Insertion Sequence-excision Enhancer Removes Transposable Elements from Bacterial Genomes and Induces Various Genomic Deletions

Overview

Journal Nat Commun

Specialty Biology

Date 2011 Jan 13

PMID 21224843

Citations 25

Authors

Masahiro Kusumoto

Tadasuke Ooka

Yoshiaki Nishiya

Yoshitoshi Ogura

Takashi Saito

Yasuhiko Sekine

Taketoshi Iwata

Masato Akiba

Tetsuya Hayashi

Affiliations

Soon will be listed here.

Abstract

Insertion sequences (ISs) are the simplest transposable elements and are widely distributed in bacteria. It has long been thought that IS excision rarely occurs in bacterial cells because most bacteria exhibit no end-joining activity to regenerate donor DNA after IS excision. Recently, however, we found that excision of IS629, an IS3 family member, occurs frequently in Escherichia coli O157. In this paper, we describe a protein IS-excision enhancer (IEE) that promotes IS629 excision from the O157 genome in an IS transposase-dependent manner. Various types of genomic deletions are also generated on IEE-mediated IS excision, and IEE promotes the excision of other IS3 family members and ISs from several other IS families. These data and the phylogeny of IEE homologues found in a broad range of bacteria suggest that IEE proteins have coevolved with IS elements and have pivotal roles in bacterial genome evolution by inducing IS removal and genomic deletion.

Citing Articles

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The enterohemorrhagic Escherichia coli insertion sequence-excision enhancer protein is a DNA polymerase with microhomology-mediated end-joining activity.

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A unique eukaryotic lineage of composite-like DNA transposons encoding a DDD/E transposase and a His-Me finger homing endonuclease.

Kojima K, Bao W Mob DNA. 2022; 13(1):24.

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Insertion Sequence (IS)-Excision Enhancer (IEE)-Mediated IS Excision from the Gene Restores the Lactose Utilization Defect of Shiga Toxin-Producing Escherichia coli O121:H19 Strains and Is Responsible for Their Delayed Lactose Utilization Phenotype.

Nakamura K, Seto K, Isobe J, Taniguchi I, Gotoh Y, Hayashi T Appl Environ Microbiol. 2022; 88(16):e0076022.

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References

Nagel R, Chan A . Enhanced Tn10 and mini-Tn10 precise excision in DNA replication mutants of Escherichia coli K12. Mutat Res. 2000; 459(4):275-84. DOI: 10.1016/s0921-8777(00)00008-2. View

Kusumoto M, Nishiya Y, Kawamura Y, Shinagawa K . Identification of an insertion sequence, IS1203 variant, in a Shiga toxin 2 gene of Escherichia coli O157:H7. J Biosci Bioeng. 2005; 87(1):93-6. DOI: 10.1016/s1389-1723(99)80014-0. View

Makino K, Ishii K, Yasunaga T, Hattori M, Yokoyama K, Yutsudo C . Complete nucleotide sequences of 93-kb and 3.3-kb plasmids of an enterohemorrhagic Escherichia coli O157:H7 derived from Sakai outbreak. DNA Res. 1998; 5(1):1-9. DOI: 10.1093/dnares/5.1.1. View

Ohnishi M, Terajima J, Kurokawa K, Nakayama K, Murata T, Tamura K . Genomic diversity of enterohemorrhagic Escherichia coli O157 revealed by whole genome PCR scanning. Proc Natl Acad Sci U S A. 2002; 99(26):17043-8. PMC: 139266. DOI: 10.1073/pnas.262441699. View

Hayashi T, Makino K, Ohnishi M, Kurokawa K, Ishii K, Yokoyama K . Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res. 2001; 8(1):11-22. DOI: 10.1093/dnares/8.1.11. View

Kothapalli S, Nair S, Alokam S, Pang T, Khakhria R, Woodward D . Diversity of genome structure in Salmonella enterica serovar Typhi populations. J Bacteriol. 2005; 187(8):2638-50. PMC: 1070368. DOI: 10.1128/JB.187.8.2638-2650.2005. View

Okitsu T, Kusumoto M, Suzuki R, Sata S, Nishiya Y, Kawamura Y . Identification of shiga toxin-producing Escherichia coli possessing insertionally inactivated Shiga toxin gene. Microbiol Immunol. 2001; 45(4):319-22. DOI: 10.1111/j.1348-0421.2001.tb02625.x. View

Turlan C, Chandler M . IS1-mediated intramolecular rearrangements: formation of excised transposon circles and replicative deletions. EMBO J. 1995; 14(21):5410-21. PMC: 394650. DOI: 10.1002/j.1460-2075.1995.tb00225.x. View

Foster T, Lundblad V, Halling S, Kleckner N . Three Tn10-associated excision events: relationship to transposition and role of direct and inverted repeats. Cell. 1981; 23(1):215-27. DOI: 10.1016/0092-8674(81)90286-5. View

10.

SANGER F, Nicklen S, Coulson A . DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977; 74(12):5463-7. PMC: 431765. DOI: 10.1073/pnas.74.12.5463. View

11.

Tamura K, Dudley J, Nei M, Kumar S . MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 2007; 24(8):1596-9. DOI: 10.1093/molbev/msm092. View

12.

Zerbib D, Polard P, Escoubas J, Galas D, Chandler M . The regulatory role of the IS1-encoded InsA protein in transposition. Mol Microbiol. 1990; 4(3):471-7. DOI: 10.1111/j.1365-2958.1990.tb00613.x. View

13.

Lundblad V, Taylor A, Smith G, Kleckner N . Unusual alleles of recB and recC stimulate excision of inverted repeat transposons Tn10 and Tn5. Proc Natl Acad Sci U S A. 1984; 81(3):824-8. PMC: 344930. DOI: 10.1073/pnas.81.3.824. View

14.

Johnson R, Yin J, Reznikoff W . Control of Tn5 transposition in Escherichia coli is mediated by protein from the right repeat. Cell. 1982; 30(3):873-82. DOI: 10.1016/0092-8674(82)90292-6. View

15.

Akiba M, Uchida I, Nishimori K, Tanaka K, Anzai T, Kuwamoto Y . Comparison of Salmonella enterica serovar Abortusequi isolates of equine origin by pulsed-field gel electrophoresis and fluorescent amplified-fragment length polymorphism fingerprinting. Vet Microbiol. 2003; 92(4):379-88. DOI: 10.1016/s0378-1135(02)00422-4. View

16.

Mead P, Griffin P . Escherichia coli O157:H7. Lancet. 1998; 352(9135):1207-12. DOI: 10.1016/S0140-6736(98)01267-7. View

17.

Blattner F, Plunkett 3rd G, Bloch C, Perna N, Burland V, Riley M . The complete genome sequence of Escherichia coli K-12. Science. 1997; 277(5331):1453-62. DOI: 10.1126/science.277.5331.1453. View

18.

Szabo M, Kiss J, Nagy Z, Chandler M, Olasz F . Sub-terminal sequences modulating IS30 transposition in vivo and in vitro. J Mol Biol. 2007; 375(2):337-52. DOI: 10.1016/j.jmb.2007.10.043. View

19.

Sekine Y, Aihara K, Ohtsubo E . Linearization and transposition of circular molecules of insertion sequence IS3. J Mol Biol. 1999; 294(1):21-34. DOI: 10.1006/jmbi.1999.3181. View

20.

Djafari S, Hauf N, Tyczka J . Generation of isogenic deletion mutants of STEC. Methods Mol Med. 2002; 73:113-24. DOI: 10.1385/1-59259-316-x:113. View