Three pathogenicity islands of Vibrio cholerae can excise from the chromosome and form circular intermediates

被引:82
作者
Murphy, Ronan A. [2 ]
Boyd, E. Fidelma [1 ]
机构
[1] Univ Delaware, Dept Biol Sci, Newark, DE 19716 USA
[2] Natl Univ Ireland Univ Coll Cork, Dept Microbiol, Cork, Ireland
关键词
D O I
10.1128/JB.00562-07
中图分类号
Q93 [微生物学];
学科分类号
071005 ; 100705 ;
摘要
Vbrio pathogenicity island-2 (VPI-2) is a 57-kb region integrated at a transfer RNA (tRNA)-serine locus that encompasses VC1758 to VC1809 on the V. cholerae N16961 genome and is present in pandemic isolates. VPI-2 encodes a P4-like integrase, a restriction modification system, a Mu phage-like region, and a sialic acid metabolism region, as well as neuraminidase (VC1784), which is a glycosylhydrolase known to release sialic acid from sialoglycoconjugates to unmask GM1 gangliosides, the receptor for cholera toxin. We examined the tRNA-serine locus among the sequenced V. cholerae genomes and identified five variant VPI-2 regions, four of which retained the sialometabolism region. Three variant VPI-2 regions contained a type three secretion system. By using an inverse nested PCR approach, we found that the VPI-2 region can form an extrachromosomal circular intermediate (CI) molecule after precise excision from its tRNA-serine attachment site. We constructed a knockout mutant of VC1758 (int) with V. cholerae strain N16961 and found that no excision PCR product was produced, indicating that a functional cognate, VPI-2 integrase, is required for excision. The Vibrio seventh pandemic island-I (VSP-I) and VSP-II regions are present in V. cholerae 01 El Tor and 0139 serogroup isolates. Novel regions are present at the VSP-I insertion site in strain MZO-3 and at the VSP-II insertion site in strain 623-39. VSP-II is a 27-kb region that integrates at a tRNA-methionine locus, is flanked by direct repeats, and encodes a P4-like integrase. We show that VSP-II can excise and form a CI and that the cognate VSP-II integrase is required for excision. Interestingly, VSP-I is not inserted at a tRNA locus and does encode a XerDC-like recombinase, but similar to VPI-2 and VSP-II, VSP-I does excise from the genome to form a CI. These results show that all three pathogenicity islands can excise from the chromosome, which is likely a first step in their horizontal transfer.
引用
收藏
页码:636 / 647
页数:12
相关论文
共 37 条
  • [1] GENESIS OF THE NOVEL EPIDEMIC VIBRIO-CHOLERAE-0139 STRAIN - EVIDENCE FOR HORIZONTAL TRANSFER OF GENES INVOLVED IN POLYSACCHARIDE SYNTHESIS
    BIK, EM
    BUNSCHOTEN, AE
    GOUW, RD
    MOOI, FR
    [J]. EMBO JOURNAL, 1995, 14 (02) : 209 - 216
  • [2] DNA fingerprinting of Vibrio cholerae strains with a novel insertion sequence element: A tool to identify epidemic strains
    Bik, EM
    Gouw, RD
    Mooi, FR
    [J]. JOURNAL OF CLINICAL MICROBIOLOGY, 1996, 34 (06) : 1453 - 1461
  • [3] The genome of non-O1 Vibrio cholerae NRT36S demonstrates the presence of pathogenic mechanisms that are distinct from those of O1 Vibrio cholerae
    Chen, Yuansha
    Johnson, Judith A.
    Pusch, Gordon D.
    Morris, J. Glenn, Jr.
    Stine, O. Colin
    [J]. INFECTION AND IMMUNITY, 2007, 75 (05) : 2645 - 2647
  • [4] Comparative genomic analysis of Vibrio cholerae:: Genes that correlate with cholera endemic and pandemic disease
    Dziejman, M
    Balon, E
    Boyd, D
    Fraser, CM
    Heidelberg, JF
    Mekalanos, JJ
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2002, 99 (03) : 1556 - 1561
  • [5] Examination of diverse toxin-coregulated pilus-positive Vibrio cholerae strains fails to demonstrate evidence for Vibrio pathogenicity island phage
    Faruque, SM
    Zhu, J
    Asadulghani
    Kamruzzaman, M
    Mekalanos, JJ
    [J]. INFECTION AND IMMUNITY, 2003, 71 (06) : 2993 - 2999
  • [6] ROLE OF VIBRIO-CHOLERAE NEURAMINIDASE IN THE FUNCTION OF CHOLERA-TOXIN
    GALEN, JE
    KETLEY, JM
    FASANO, A
    RICHARDSON, SH
    WASSERMAN, SS
    KAPER, JB
    [J]. INFECTION AND IMMUNITY, 1992, 60 (02) : 406 - 415
  • [7] Pathogenicity islands and the evolution of microbes
    Hacker, J
    Kaper, JB
    [J]. ANNUAL REVIEW OF MICROBIOLOGY, 2000, 54 : 641 - 679
  • [8] Ecological fitness, genomic islands and bacterial pathogenicity - A Darwinian view of the evolution of microbes
    Hacker, J
    Carniel, E
    [J]. EMBO REPORTS, 2001, 2 (05) : 376 - 381
  • [9] Pathogenicity islands of virulent bacteria: Structure, function and impact on microbial evolution
    Hacker, J
    BlumOehler, G
    Muhldorfer, I
    Tschape, H
    [J]. MOLECULAR MICROBIOLOGY, 1997, 23 (06) : 1089 - 1097
  • [10] DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae
    Heidelberg, JF
    Eisen, JA
    Nelson, WC
    Clayton, RA
    Gwinn, ML
    Dodson, RJ
    Haft, DH
    Hickey, EK
    Peterson, JD
    Umayam, L
    Gill, SR
    Nelson, KE
    Read, TD
    Tettelin, H
    Richardson, D
    Ermolaeva, MD
    Vamathevan, J
    Bass, S
    Qin, HY
    Dragoi, I
    Sellers, P
    McDonald, L
    Utterback, T
    Fleishmann, RD
    Nierman, WC
    White, O
    Salzberg, SL
    Smith, HO
    Colwell, RR
    Mekalanos, JJ
    Venter, JC
    Fraser, CM
    [J]. NATURE, 2000, 406 (6795) : 477 - 483