Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 24 April 1998:
Vol. 280. no. 5363, pp. 605 - 608
DOI: 10.1126/science.280.5363.605
Prev | Table of Contents

Reports

A Distinctive Class of Integron in the Vibrio cholerae Genome

Didier Mazel, * Broderick Dychinco, Vera A. Webb, Julian Davies dagger

The ability of bacteria to acquire and disseminate heterologous genes has been a major factor in the development of multiple drug resistance. A gene, intI4, was identified that encodes a previously unknown integrase that is associated with a "gene-VCR" organization (VCRs are Vibrio cholerae repeated sequences), similar to that of the well-characterized antibiotic resistance integrons. The similarity was confirmed by IntI1-mediated recombination of a gene-VCR cassette into a class 1 integron. VCR cassettes are found in a number of Vibrio species including a strain of V. metschnikovii isolated in 1888, suggesting that this mechanism of heterologous gene acquisition predated the antibiotic era.

Department of Microbiology and Immunology, University of British Columbia, 6174 University Boulevard, Vancouver, B.C., V6T 1Z3, Canada.
*   Present address: Institut Pasteur, 25-28 rue du Dr. Roux, 75724 Paris Cedex 15, France.

dagger    To whom correspondence should be addressed.

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
First Gene Cassettes of Integrons as Targets in Finding Adaptive Genes in Metagenomes.
L. Huang, C. Cagnon, P. Caumette, and R. Duran (2009)
Appl. Envir. Microbiol. 75, 3823-3825
   Abstract »    Full Text »    PDF »
Analysis by Mutagenesis of a Chromosomal Integron Integrase from Shewanella amazonensis SB2BT.
A. Larouche and P. H. Roy (2009)
J. Bacteriol. 191, 1933-1940
   Abstract »    Full Text »    PDF »
The Evolution of Class 1 Integrons and the Rise of Antibiotic Resistance.
M. Gillings, Y. Boucher, M. Labbate, A. Holmes, S. Krishnan, M. Holley, and H. W. Stokes (2008)
J. Bacteriol. 190, 5095-5100
   Abstract »    Full Text »    PDF »
Three Pathogenicity Islands of Vibrio cholerae Can Excise from the Chromosome and Form Circular Intermediates.
R. A. Murphy and E. F. Boyd (2008)
J. Bacteriol. 190, 636-647
   Abstract »    Full Text »    PDF »
Identification of key structural determinants of the IntI1 integron integrase that influence attC x attI1 recombination efficiency.
G. Demarre, C. Frumerie, D. N. Gopaul, and D. Mazel (2007)
Nucleic Acids Res. 35, 6475-6489
   Abstract »    Full Text »    PDF »
Molecular Characterization of Class 3 Integrons from Delftia spp..
H. Xu, J. Davies, and V. Miao (2007)
J. Bacteriol. 189, 6276-6283
   Abstract »    Full Text »    PDF »
Detection and Transformation of Genome Segments That Differ within a Coastal Population of Vibrio cholerae Strains.
M. C. Miller, D. P. Keymer, A. Avelar, A. B. Boehm, and G. K. Schoolnik (2007)
Appl. Envir. Microbiol. 73, 3695-3704
   Abstract »    Full Text »    PDF »
Use of chromosomal integron arrays as a phylogenetic typing system for Vibrio cholerae pandemic strains.
M. Labbate, Y. Boucher, M. J. Joss, C. A. Michael, M. R. Gillings, and H. W. Stokes (2007)
Microbiology 153, 1488-1498
   Abstract »    Full Text »    PDF »
Construction of a Vibrio splendidus Mutant Lacking the Metalloprotease Gene vsm by Use of a Novel Counterselectable Suicide Vector.
F. Le Roux, J. Binesse, D. Saulnier, and D. Mazel (2007)
Appl. Envir. Microbiol. 73, 777-784
   Abstract »    Full Text »    PDF »
Modes and Modulations of Antibiotic Resistance Gene Expression.
