Transposition of IntAs into the Conserved Regions of IS3 Family Elements

  • Han, Chang-Gyun (The Institute of Physical and Chemical Research (Riken))
  • Published : 2004.03.01

Abstract

Together with the previous reports, my computer survey revealed that several bacteria contain six copies of the type group II intron IntA. The sequence analysis of IntAs showed the high level of homology in the nucleotide sequence (91.9-99.8%). The consensus sequence, 2,270 base pair long, was derived from the nucleotide sequences of all IntA members. The size of the open reading frame intA was 502 amino acids long, that is homologous to reverse transcriptase-like proteins encoded within the group II introns. It was reported that EPEC.IntA and Sf.IntA were inserted into IS911 and IS629, respectively. The sequence of the flanking region IntA was analyzed here. The data show the insertion of EC.IntA into IS629, the insertion of EHEC.IntA into IS3, the insertion of Yp.IntA into IS904-like sequence, and the insertion of EK12.IntA into IS911. Interestingly, these IS elements nested by IntAs were the members of IS3 family elements. The sequences of the IS3 members correspond to the OrfB with the DDE motif conserved in retroviral integrases. Alignment of the flanking sequences of IntAs revealed that the flanking regions -25 to + 10 of insertion sites, that are generally believed to be required for the retrohoming, were not strongly conserved. The data presented here suggests that the retrohoming pathway of IntA seems to differ from those of other group II introns.

