YAPI, a New Yersinia pseudotuberculosis Pathogenicity Island

Abstract

Pathogenicity islands (PAIs) are chromosomal clusters of pathogen-specific virulence genes often found at tRNA loci. In the Yersinia pseudotuberculosis 32777 chromosome, we characterized a 98-kb segment that has all of the characteristic features of a PAI, including insertion in a (phenylalanine) tRNA gene, the presence of a bacteriophage-like integrase-encoding gene, and direct repeats at the integration sites. The G؉C content of the segment ranges from 31 to 60%, reflecting a genetic mosaic: this is consistent with the notion that the sequences were horizontally acquired. The PAI, termed YAPI (for Yersinia adhesion pathogenicity island), carries 95 open reading frames and includes (i) the previously described pil operon, encoding a type IV pilus that contributes to pathogenicity (F. Collyn et al., Infect. Immun. 70:6196-6205, 2002); (ii) a block of genes potentially involved in general metabolism; (iii) a gene cluster for a restriction-modification system; and (iv) a large number of mobile genetic elements. Furthermore, the PAI can excise itself from the chromosome at low frequency and in a precise manner, and deletion does not result in a significant decrease of bacterial virulence compared to inactivation of the fimbrial gene cluster alone. The prevalence and size of the PAI vary from one Y. pseudotuberculosis strain to another, and it can be found integrated into either of the two phe tRNA loci present on the species' chromosome. YAPI was not detected in the genome of the genetically closely related species Y. pestis, whereas a homologous PAI is harbored by the Y. enterocolitica chromosome.Pathogenicity islands (PAIs) are DNA segments of 10 to 200 kb which are present in the genome of pathogenic strains but absent from those of nonpathogenic members of the same (or related) bacterial species and typically carry genes encoding one or more virulence factors. Since their discovery in pathogenic strains of Escherichia coli during the late 1980s (11), PAIs have been described in many other gram-negative (mostly Enterobacteriaceae) bacteria, as well as in certain gram-positive species (23). These genetic elements have common features: they are often DNA regions which (i) have a GϩC content and codon usage that differ from that of the rest of the genome; (ii) are flanked by small, direct-repeat sequences; (iii) are associated with tRNA genes; (iv) harbor cryptic or functional genes that encode mobility factors such as integrases, transposases, and insertion sequence (IS) elements or parts of these elements; and (v) are unstable (8). To date, only one chromosomal PAI (called the high-pathogenicity island [HPI]) has been well characterized in the three pathogenic Yersinia species: Yersinia pestis (the causative agent of plague) and Yersinia pseudotuberculosis and Yersinia enterocolitica (both responsible for digestive tract infections) (24). The HPI ranges from 36 to 43 kb (according to the species in question) and bears genes involved in the biosynthesis, transport, and regulation of the yersiniabactin siderophore ...

Structure, Diversity, and Mobility of the Salmonella Pathogenicity Island 7 Family of Integrative and Conjugative Elements within Enterobacteriaceae

“…Several elements representing a broader family of SPI-7-related elements have been previously reported in other enterobacterial genomes (11,31,48), including HAI2 (Erwinia carotovora strain SCRI1043) (3), ICEEc2 (avian pathogenic Escherichia coli [APEC] strain BEN374) (60), a region within Photorhabdus luminescens strain TT01 (spanning genes plu1030 to plu1166) (16), YAPI ye (Yersinia enterocolitica strain 8081) (66), and YAPI yptb (Yersinia pseudotuberculosis strain IP32777) (10). We aimed to identify further elements within the wider family of SPI-7-related ICEs.…”

Evolutionary Dynamics of the Yersinia enterocolitica Complex

“…It is thought that YAPI might have derived from the Salmonella Typhi island SPI-7 due to extensive homology and is also found in other Enterobacteriaceae, such as Photorhabdus luminescens (Collyn, et al, 2004;Thomson, et al, 2006;Eppinger, et al, 2007 (Carniel, Guilvout and Prentice, 1996;Carniel, 2002). In Y. enterocolitica, it is only present in the highpathogenic BT 1B.…”

“…The variable part of YAPI in Y. pseudotuberculosis contains metabolic genes, a restriction-modification system, IS elements and phage genes, which do not appear to contribute to pathogenicity (Collyn, et al, 2004). In Y. enterocolitica, the island is smaller than in Y. pseudotuberculosis, and apart from the shared pilin cluster encodes for a possible hemolysin, toxin/antitoxin system, and an arsenic resistance operon (Thomson, et al, 2006).…”

“…The conserved part of YAPI encodes a polycistronic pilin cluster that is involved in adhesion of bacteria to the respiratory epithelium in a mouse infection model (Collyn, et al, 2004;Eppinger, et al, 2007). The variable part of YAPI in Y. pseudotuberculosis contains metabolic genes, a restriction-modification system, IS elements and phage genes, which do not appear to contribute to pathogenicity (Collyn, et al, 2004).…”

Linkage of the Horizontally AcquiredypmandpilGenes inYersinia pseudotuberculosis

“…We recently reported the presence in Y. pseudotuberculosis of an 11-kb, 11-gene pil locus (pilLMNOPQRSUVW) that encodes a type IV pilus (7). It is located in the 5Ј part of a large (98-kb) pathogenicity island (PAI) called YAPI (6). Like ypm, the pil gene cluster is not present in all Y. pseudotuberculosis strains (7).…”