Abstract
The attC sites are well-known integrase-targeted elements involved in the insertion and excision of gene cassettes from integrons. Recently, functional analysis of Sma.I2, a class C-attC group II intron, showed that this mobile element invades the attC sites through a specific process. The analysis of genomic data indicates that class C-attC group II introns are independently acquired by their bacterial hosts and evolve in the recognition of a variety of target sites, including the attCs. In addition, adaptation of class C-attC group II introns seemed to be favourable for particular genera, such as Shewanella, suggesting a possible niche for the spread of class C-attC group II introns inserted at attC sites. This understanding suggests a functional role of short palindromic DNA sequences, such as the attCs, as important tools for the acquisition of mobile elements associated with horizontal gene transfer.
Similar content being viewed by others
References
Boucher Y, Nesbo CL, Joss MJ, Robinson A, Mabbutt BC, Gillings MR, Doolittle WF, Stokes HW (2006) Recovery and evolutionary analysis of complete integron gene cassette arrays from Vibrio. BMC Evol Biol 6:3
Boucher Y, Labbate M, Koenig JE, Stokes HW (2007) Integrons: mobilizable platforms that promote genetic diversity in bacteria. Trends Microbiol 15:301–309
Bouvier M, Demarre G, Mazel D (2005) Integron cassette insertion: a recombination process involving a folded single strand substrate. EMBO J 24:4356–4367
Centrón D, Roy PH (2002) Presence of a group II intron in a multiresistant Serratia marcescens strain that harbors three integrons and a novel gene fusion. Antimicrob Agents Chemother 46:1402–1409
Chen S, Zhao S, White DG, Schroeder CM, Lu R, Yang H, McDermott PF, Ayers S, Meng J (2004) Characterization of multiple-antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl Environ Microbiol 70:1–7
Cousineau B, Smith D, Lawrence-Cavanagh S, Mueller JE, Yang J, Mills D, Manias D, Dunny G, Lambowitz AM, Belfort M (1998) Retrohoming of a bacterial group II intron: mobility via complete reverse splicing, independent of homologous DNA recombination. Cell 94:451–462
Cousineau B, Lawrence S, Smith D, Belfort M (2000) Retrotransposition of a bacterial group II intron. Nature 404:1018–1021
Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190
Dai L, Zimmerly S (2002) Compilation and analysis of group II intron insertions in bacterial genomes: evidence for retroelement behavior. Nucleic Acids Res 30:1091–1102
Francia MV, Zabala JC, de la Cruz F, Garcia Lobo JM (1999) The IntI1 integron integrase preferentially binds single-stranded DNA of the attC site. J Bacteriol 181:6844–6849
Hall RM, Stokes HW (1993) Integrons: novel DNA elements which capture genes by site-specific recombination. Genetica 90:115–132
Hall RM, Brookes DE, Stokes HW (1991) Site-specific insertion of genes into integrons: role of the 59-base element and determination of the recombination cross-over point. Mol Microbiol 5:1941–1959
Hau HH, Gralnick JA (2007) Ecology and biotechnology of the genus Shewanella. Annu Rev Microbiol 61:237–258
Holmes AJ, Gillings MR, Nield BS, Mabbutt BC, Nevalainen KM, Stokes HW (2003) The gene cassette metagenome is a basic resource for bacterial genome evolution. Environ Microbiol 5:383–394
Holt HM, Gahrn-Hansen B, Bruun B (2005) Shewanella algae and Shewanella putrefaciens: clinical and microbiological characteristics. Clin Microbiol Infect 11:347–352
Johansson C, Kamali-Moghaddam M, Sundstrom L (2004) Integron integrase binds to bulged hairpin DNA. Nucleic Acids Res 32:4033–4043
Labbate M, Boucher Y, Joss MJ, Michael CA, Gillings MR, Stokes HW (2007) Use of chromosomal integron arrays as a phylogenetic typing system for Vibrio cholerae pandemic strains. Microbiol 153:1488–1498
Lambowitz AM, Belfort M (1993) Introns as mobile genetic elements. Annu Rev Biochem 62:587–622
