake, and none is shown in this model.

Citation: Perry R. 2004. Yersinia, p 219-240. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch15
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Image of FIGURE 4
FIGURE 4

Genetic organization of the locus of . Numbering indicates base pairs of a cloned DNA fragment. Arrows indicate the ORFs and direction of transcription. Putative biosynthetic enzymes are indicated by solid arrows, and putative transport functions are indicated by diagonally striped arrows. YsuF (cross-hatched arrow) shows similarity to FhuF, an Fe/ siderophore reductase in . YegH contains domains present in export proteins and is a homologue of YegH. is intact in CO92; in KIM10+, and are probably pseudogenes resulting from a frameshift mutation. Deduced protein molecular masses are given in kilodaltons; YsuR and YsuA have predicted signal sequences, and the numbers in parentheses are sizes after processing. SBE, siderophore-biosynthetic enzyme; IMP, inner membrane permease; ATPase, ATP hydrolase.

Citation: Perry R. 2004. Yersinia, p 219-240. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch15
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Image of FIGURE 5
FIGURE 5

Genetic organization of the locus of . Numbering in base pairs corresponds to the size of a cloned DNA fragment. Arrows indicate the ORFs and direction of transcription. Deduced protein molecular masses are given in kilodaltons. YfeA has a predicted signal sequence, and sizes indicated are for the unprocessed/processed forms. IMP, inner membrane permease; ATPase, ATP hydrolase.

Citation: Perry R. 2004. Yersinia, p 219-240. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch15
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Image of FIGURE 6
FIGURE 6

Model of the Yfe iron and manganese transport and regulatory system of . No OM component for the Yfe transport system has been identified. The YfeR receptor and porin are alternative speculative channels through the OM. The question mark indicates the uncertainty about Zn uptake by the Yfe system. Dashed arrows identify mechanisms or steps that have not been determined experimentally.

Citation: Perry R. 2004. Yersinia, p 219-240. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch15
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Image of FIGURE 7
FIGURE 7

Model of the Hmu/Hem hemoprotein transport and regulatory system. Only Hmu designations are used for clarity. Dashed arrows designate predicted functions or mechanisms that have not been fully demonstrated experimentally. Abbreviations: Hx, heme-hemopexin; Hb, hemoglobin; Hb-Hp, hemoglobin-haptoglobin; He, heme; He-alb, heme-albumin; Mb, myoglobin.

Citation: Perry R. 2004. Yersinia, p 219-240. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch15
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Image of FIGURE 8
FIGURE 8

Genetic organization of the ~6.9-kb locus of . Sizes of the Hmu proteins are shown in Table 5 . Predicted proteins Y0547 (437 residues; 49.2 kDa), Y0546 (181 residues; 20.2 kDa), and Y0545 (216 residues; 23.2 kDa) correspond to W, X, and Y proteins in other enteric hemoprotein ABC transport systems. The genetic organization of is identical. However, analysis of the promoter region and sequencing of the region upstream of has not been performed.

Citation: Perry R. 2004. Yersinia, p 219-240. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch15
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References

