Identification and characterization of repetitive extragenic palindromes (REP)-associated tyrosine transposases: implications for REP evolution and dynamics in bacterial genomes
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
20085626
PubMed Central
PMC2817692
DOI
10.1186/1471-2164-11-44
PII: 1471-2164-11-44
Knihovny.cz E-zdroje
- MeSH
- Bacteria chemie genetika MeSH
- fylogeneze MeSH
- genom bakteriální * MeSH
- konzervovaná sekvence MeSH
- molekulární evoluce * MeSH
- molekulární sekvence - údaje MeSH
- obrácené repetice * MeSH
- otevřené čtecí rámce MeSH
- sekvence aminokyselin MeSH
- sekvenční seřazení MeSH
- transposasy analýza chemie genetika metabolismus MeSH
- tyrosin metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- transposasy MeSH
- tyrosin MeSH
BACKGROUND: Bacterial repetitive extragenic palindromes (REPs) compose a distinct group of genomic repeats. They usually occur in high abundance (>100 copies/genome) and are often arranged in composite repetitive structures - bacterial interspersed mosaic elements (BIMEs). In BIMEs, regularly spaced REPs are present in alternating orientations. BIMEs and REPs have been shown to serve as binding sites for several proteins and suggested to play role in chromosome organization and transcription termination. Their origins are, at present, unknown. RESULTS: In this report, we describe a novel class of putative transposases related to IS200/IS605 transposase family and we demonstrate that they are obligately associated with bacterial REPs. Open reading frames coding for these REP-associated tyrosine transposases (RAYTs) are always flanked by two REPs in inverted orientation and thus constitute a unit reminiscent of typical transposable elements. Besides conserved residues involved in catalysis of DNA cleavage, RAYTs carry characteristic structural motifs that are absent in typical IS200/IS605 transposases. DNA sequences flanking rayt genes are in one third of examined cases arranged in modular BIMEs. RAYTs and their flanking REPs apparently coevolve with each other. The rayt genes themselves are subject to rapid evolution, substantially exceeding the substitution rate of neighboring genes. Strong correlation was found between the presence of a particular rayt in a genome and the abundance of its cognate REPs. CONCLUSIONS: In light of our findings, we propose that RAYTs are responsible for establishment of REPs and BIMEs in bacterial genomes, as well as for their exceptional dynamics and species-specifity. Conversely, we suggest that BIMEs are in fact a special type of nonautonomous transposable elements, mobilizable by RAYTs.
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Lam S, Roth JR. IS200: a Salmonella-specific insertion sequence. Cell. 1983;34(3):951–960. doi: 10.1016/0092-8674(83)90552-4. PubMed DOI
Filee J, Siguier P, Chandler M. Insertion sequence diversity in archaea. Microbiol Mol Biol Rev. 2007;71(1):121–157. doi: 10.1128/MMBR.00031-06. PubMed DOI PMC
IS Finder. http://www-is.biotoul.fr/
Ronning DR, Guynet C, Ton-Hoang B, Perez ZN, Ghirlando R, Chandler M, Dyda F. Active site sharing and subterminal hairpin recognition in a new class of DNA transposases. Mol Cell. 2005;20(1):143–154. doi: 10.1016/j.molcel.2005.07.026. PubMed DOI
Lee HH, Yoon JY, Kim HS, Kang JY, Kim KH, Kim DJ, Ha JY, Mikami B, Yoon HJ, Suh SW. Crystal structure of a metal ion-bound IS200 transposase. J Biol Chem. 2006;281(7):4261–4266. doi: 10.1074/jbc.M511567200. PubMed DOI
Barabas O, Ronning DR, Guynet C, Hickman AB, Ton-Hoang B, Chandler M, Dyda F. Mechanism of IS200/IS605 family DNA transposases: activation and transposon-directed target site selection. Cell. 2008;132(2):208–220. doi: 10.1016/j.cell.2007.12.029. PubMed DOI PMC
