Pathogenicity Island Cross Talk Mediated by Recombination Directionality Factors Facilitates Excision from the Chromosome

Carpenter, Megan R.; Rozovsky, Sharon; Boyd, E. Fidelma

doi:10.1128/jb.00704-15

Cited by 22 publications

(39 citation statements)

References 59 publications

(109 reference statements)

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“…The RDFs were shown to be essential for VPI-2 excision and could induce VPI-1 excision. The cognate TR integrases for both VPI-1 and VPI-2 were shown to be essential for efficient excision of these islands from the bacterial chromosome (13). Various combinations of the components (integrases, RDFs, and att sites) of the VPI-1 and VPI-2 recombination modules were found in additional strains of V. cholerae and other Vibrio species, but they contained diverse cargo genes (11,(13)(14)(15)(16).…”

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confidence: 99%

“…IntV1 and IntV2 share less than 50% amino acid identity and can catalyze both integrative and excisive recombination. VPI-2 contains two excisionases (also known as recombination directionality factors [RDFs]), VefA and VefB, while VPI-1 contains none (13). The RDFs were shown to be essential for VPI-2 excision and could induce VPI-1 excision.…”

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confidence: 99%

“…Both VPI-1 and VPI-2 were shown to excise as complete units from the bacterial chromosome (10)(11)(12)(13). The mechanisms of excision for both islands have recently been determined (13).…”

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confidence: 99%

“…The cognate TR integrases for both VPI-1 and VPI-2 were shown to be essential for efficient excision of these islands from the bacterial chromosome (13). Various combinations of the components (integrases, RDFs, and att sites) of the VPI-1 and VPI-2 recombination modules were found in additional strains of V. cholerae and other Vibrio species, but they contained diverse cargo genes (11,(13)(14)(15)(16). Of particular note were two island regions, one that contained a clustered regularly interspaced short palindromic repeat (CRISPR) and CRISPR-associated protein (Cas protein) system and a type VI secretion system (T6SS) gene cluster and a second island that carried genes encoding a type III secretion system (T3SS).…”

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confidence: 99%

“…The mechanisms of excision for both islands have recently been determined (13). The recombination modules of VPI-1 and VPI-2 consist of a cognate integrase from the tyrosine recombinase (TR) family, IntV1 (VC0847) and IntV2 (VC1758), respectively, and each island contains flanking attL and attR attachment sites marking the site of chromosomal integration.…”

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confidence: 99%

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CRISPR-Cas and Contact-Dependent Secretion Systems Present on Excisable Pathogenicity Islands with Conserved Recombination Modules

et al. 2017

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Pathogenicity islands (PAIs) are mobile integrated genetic elements that contain a diverse range of virulence factors. PAIs integrate into the host chromosome at a tRNA locus that contains their specific bacterial attachment site, attB, via integrase-mediated site-specific recombination generating attL and attR sites. We identified conserved recombination modules (integrases and att sites) previously described in choleragenic Vibrio cholerae PAIs but with novel cargo genes. Clustered regularly interspaced short palindromic repeat (CRISPR)-associated proteins (Cas proteins) and a type VI secretion system (T6SS) gene cluster were identified at the Vibrio pathogenicity island 1 (VPI-1) insertion site in 19 V. cholerae strains and contained the same recombination module. Two divergent type I-F CRISPR-Cas systems were identified, which differed in Cas protein homology and content. The CRISPR repeat sequence was identical among all V. cholerae strains, but the CRISPR spacer sequences and the number of spacers varied. In silico analysis suggests that the CRISPR-Cas systems were active against phages and plasmids. A type III secretion system (T3SS) was present in 12 V. cholerae strains on a 68-kb island inserted at the same tRNA-serine insertion site as VPI-2 and contained the same recombination module. Bioinformatics analysis showed that two divergent T3SSs exist among the strains examined. Both the CRISPR and T3SS islands excised site specifically from the bacterial chromosome as complete units, and the cognate integrases were essential for this excision. These data demonstrated that identical recombination modules that catalyze integration and excision from the chromosome can acquire diverse cargo genes, signifying a novel method of acquisition for both CRISPR-Cas systems and T3SSs. IMPORTANCE This work demonstrated the presence of CRISPR-Cas systems and T3SSs on PAIs. Our work showed that similar recombination modules can associate with different cargo genes and catalyze their incorporation into bacterial chromosomes, which could convert a strain into a pathogen with very different disease pathologies. Each island had the ability to excise from the chromosome as distinct, complete units for possible transfer. Evolutionary analysis of these regions indicates that they were acquired by horizontal transfer and that PAIs are the units of transfer. Similar to the case for phage evolution, PAIs have a modular structure where different functional regions are acquired by identical recombination modules.KEYWORDS CRISPR-Cas, type III secretion, Vibrio cholerae, pathogenicity islands V ibrio cholerae is the causative agent of the severe diarrheal disease cholera. The factors necessary for manifestation of this disease were acquired by horizontal gene transfer. The cholera toxin (CT), a potent enterotoxin whose effects are respon-

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confidence: 99%

mentioning

confidence: 99%

“…Both VPI-1 and VPI-2 were shown to excise as complete units from the bacterial chromosome (10)(11)(12)(13). The mechanisms of excision for both islands have recently been determined (13).…”

mentioning

confidence: 99%