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1. Bäumler, A.,, R. Koebnik,, I. Stojiljkovic,, J. Heesemann,, V. Braun,, and K. Hantke. 1993. Survey on newly characterized iron uptake systems of Yersinia enterocolitica. Zentbl. Bakteriol. 278:416424.
2. Bearden, S. W.,, and R. D. Perry. 1999. The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol. Microbiol. 32:403414.
3. Bobrov, A. G.,, V. A. Geoffroy,, and R. D. Perry. 2002. Yersiniabactin production requires the thioesterase domain of HMWP2 and YbtD, a putative phosphopantetheinylate transferase. Infect. Immun. 70:42044214.
4. Brem, D.,, C. Pelludat,, A. Rakin,, C. A. Jacobi,, and J. Heesemann. 2001. Functional analysis of yersiniabactin transport genes of Yersinia enterocolitica. Microbiology 147:11151127.
5. Carniel, E. 2001. The Yersinia high-pathogenicity island: an iron-uptake island. Microbes Infect. 3:561569.
6. Carniel, E.,, A. Guiyoule,, I. Guilvout,, and O. Mercereau-Puijalon. 1992. Molecular cloning, iron-regulation and mutagenesis of the irp2 gene encoding HMWP2, a protein specific for the highly pathogenic Yersinia. Mol. Microbiol. 6:379388.
7. Fetherston, J. D.,, V. J. Bertolino,, and R. D. Perry. 1999. YbtP and YbtQ: two ABC transporters required for iron uptake in Yersinia pestis. Mol. Microbiol. 32:289299.
8. Gong, S.,, S. W. Bearden,, V. A. Geoffroy,, J. D. Fetherston,, and R. D. Perry. 2001. Characterization of the Yersinia pestis Yfu ABC iron transport system. Infect. Immun. 67:28292837.
9. Jacobi, C. A.,, S. Gregor,, A. Rakin,, and J. Heesemann. 2001. Expression analysis of the yersiniabactin receptor gene fyuA and the heme receptor hemR of Yersinia enterocolitica in vitro and in vivo using the reporter genes for green fluorescent protein and luciferase. Infect. Immun. 69:77727782.
10. Koebnik, R.,, K. Hantke,, and V. Braun. 1993. The TonB-dependent ferrichrome receptor FcuA of Yersinia enterocolitica: evidence against a strict coevolution of receptor structure and substrate specificity. Mol. Microbiol. 7:383393.
11. Perry, R. D.,, J. Abney,, I. Mier, Jr.,, Y. Lee,, S. W. Bearden,, and J. D. Fetherston,. 2003. Regulation of the Yersinia pestis Yfe and Ybt iron transport systems, p. 275283. In M. Skurnik,, K. Granfors,, and J. A. Bengoechea (ed.), The Genus Yersinia: Enteringthe Functional Genomic Era. Kluwer Academic/ Plenum Publishers, New York, N.Y.
12. Perry, R. D.,, S. W. Bearden,, and J. D. Fetherston. 2001. Iron and heme acquisition and storage systems of Yersinia pestis. Recent Res. Dev. Microbiol. 5:1327.
13. Rakin, A.,, E. Saken,, D. Harmsen,, and J. Heesemann. 1994. The pesticin receptor of Yersinia enterocolitica: a novel virulence factor with dual function. Mol. Microbiol. 13:253263.
14. Rossi, M.-S.,, J. D. Fetherston,, S. Létoffé,, E. Carniel,, R. D. Perry,, and J.-M. Ghigo. 2001. Identi fication and characterization of the hemophore-dependent heme acquisition system of Yersinia pestis. Infect. Immun. 69:67076717.
15. Saken, E.,, A. Rakin,, and J. Heesemann. 2000. Molecular characterization of a novel siderophore-independent iron transport system in Yersinia. Int. J. Med. Microbiol. 290:5160.
16. Schubert, S.,, D. Fischer,, and J. Heesemann. 1999. Ferric enterochelin transport in Yersinia enterocolitica: molecular and evolutionary aspects. J. Bacteriol. 181:63876395.
17. Stojiljkovic, I.,, and D. Perkins-Balding. 2002. Processing of heme and heme-containing proteins by bacteria. DNA Cell Biol. 21:281295.
18. Straley, S. C.,, and M. N. Starnbach,. 2000. Yersinia: strategies that thwart immune defenses, p. 7192. In M. W. Cunningham, and R. S. Fujinami (ed.), Effects of Microbes on the Immune System. Lippincott Williams & Wilkins, Philadelphia, Pa.
19. Stuart, S. J.,, J. K. Prpic,, and R. M. Robins- Browne. 1986. Production of aerobactin by some species of the genus Yersinia. J. Bacteriol. 166:11311133.
20. Thompson, J. M.,, H. A. Jones,, and R. D. Perry. 1999. Molecular characterization of the hemin uptake locus (hmu) from Yersinia pestis and analysis of hmu mutants for hemin and hemoprotein utilization. Infect. Immun. 67:38793892.

Tables

Generic image for table
TABLE 1

Effects of iron and hemoprotein transport systems on the pathogenesis of Yersinia

Citation: Perry R. 2004. Yersinia, p 219-240. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch15
Generic image for table
TABLE 2

Expression of a promoter gene fusion in derivatives grown in Fe-deficient medium

Citation: Perry R. 2004. Yersinia, p 219-240. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch15
Generic image for table
TABLE 3

Components of the Fhu, enterobactin, and Ynp systems

Citation: Perry R. 2004. Yersinia, p 219-240. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch15
Generic image for table
TABLE 4

Components of selected siderophore-independent iron transport systems

Citation: Perry R. 2004. Yersinia, p 219-240. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch15
Generic image for table
TABLE 5

Components of the Hmu/Hem and Has systems

Citation: Perry R. 2004. Yersinia, p 219-240. In Crosa J, Mey A, Payne S, Iron Transport in Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816544.ch15

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