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Chapter 6 : The 70-Kilobase Virulence Plasmid of Yersiniae

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Abstract:

This chapter describes the 70-kb plasmid encoding the Yop virulon. It first describes the virulon, followed by a description of the organization of the pYVe227 plasmid of W227. It finally compares this plasmid to pCD1 and pIB1. SycD (called LcrH in and ) is a bivalent chaperone serving both YopB and YopD. In the absence of SycD, the YopD and YopB are less detectable inside the bacterial cell. SycD appears to be somewhat different from SycE and SycH in that it binds to several domains on YopB. LcrQ/YscM is thought to be a regulator, and YopN is considered an element of the plug closing down the channel. Altogether, the genes encoding the Yop virulon occupy about two-thirds of the plasmid, with only two IS elements interspersed among the yop and syc genes. The other one-third of the plasmid, localized between the replication origin and the partition site, which underwent some genetic rearrangements during evolution, contains only three genes that are or could be involved in pathogenicity: and two newly identified genes, and . The proteins required for translocation of the effectors across the eukaryotic cell membrane, YopB, YopD, their chaperone SycD, LcrV, and LcrG, are all encoded by the same operon, which is located next to and transcribed in the same orientation. The genes that are still conserved, such as , homologous to and , could have evolved to fulfill another, still unknown function.

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6

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Gene Expression and Regulation
0.45114616
Tumor Necrosis Factor alpha
0.44778222
Outer Membrane Protein A
0.42377868
Type III Secretion System
0.42377868
Outer Membrane Protein A
0.42377868
0.45114616
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Figures

Image of Figure 1
Figure 1

The basic model. When Yersinia organisms are placed at 37°C in a rich environment, the Ysc secretion apparatus is activated and a stock of Yop proteins is synthesized. As long as there is no contact with a eukaryotic cell, a stop valve, possibly made of YopN, TyeA, and LcrG, blocks the Ysc secretion channel. Upon contact with the eukaryotic target cell, a sensor interacts with a receptor on the cell surface, resulting in the opening of the secretion channel at the zone of contact. The Yops are then transported through the secretion channels, and the Yop effectors are translocated across the plasma membrane, guided by YopB and YopD. During their intrabacterial stage, Yops are capped with their specific chaperone, presumably to prevent premature associations. Reprinted from reference 38 with permission of the publisher.

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Image of Figure 2
Figure 2

Similarity between the flagellum and the hypothetical Yersinia secretion translocation machinery. (A) Flagellum (left) and hypothetical Ysc secretion machinery (right). (B) Similarities between the Ysc secretion machinery and the proteins involved in the assembly of the flagellum ( ).

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Image of Figure 3
Figure 3

Detailed genetic map of the pYVe227 plasmid of Y. enterocolitica W22703 ( ). The genes are colored according to the part of the apparatus they encode. Genes in green encode the Ysc secretion machinery and its control, genes in light blue encode the translocation machinery, genes in dark blue encode the effector Yops and their chaperones, genes in orange are involved in regulation of gene expression, the gene in khaki encodes an adhesin, and genes in mustard encode arsenic resistance proteins.

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Image of Figure 4
Figure 4

Partition site of the pYVe227 plasmid. Comparison between the sequence of the two direct repeats forming the spyC site of the pYVe227 plasmid and the consensus sequence derived from the 12 direct repeats of the sopC site of the E. coli F plasmid. The internal inverted repeats present in the central part of the direct repeats are indicated by two arrows and labeled I.R.

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Image of Figure 5
Figure 5

Amino acid sequence alignment of YomA from pYVe227 ( ) and PagO from 5. typhimurium ( ).

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Figure 6

Remains of a transfer operon. (A) Schematic representation of the region in pYVe227. The upper part of the panel represents the tral and traX region of the F plasmid. The lower panel indicates the region between coordinates 63.4 and 69.4. Solid boxes indicate insertion-like elements. The putative ORFs are shown by arrows. (B) Amino acid sequence alignment of the partial Tral protein encoded by the pYVe227 plamid and the corresponding part of Tral from the F plasmid. The conserved ATP- and GTP-binding domains are underlined. (C) Amino acid sequence alignment of the partial TraX protein encoded by the pYVe227 plamid and the corresponding part of TraX from F. The lipid attachment motif is underlined. (D) Amino acid sequence alignment of the Nuc endonucle-ase encoded by pYVe227 and Nuc encoded by pKMlOl of S. typhimurium (Nuc S.).