Monzingo AF, Ozburn A, Xia S, Meyer RJ, Robertus JD. The structure of the minimal relaxase domain of MobA at 2.1 A resolution. J Mol Biol. 2007;366(1):165–178. doi: 10.1016/j.jmb.2006.11.031. PubMed DOI PMC
Prak ET, Kazazian HH Jr. Mobile elements and the human genome. Nat Rev Genet. 2000;1(2):134–144. doi: 10.1038/35038572. PubMed DOI
Kapitonov VV, Jurka J. Rolling-circle transposons in eukaryotes. Proc Natl Acad Sci USA. 2001;98(15):8714–8719. doi: 10.1073/pnas.151269298. PubMed DOI PMC
Siguier P, Filee J, Chandler M. Insertion sequences in prokaryotic genomes. Curr Opin Microbiol. 2006;9(5):526–531. doi: 10.1016/j.mib.2006.08.005. PubMed DOI
Buisine N, Tang CM, Chalmers R. Transposon-like Correia elements: structure, distribution and genetic exchange between pathogenic Neisseria sp. FEBS Lett. 2002;522(1-3):52–58. doi: 10.1016/S0014-5793(02)02882-X. PubMed DOI
Oggioni MR, Claverys JP. Repeated extragenic sequences in prokaryotic genomes: a proposal for the origin and dynamics of the RUP element in Streptococcus pneumoniae. Microbiology. 1999;145(Pt 10):2647–2653. PubMed
Higgins CF, Ames GF, Barnes WM, Clement JM, Hofnung M. A novel intercistronic regulatory element of prokaryotic operons. Nature. 1982;298(5876):760–762. doi: 10.1038/298760a0. PubMed DOI
Tobes R, Ramos JL. REP code: defining bacterial identity in extragenic space. Environ Microbiol. 2005;7(2):225–228. doi: 10.1111/j.1462-2920.2004.00704.x. PubMed DOI
Tobes R, Pareja E. Repetitive extragenic palindromic sequences in the Pseudomonas syringae pv. tomato DC3000 genome: extragenic signals for genome reannotation. Res Microbiol. 2005;156(3):424–433. doi: 10.1016/j.resmic.2004.10.014. PubMed DOI
Aranda-Olmedo I, Tobes R, Manzanera M, Ramos JL, Marques S. Species-specific repetitive extragenic palindromic (REP) sequences in Pseudomonas putida. Nucleic Acids Res. 2002;30(8):1826–1833. doi: 10.1093/nar/30.8.1826. PubMed DOI PMC
Gilson E, Saurin W, Perrin D, Bachellier S, Hofnung M. Palindromic units are part of a new bacterial interspersed mosaic element (BIME) Nucleic Acids Res. 1991;19(7):1375–1383. doi: 10.1093/nar/19.7.1375. PubMed DOI PMC
Boccard F, Prentki P. Specific interaction of IHF with RIBs, a class of bacterial repetitive DNA elements located at the 3' end of transcription units. Embo J. 1993;12(13):5019–5027. PubMed PMC
Bachellier S, Clement JM, Hofnung M. Short palindromic repetitive DNA elements in enterobacteria: a survey. Res Microbiol. 1999;150(9-10):627–639. doi: 10.1016/S0923-2508(99)00128-X. PubMed DOI
Espeli O, Boccard F. In vivo cleavage of Escherichia coli BIME-2 repeats by DNA gyrase: genetic characterization of the target and identification of the cut site. Mol Microbiol. 1997;26(4):767–777. doi: 10.1046/j.1365-2958.1997.6121983.x. PubMed DOI
Gilson E, Perrin D, Hofnung M. DNA polymerase I and a protein complex bind specifically to E. coli palindromic unit highly repetitive DNA: implications for bacterial chromosome organization. Nucleic Acids Res. 1990;18(13):3941–3952. doi: 10.1093/nar/18.13.3941. PubMed DOI PMC
Espeli O, Moulin L, Boccard F. Transcription attenuation associated with bacterial repetitive extragenic BIME elements. J Mol Biol. 2001;314(3):375–386. doi: 10.1006/jmbi.2001.5150. PubMed DOI
Gilson E, Perrin D, Saurin W, Hofnung M. Species specificity of bacterial palindromic units. J Mol Evol. 1987;25(4):371–373. doi: 10.1007/BF02603122. PubMed DOI