Lambowitz AM, Zimmerly S (2004) Mobile group II introns. Annu Rev Genet 38:1–35
Leon G, Roy PH (2003) Excision and integration of cassettes by an integron integrase of Nitrosomonas europaea. J Bacteriol 185:2036–2041
MacDonald D, Demarre G, Bouvier M, Mazel D, Gopaul DN (2006) Structural basis for broad DNA-specificity in integron recombination. Nature 440:1157–1162
Messier N, Roy PH (2001) Integron integrases possess a unique additional domain necessary for activity. J Bacteriol 183:6699–6706
Navarre WW, McClelland M, Libby SJ, Fang FC (2007) Silencing of xenogeneic DNA by H-NS-facilitation of lateral gene transfer in bacteria by a defense system that recognizes foreign DNA. Genes Dev 21:1456–1471
Nemergut DR, Robeson MS, Kysela RF, Martin AP, Schmidt SK, Knight R (2008) Insights and inferences about integron evolution from genomic data. BMC Genomics 9:261
Orman BE, Pineiro SA, Arduino S, Galas M, Melano R, Caffer MI, Sordelli DO, Centron D (2002) Evolution of multiresistance in nontyphoid Salmonella serovars from 1984 to 1998 in Argentina. Antimicrob Agents Chemother 46:3963–3970
Petrillo M, Silvestro G, Di Nocera PP, Boccia A, Paolella G (2006) Stem-loop structures in prokaryotic genomes. BMC Genomics 7:170
Quiroga C, Roy PH, Centron D (2008) The S.ma.I2 class C group II intron inserts at integron attC sites. Microbiology 154:1341–1353
Robart AR, Seo W, Zimmerly S (2007) Insertion of group II intron retroelements after intrinsic transcriptional terminators. Proc Natl Acad Sci U S A 104:6620–6625
Rowe-Magnus DA, Guerout AM, Biskri L, Bouige P, Mazel D (2003) Comparative analysis of superintegrons: engineering extensive genetic diversity in the Vibrionaceae. Genome Res 13:428–442
Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualization and annotation. Bioinformatics 16:944–945
Stokes HW, O’Gorman DB, Recchia GD, Parsekhian M, Hall RM (1997) Structure and function of 59-base element recombination sites associated with mobile gene cassettes. Mol Microbiol 26:731–745
Sunde M (2005) Class I integron with a group II intron detected in an Escherichia coli strain from a free-range reindeer. Antimicrob Agents Chemother 49:2512–2514
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Tetu SG, Holmes AJ (2008) A family of insertion sequences that impacts integrons by specific targeting of gene cassette recombination sites, the IS1111-attC Group. J Bacteriol 190:4959–4970
Tobes R, Pareja E (2006) Bacterial repetitive extragenic palindromic sequences are DNA targets for insertion sequence elements. BMC Genomics 7:62
Toor N, Hausner G, Zimmerly S (2001) Coevolution of group II intron RNA structures with their intron-encoded reverse transcriptases. RNA 7:1142–1152
Val ME, Bouvier M, Campos J, Sherratt D, Cornet F, Mazel D, Barre FX (2005) The single-stranded genome of phage CTX is the form used for integration into the genome of Vibrio cholerae. Mol Cell 19:559–566
Yum JH, Yi K, Lee H, Yong D, Lee K, Kim JM, Rossolini GM, Chong Y (2002) Molecular characterization of metallo-beta-lactamase-producing A. baumannii and Acinetobacter genomospecies 3 from Korea: identification of two new integrons carrying the bla(VIM-2) gene cassettes. J Antimicrob Chemother 49:837–840
Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415
Acknowledgments
This study was supported by grant BID/OC-AR 1723 ANPCyT 13431 and BID 1728/OC-AR ANPCyT 0690 to D. C. and BID 1728/OC-AR ANPCyT 0730 to C. Q. from the Agencia Nacional de Promoción de Ciencia y Técnica C. Q. is a recipient of a CONICET fellowship. D. C. is a member of Carrera del Investigador Científico at CONICET.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Quiroga, C., Centrón, D. Using Genomic Data to Determine the Diversity and Distribution of Target Site Motifs Recognized by Class C-attC Group II Introns. J Mol Evol 68, 539–549 (2009). https://doi.org/10.1007/s00239-009-9228-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-009-9228-3