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Image of Figure 9
Figure 9

Comparison of the region encoding YopM in pCDl (K pestis) and pYVe227 (y. enterocolitica). The region situated upstream and downstream from yopM contains repeated sequences (represented by open arrow labeled R) that led to genetic rearrangement. The gene is oriented in the same direction as yopD in Y. pestis and Y. pseudotuberculosis (not shown) and in the opposite direction in Y. enterocolitica. The distance between the stop codon of sycT and the start codon of yopM is 3.4 kb in Y. enterocolitica. while the distance between the stop codon of yopM and the stop codon of sycT is 2.3 kb in Y. pestis. Putative ORFs identified upstream and downstream of yopM in the different species are shown by thin arrows labeled ORF followed by a number corresponding to the putative calculated molecular weight. The products of these ORFs have no match in the databases. The stippled areas indicate conserved regions between the downstream and upstream regions of yopM.

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Figure 7

Amino acid sequence alignment of the ORF80 product from pYVe227 ( ) and the product of an ORF of 83 codons identified in the genome of Mycobacterium tuberculosis ( ).

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Image of Figure 8
Figure 8

Genetic maps of pYVe227 from Y. enterocolitica W227 (serotype 0:9) (redrawn from reference ), pIB 1 from Y. pseudotuberculosis YPin (redrawn from reference ), and pCDl from Y. pestis KIM (redrawn from references and ). None of these maps is complete. For pCDl, the plasmid has been sequenced twice ( ) and only the genes that are identified in the two sequences or in one sequence and in Y. enterocolitica are shown. Plasmid pYVe227 has also been completely sequenced ( ) ( Fig. 3 ). The genes are shaded on the basis of the data presented in this chapter. The genes encoding the partition system are called soph and sopB in pCDl of Y. pestis ( ). yopQ, yopO, and yopP are yopK, ypkA and yopJ, respectively, in Y. pseudotuberculosis and Y. pestis. Reprinted from reference 39 with permission of the publisher.

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Figure 10

Amino acid sequence alignment of YadA from Y. enterocolitica O:9 (YadA09) ( ), Y. enterocolitica O:3 (YadA03), Y. enterocolitica 0:8 (YadA08), and Y. pseudotuberculosis (YadAPS). The three last sequences are from reference 168. The boxes and the bold letters indicate the different domains of the protein. (A) Signal sequence. (B) Residues required for adhesion to polymorphonuclear leukocytes and inhibition of the oxidative burst in Y. enterocolitica O:8. (C) Residues required for autoagglutination, collagen binding, and persistence in Peyer's patches of Y. enterocolitica O:3 and O:8. (D) Histidines 156 and 159 in Y. enterocolitica O:8, required for binding to different substrates and dissemination from Peyer's patches. (E) Residues required for anchoring to the outer membrane and polymer formation ( ).

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Tables

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Table 1

Yop effectors

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Table 2

Syc cytosolic chaperones

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Table 3

Secretion apparatus

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Table 4

Proteins required for translocation of Yop effectors

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
Generic image for table
Table 5

Proteins involved in control of Yop release

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Table 6

Promoters identified in pYVe227

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Table 7

Terminators identified in pYVe227

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Table 8

Functional and phenotypic classification of the predicted proteins encoded by pYVe227

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Table 10

Elements present in Y. enterocolitica pYVe227

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6
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Table 9

Putative ORFs of unknown function present in pYVe227

Citation: Iriarte M, Cornells G. 1999. The 70-Kilobase Virulence Plasmid of Yersiniae, p 91-126. In Kaper J, Hacker J (ed), Pathogenicity Islands and Other Mobile Virulence Elements. ASM Press, Washington, DC. doi: 10.1128/9781555818173.ch6

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