F. Depardieu, I. Podglajen, R. Leclercq, E. Collatz, and P. Courvalin (2007)
Clin. Microbiol. Rev. 20, 79-114
   Abstract »    Full Text »    PDF »
Genetic characteristics of Matlab variants of Vibrio cholerae O1 that are hybrids between classical and El Tor biotypes..
A. Safa, N. A. Bhuyian, S. Nusrin, M. Ansaruzzaman, M. Alam, T. Hamabata, Y. Takeda, D. A. Sack, and G. B. Nair (2006)
J. Med. Microbiol. 55, 1563-1569
   Abstract »    Full Text »    PDF »
Class 1 integrons potentially predating the association with tn402-like transposition genes are present in a sediment microbial community..
H. W. Stokes, C. L. Nesbo, M. Holley, M. I. Bahl, M. R. Gillings, and Y. Boucher (2006)
J. Bacteriol. 188, 5722-5730
   Abstract »    Full Text »    PDF »
Vibrio2005: the First International Conference on the Biology of Vibrios.
F. L. Thompson, K. E. Klose, and the AVIB Group (2006)
J. Bacteriol. 188, 4592-4596
   Full Text »    PDF »
Distribution and characterization of integrons in various serogroups of Vibrio cholerae strains isolated from diarrhoeal patients between 1992 and 2000 in Kolkata, India..
L. Shi, K. Fujihara, T. Sato, H. Ito, P. Garg, R. Chakrabarty, T. Ramamurthy, G. B. Nair, Y. Takeda, and S. Yamasaki (2006)
J. Med. Microbiol. 55, 575-583
   Abstract »    Full Text »    PDF »
Iron and Fur Regulation in Vibrio cholerae and the Role of Fur in Virulence.
A. R. Mey, E. E. Wyckoff, V. Kanukurthy, C. R. Fisher, and S. M. Payne (2005)
Infect. Immun. 73, 8167-8178
   Abstract »    Full Text »    PDF »
Comparative Study of Class 1 Integron and Vibrio cholerae Superintegron Integrase Activities.
L. Biskri, M. Bouvier, A.-M. Guerout, S. Boisnard, and D. Mazel (2005)
J. Bacteriol. 187, 1740-1750
   Abstract »    Full Text »    PDF »
Genomic characterization of non-O1, non-O139 Vibrio cholerae reveals genes for a type III secretion system.
M. Dziejman, D. Serruto, V. C. Tam, D. Sturtevant, P. Diraphat, S. M. Faruque, M. H. Rahman, J. F. Heidelberg, J. Decker, L. Li, et al. (2005)
PNAS 102, 3465-3470
   Abstract »    Full Text »    PDF »
Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes.
D. P. Pandey and K. Gerdes (2005)
Nucleic Acids Res. 33, 966-976
   Abstract »    Full Text »    PDF »
CARB-9, a Carbenicillinase Encoded in the VCR Region of Vibrio cholerae Non-O1, Non-O139 Belongs to a Family of Cassette-Encoded {beta}-Lactamases.
A. Petroni, R. G. Melano, H. A. Saka, A. Garutti, L. Mange, F. Pasteran, M. Rapoport, M. Miranda, D. Faccone, A. Rossi, et al. (2004)
Antimicrob. Agents Chemother. 48, 4042-4046
   Abstract »    Full Text »    PDF »
Biodiversity of Vibrios.
F. L. Thompson, T. Iida, and J. Swings (2004)
Microbiol. Mol. Biol. Rev. 68, 403-431
   Abstract »    Full Text »    PDF »
Integron integrase binds to bulged hairpin DNA.
C. Johansson, M. Kamali-Moghaddam, and L. Sundstrom (2004)
Nucleic Acids Res. 32, 4033-4043
   Abstract »    Full Text »    PDF »
Gram-positive bacteria are a major reservoir of Class 1 antibiotic resistance integrons in poultry litter.
S. Nandi, J. J. Maurer, C. Hofacre, and A. O. Summers (2004)
PNAS 101, 7118-7122
   Abstract »    Full Text »    PDF »
Integron Diversity in Heavy-Metal-Contaminated Mine Tailings and Inferences about Integron Evolution.