Roscetto E, Rocco F, Carlomagno MS, Casalino M, Colonna B, Zarrilli R, Di Nocera PP. PCR-based rapid genotyping of Stenotrophomonas maltophilia isolates. BMC Microbiol. 2008;8:202. doi: 10.1186/1471-2180-8-202. PubMed DOI PMC
Distribution of repeated palindromes on E. coli K-12 chromosome. http://www.pasteur.fr/recherche/unites/pmtg/repet/distrib.html
Silby MW, Cerdeno-Tarraga AM, Vernikos GS, Giddens SR, Jackson RW, Preston GM, Zhang XX, Moon CD, Gehrig SM, Godfrey SA. et al.Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biol. 2009;10(5):R51. doi: 10.1186/gb-2009-10-5-r51. PubMed DOI PMC
Bachellier S, Clement JM, Hofnung M, Gilson E. Bacterial interspersed mosaic elements (BIMEs) are a major source of sequence polymorphism in Escherichia coli intergenic regions including specific associations with a new insertion sequence. Genetics. 1997;145(3):551–562. PubMed PMC
Tobes R, Pareja E. Bacterial repetitive extragenic palindromic sequences are DNA targets for Insertion Sequence elements. BMC Genomics. 2006;7:62. doi: 10.1186/1471-2164-7-62. PubMed DOI PMC
Ramos-Gonzalez MI, Campos MJ, Ramos JL, Espinosa-Urgel M. Characterization of the Pseudomonas putida mobile genetic element ISPpu10: an occupant of repetitive extragenic palindromic sequences. J Bacteriol. 2006;188(1):37–44. doi: 10.1128/JB.188.1.37-44.2006. PubMed DOI PMC
Clement JM, Wilde C, Bachellier S, Lambert P, Hofnung M. IS1397 is active for transposition into the chromosome of Escherichia coli K-12 and inserts specifically into palindromic units of bacterial interspersed mosaic elements. J Bacteriol. 1999;181(22):6929–6936. PubMed PMC
Choi S, Ohta S, Ohtsubo E. A novel IS element, IS621, of the IS110/IS492 family transposes to a specific site in repetitive extragenic palindromic sequences in Escherichia coli. J Bacteriol. 2003;185(16):4891–4900. doi: 10.1128/JB.185.16.4891-4900.2003. PubMed DOI PMC
Wilde C, Bachellier S, Hofnung M, Carniel E, Clement JM. Palindromic unit-independent transposition of IS1397 in Yersinia pestis. J Bacteriol. 2002;184(17):4739–4746. doi: 10.1128/JB.184.17.4739-4746.2002. PubMed DOI PMC
Wilde C, Escartin F, Kokeguchi S, Latour-Lambert P, Lectard A, Clement JM. Transposases are responsible for the target specificity of IS1397 and ISKpn1 for two different types of palindromic units (PUs) Nucleic Acids Res. 2003;31(15):4345–4353. doi: 10.1093/nar/gkg494. PubMed DOI PMC
Wilde C, Bachellier S, Hofnung M, Clement JM. Transposition of IS1397 in the family Enterobacteriaceae and first characterization of ISKpn1, a new insertion sequence associated with Klebsiella pneumoniae palindromic units. J Bacteriol. 2001;183(15):4395–4404. doi: 10.1128/JB.183.15.4395-4404.2001. PubMed DOI PMC
Canceill D, Viguera E, Ehrlich SD. Replication slippage of different DNA polymerases is inversely related to their strand displacement efficiency. J Biol Chem. 1999;274(39):27481–27490. doi: 10.1074/jbc.274.39.27481. PubMed DOI
Versalovic J, Koeuth T, Lupski JR. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res. 1991;19(24):6823–6831. doi: 10.1093/nar/19.24.6823. PubMed DOI PMC
National Center for Biotechnology Information. http://www.ncbi.nlm.nih.gov/
OligoRep system. http://wwwmgs.bionet.nsc.ru/mgs/programs/oligorep/
pDRAW32 DNA analysis software. http://www.acaclone.com/
Moretti S, Armougom F, Wallace IM, Higgins DG, Jongeneel CV, Notredame C. The M-Coffee web server: a meta-method for computing multiple sequence alignments by combining alternative alignment methods. Nucleic Acids Res. 2007. pp. W645–648. PubMed DOI PMC
Mobyle, a portal for bioinformatics analyses. http://mobyle.pasteur.fr/cgi-bin/portal.py
Structural variability of CG-rich DNA 18-mers accommodating double T-T mismatches