Keywords

References

  1. J.Mol.Biol. v.215 Basic local alignment search tool Altschul,S.F.;W.Gish;W.Miller;E.W.Myers;D.J.Lipman https://doi.org/10.1016/S0022-2836(05)80360-2
  2. J.Bacteriol v.177 Prokaryotic introns and inteins, a panoply of form and function Belfort,M.;M.E.Reaban;T.Coetzee;J.Z.Dalgaard https://doi.org/10.1128/jb.177.14.3897-3903.1995
  3. Cell 94 Retrohoming of a bacterial group II intron, mobiliy via complete reverse splicing, inependent of homologous DNA recombination Cousineau,B.;D.Smith;S.Lawrence-Cavanagh;J.E.Mueller;J.Yang;D.Mills;D.Manias;G.Dunny;A.M.Lambowitz;M.Belfort
  4. Mol.Microbiol v.4 Functional similarities between retroviruses and the IS3 family of bacterial insertion sequences? Fayet,O.;P.Ramond;P.Polard;M.F.Prere;M.Chandler https://doi.org/10.1111/j.1365-2958.1990.tb00555.x
  5. CR Acad.Sci.III v.317 Multiple group II self-splicing introns in mobile DNA from Escherichia coli Ferat,J.L.;M.LeGouar;F.Michel
  6. Nature v.364 Group II self-splicing introns in bacteria Ferat,J.L.;F,Michel https://doi.org/10.1038/364358a0
  7. J. Bacteriol v.183 Structural and functional characterization of IS679 and IS66- family elements Han,C.-G;Y.Shiga;T.Tobe;C.Sasakawa;E.Ohtsubo https://doi.org/10.1128/JB.183.14.4296-4304.2001
  8. J. Bacteriol v.180 Structural organization of virulence-associated plasmids o Yersinia pestis Hu.P.;J.Elliott;P.McCready;E.Skowronski;J.Garnes;A.Kobayashi;R.R.Brubaker;E.Garcia
  9. Nucleic Acids Res v.19 Retroviral integrase domains:DNA biningand the recognition of LTR sequences Khan,E.;J.P.G.Mack;R.A.Katz;J.Kulkosky;A.M.Skalka https://doi.org/10.1093/nar/19.4.851
  10. Nucleic Acids Res v.22 Evidence for a group II intron in Escherichia coli inserted into a highly conserved reading frame associated with mobile DNA sequences Knoop,V.;A.Brennicke https://doi.org/10.1093/nar/22.7.1167
  11. Mol.Cell. Biol v.12 Residues critical for retroiral integrative recombination in a region hat is highly conserved among retroviral/retrotransposon integrases and bacterial insertion sequence transposases Kulkosky,J.;K.S.Jones;R.A.Katz;J.P.G.Mack;A.M.Skalka https://doi.org/10.1128/MCB.12.5.2331
  12. Infect. Immun v.66 Complete DNA sequence and detailed analysis of the Yersinia pestis KIM5 plasmid encoding murine toxin and capsular antigen Lindler,L.E;G..Plano;V.Burland;G.F.Mayhew;F.R.Blattner
  13. Mol.Microbiol v.28 Characterization and splicing in vivo of a Simorhizobium meliloti group II intron associated with particular insertion sequences of the IS630-Tc/IS3 retroposon superfamily Matinez-Abarca,F.;S.Zekri;N.Toro https://doi.org/10.1046/j.1365-2958.1998.00894.x
  14. Nucleic Acids Res v.18 Nucleotide sequence of insertion element IS629 Matsutani,S.;E.Ohtsubo https://doi.org/10.1093/nar/18.7.1899
  15. Genes Dev v.11 A bacteial group II intron encoding reverse transcriptase, maturase, and DNA endonuclease activities: Biochemical demonstration of maturase activity and insertion of new genetic information within the intron Matsuura,M.;R.Saldanha,H.Ma;H.Wank;J.Yang;G.Mohr;S.Cavanagh;G.M.Dunny;M.Belfort;A.M.Lambowitz https://doi.org/10.1101/gad.11.21.2910
  16. Annu. Rev. Biochem v.64 Structure and activities of group II introns Michel,F.;J.L.Ferat https://doi.org/10.1146/annurev.bi.64.070195.002251
  17. Gene v.82 Comparative and functional anatomy o group II catalytic introns-a review Michel,F.;K.Umesono;H.Ozeki https://doi.org/10.1016/0378-1119(89)90026-7
  18. J. Bacteriol v.179 Homing of a group II intron from Lactococcus lactis subsp. lactis ML3 Mills,D.A.;D.A.Manias;L.L.McKay;G.M.Dunny https://doi.org/10.1128/jb.179.19.6107-6111.1997
  19. J. Bacteriol v.178 Splicing of a group II intron involved in the conjugative transfer of pRS01 in lactococci Mills,D.A.;L.L.McKay;G.M.Dunn https://doi.org/10.1128/jb.178.12.3531-3538.1996
  20. Gene v.174 A group II intron in a conjugative transposon fromthe gram-positive bacterium, Clostridium difficile Mullany,P.;M.Pallen;M.Wilks;J.R.Stephen;S.Tabaqchali https://doi.org/10.1016/0378-1119(96)00511-2
  21. Curr. Top Microbiol. Immunol v.204 Bacterial insertion sequence Ohtsubo,E.;Y.Sekine https://doi.org/10.1007/978-3-642-79795-8_1
  22. Proc. Natl. Acad. Sci. USA. v.85 Improved tools for biological sequence comparison Parson,W.R.;D.J.Lipman https://doi.org/10.1073/pnas.85.8.2444
  23. J. Bacteriol v.172 Isolation and analysis of IS911, a new member of the IS3 group of insertion sequences Prere,M.F.;M.Chandler;O.Fayet. https://doi.org/10.1128/jb.172.7.4090-4099.1990
  24. Infect. Immun v.65 Use of a novel appoach, temed island probing, identifies the Shigella flexnerishe pathogenicity island which encodes a homolog of he immunoglobulia A protease-like family o fproteins Rajakumar,K.;C.Sasakawa;B.Adler
  25. lactis strain NIZO R5 Nucleic Acids Res. v.18 Nucleotide sequence of IS904 from Lactococcus lactis subsp Rauch,P.J.;M.M.Beerthuyzen;W.M.deVos. https://doi.org/10.1093/nar/18.14.4253
  26. Mol.Microbiol v.9 The IS4 family of insertio sequences: evidence for a conserved transposase motif Rezsohazy,R.;B.Hallet,J.Delcour;J.Mahillon https://doi.org/10.1111/j.1365-2958.1993.tb01258.x
  27. Nucleic Acids Res v.16 IS150: distribution, nucleotide sequence and phylogenetic relationships of a new E.coli insertion element Schwartz,E.;M.Kroeger;B.Rak. https://doi.org/10.1093/nar/16.14.6789
  28. Mol.Microbiol v.21 Splicing of a group II intron in a functional ansfer gene of Lactococcus lactis Shearman,C.;J.J.Godon;M.Gasson https://doi.org/10.1046/j.1365-2958.1996.00610.x
  29. J. Bacteriol v.183 Identification and distribution of new insertion sequences in the genome of alkalipili Bacillus halodurans C-125. Takami,H.;C.-G.Han;Y.Takaki;E.Ohtsubo https://doi.org/10.1128/JB.183.14.4345-4356.2001
  30. Nucleic Acids Res v.22 CLUSTALW: improvingthe sensitivity of progressie multiple sequence alignment through sequence weighting, position-specifie gap penalities and weight matrix choice Thompson,J.D.;D.G.Higgins;T.J.Gibson https://doi.org/10.1093/nar/22.22.4673
  31. Nucleic Acids Res v.13 Complete sequence of IS3. Timmerman,K.P.;C.-P.Tu. https://doi.org/10.1093/nar/13.6.2127
  32. Infect. Immun v.67 Complete DNA sequence and structural analysis of the enteropathogenic Escherichia coli adherence factor plasmid Tobe,T.;T.Hayashi,C.-G.Han;G.K.Schoolnik;E.Ohtsubo;C.Sasakawa