D. R. Nemergut, A. P. Martin, and S. K. Schmidt (2004)
Appl. Envir. Microbiol. 70, 1160-1168
   Abstract »    Full Text »    PDF »
Integrons or super integrons?.
R. M. Hall and H. W. Stokes (2004)
Microbiology 150, 3-4
   Full Text »    PDF »
Comparative Genome Analysis of Vibrio vulnificus, a Marine Pathogen.
C.-Y. Chen, K.-M. Wu, Y.-C. Chang, C.-H. Chang, H.-C. Tsai, T.-L. Liao, Y.-M. Liu, H.-J. Chen, A. B.-T. Shen, J.-C. Li, et al. (2003)
Genome Res. 13, 2577-2587
   Abstract »    Full Text »    PDF »
Multiple-Drug Resistance in D-Tartrate-Positive Salmonella enterica Serovar Paratyphi B Isolates from Poultry Is Mediated by Class 2 Integrons Inserted into the Bacterial Chromosome.
A. Miko, K. Pries, A. Schroeter, and R. Helmuth (2003)
Antimicrob. Agents Chemother. 47, 3640-3643
   Abstract »    Full Text »    PDF »
Molecular Characterization of a New Class 3 Integron in Klebsiella pneumoniae.
M. Correia, F. Boavida, F. Grosso, M. J. Salgado, L. M. Lito, J. M. Cristino, S. Mendo, and A. Duarte (2003)
Antimicrob. Agents Chemother. 47, 2838-2843
   Abstract »    Full Text »    PDF »
Excision and Integration of Cassettes by an Integron Integrase of Nitrosomonas europaea.
G. Leon and P. H. Roy (2003)
J. Bacteriol. 185, 2036-2041
   Abstract »    Full Text »    PDF »
Identification of Genetic Loci Required for Capsular Expression in Vibrio vulnificus.
A. B. Smith and R. J. Siebeling (2003)
Infect. Immun. 71, 1091-1097
   Abstract »    Full Text »    PDF »
Comparative Analysis of Superintegrons: Engineering Extensive Genetic Diversity in the Vibrionaceae.
D. A. Rowe-Magnus, A.-M. Guerout, L. Biskri, P. Bouige, and D. Mazel (2003)
Genome Res. 13, 428-442
   Abstract »    Full Text »    PDF »
Inaugural Article: Emergence and evolution of Vibrio cholerae O139.
S. M. Faruque, D. A. Sack, R. B. Sack, R. R. Colwell, Y. Takeda, and G. B. Nair (2003)
PNAS 100, 1304-1309
   Abstract »    Full Text »    PDF »
Interactions among Strategies Associated with Bacterial Infection: Pathogenicity, Epidemicity, and Antibiotic Resistance.
J. L. Martinez and F. Baquero (2002)
Clin. Microbiol. Rev. 15, 647-679
   Abstract »    Full Text »    PDF »
Comparison of Genome Structures of Vibrios, Bacteria Possessing Two Chromosomes.
K. Tagomori, T. Iida, and T. Honda (2002)
J. Bacteriol. 184, 4351-4358
   Abstract »    Full Text »    PDF »
New Carbenicillin-Hydrolyzing {beta}-Lactamase (CARB-7) from Vibrio cholerae Non-O1, Non-O139 Strains Encoded by the VCR Region of the V. cholerae Genome.
R. Melano, A. Petroni, A. Garutti, H. A. Saka, L. Mange, F. Pasteran, M. Rapoport, A. Rossi, and M. Galas (2002)
Antimicrob. Agents Chemother. 46, 2162-2168
   Abstract »    Full Text »    PDF »
Characterization of the Class 3 Integron and the Site-Specific Recombination System It Determines.
C. M. Collis, M.-J. Kim, S. R. Partridge, H. W. Stokes, and R. M. Hall (2002)
J. Bacteriol. 184, 3017-3026
   Abstract »    Full Text »    PDF »
Presence of a Group II Intron in a Multiresistant Serratia marcescens Strain That Harbors Three Integrons and a Novel Gene Fusion.
D. Centron and P. H. Roy (2002)
Antimicrob. Agents Chemother. 46, 1402-1409
   Abstract »    Full Text »    PDF »
The IntI-Like Tyrosine Recombinase of Shewanella oneidensis Is Active as an Integron Integrase.
F. Drouin, J. Melancon, and P. H. Roy (2002)
J. Bacteriol. 184, 1811-1815
   Abstract »    Full Text »    PDF »
Comparative genomic analysis of Vibrio cholerae: Genes that correlate with cholera endemic and pandemic disease.
M. Dziejman, E. Balon, D. Boyd, C. M. Fraser, J. F. Heidelberg, and J. J. Mekalanos (2002)
PNAS
   Abstract »    Full Text »    PDF »
Integron Integrases Possess a Unique Additional Domain Necessary for Activity.
N. Messier and P. H. Roy (2001)
J. Bacteriol. 183, 6699-6706
   Abstract »    Full Text »    PDF »
Molecular Analysis of Antibiotic Resistance Gene Clusters in Vibrio cholerae O139 and O1 SXT Constins.
B. Hochhut, Y. Lotfi, D. Mazel, S. M. Faruque, R. Woodgate, and M. K. Waldor (2001)
Antimicrob. Agents Chemother. 45, 2991-3000
   Abstract »    Full Text »    PDF »
Clinical and Environmental Isolates of Vibrio cholerae Serogroup O141 Carry the CTX Phage and the Genes Encoding the Toxin-Coregulated Pili.
A. Dalsgaard, O. Serichantalergs, A. Forslund, W. Lin, J. Mekalanos, E. Mintz, T. Shimada, and J. G. Wells (2001)
J. Clin. Microbiol. 39, 4086-4092
   Abstract »    Full Text »    PDF »
Integrons and Gene Cassettes in the Enterobacteriaceae.
P. A. White, C. J. McIver, and W. D. Rawlinson (2001)
Antimicrob. Agents Chemother. 45, 2658-2661
   Abstract »    Full Text »    PDF »
Role of Genomic Typing in Taxonomy, Evolutionary Genetics, and Microbial Epidemiology.
A. van Belkum, M. Struelens, A. de Visser, H. Verbrugh, and M. Tibayrenc (2001)
Clin. Microbiol. Rev. 14, 547-560
   Abstract »    Full Text »    PDF »
Efficiency of Recombination Reactions Catalyzed by Class 1 Integron Integrase IntI1.
C. M. Collis, G. D. Recchia, M.-J. Kim, H. W. Stokes, and R. M. Hall (2001)
J. Bacteriol. 183, 2535-2542
   Abstract »    Full Text »
Identification and Characterization of Integron-Mediated Antibiotic Resistance among Shiga Toxin-Producing Escherichia coli Isolates.
S. Zhao, D. G. White, B. Ge, S. Ayers, S. Friedman, L. English, D. Wagner, S. Gaines, and J. Meng (2001)
Appl. Envir. Microbiol. 67, 1558-1564
   Abstract »    Full Text »
Incidence of Class 1 and 2 Integrases in Clinical and Commensal Bacteria from Livestock, Companion Animals, and Exotics.
C. Goldstein, M. D. Lee, S. Sanchez, C. Hudson, B. Phillips, B. Register, M. Grady, C. Liebert, A. O. Summers, D. G. White, et al. (2001)
Antimicrob. Agents Chemother. 45, 723-726
   Abstract »    Full Text »
The evolutionary history of chromosomal super-integrons provides an ancestry for multiresistant integrons.
D. A. Rowe-Magnus, A.-M. Guerout, P. Ploncard, B. Dychinco, J. Davies, and D. Mazel (2001)
PNAS 98, 652-657
   Abstract »    Full Text »    PDF »
pepA, a Gene Mediating pH Regulation of Virulence Genes in Vibrio cholerae.
J. Behari, L. Stagon, and S. B. Calderwood (2001)
J. Bacteriol. 183, 178-188
   Abstract »    Full Text »
Characterization of In53, a Class 1 Plasmid- and Composite Transposon-Located Integron of Escherichia coli Which Carries an Unusual Array of Gene Cassettes.
T. Naas, Y. Mikami, T. Imai, L. Poirel, and P. Nordmann (2001)
J. Bacteriol. 183, 235-249
   Abstract »    Full Text »
Definition of the attI1 site of class 1 integrons.
S. R. Partridge, G. D. Recchia, C. Scaramuzzi, C. M. Collis, H. W. Stokes, and R. M. Hall (2000)
Microbiology 146, 2855-2864
   Abstract »    Full Text »
The Vibrio cholerae O1 chromosomal integron.
C. A. Clark, L. Purins, P. Kaewrakon, T. Focareta, and P. A. Manning (2000)
Microbiology 146, 2605-2612
   Abstract »    Full Text »
Bacteria are different: Observations, interpretations, speculations, and opinions about the mechanisms of adaptive evolution in prokaryotes.
B. R. Levin and C. T. Bergstrom (2000)
PNAS 97, 6981-6985
   Abstract »    Full Text »    PDF »
Antibiotic Resistance in the ECOR Collection: Integrons and Identification of a Novel aad Gene.
D. Mazel, B. Dychinco, V. A. Webb, and J. Davies (2000)
Antimicrob. Agents Chemother. 44, 1568-1574
   Abstract »    Full Text »
Toxin-Antitoxin Modules May Regulate Synthesis of Macromolecules during Nutritional Stress.
K. Gerdes (2000)
J. Bacteriol. 182, 561-572
   Full Text »
Incidence and Characterization of Integrons, Genetic Elements Mediating Multiple-Drug Resistance, in Avian Escherichia coli.
L. Bass, C. A. Liebert, M. D. Lee, A. O. Summers, D. G. White, S. G. Thayer, and J. J. Maurer (1999)
Antimicrob. Agents Chemother. 43, 2925-2929
   Abstract »    Full Text »
Identification and characterization of class 1 integrons in bacteria from an aquatic environment.
S. J. Rosser and H.-K. Young (1999)
J. Antimicrob. Chemother. 44, 11-18
   Abstract »    Full Text »
Many Class I Integrons Comprise Distinct Stable Structures Occurring in Different Species of Enterobacteriaceae Isolated from Widespread Geographic Regions in Europe.
P. Martinez-Freijo, A. C. Fluit, F.-J. Schmitz, J. Verhoef, and M. E. Jones (1999)
Antimicrob. Agents Chemother. 43, 686-689
   Abstract »    Full Text »
Antibiotic Resistance Conferred by a Conjugative Plasmid and a Class I Integron in Vibrio cholerae O1 El Tor Strains Isolated in Albania and Italy.
V. Falbo, A. Carattoli, F. Tosini, C. Pezzella, A. M. Dionisi, and I. Luzzi (1999)
Antimicrob. Agents Chemother. 43, 693-696
   Abstract »    Full Text »
Structural and Functional Characterization of IS1358 from Vibrio cholerae.
S. Dumontier, P. Trieu-Cuot, and P. Berche (1998)
J. Bacteriol. 180, 6101-6106
   Abstract »    Full Text »
Epidemiology, Genetics, and Ecology of Toxigenic Vibrio cholerae.
S. M. Faruque, M. J. Albert, and J. J. Mekalanos (1998)
Microbiol. Mol. Biol. Rev. 62, 1301-1314
   Abstract »    Full Text »    PDF »
Characterization of In40 of Enterobacter aerogenes BM2688, a Class 1 Integron with Two New Gene Cassettes, cmlA2 and qacF.
M.-C. Ploy, P. Courvalin, and T. Lambert (1998)
Antimicrob. Agents Chemother. 42, 2557-2563
   Abstract »    Full Text »
Comparative genomic analysis of Vibrio cholerae: Genes that correlate with cholera endemic and pandemic disease.
M. Dziejman, E. Balon, D. Boyd, C. M. Fraser, J. F. Heidelberg, and J. J. Mekalanos (2002)
PNAS 99, 1556-1561
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)