Skip to main content
Log in

A large inversion in the linear chromosome of Streptomyces griseus caused by replicative transposition of a new Tn3 family transposon

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

We have comprehensively analyzed the linear chromosomes of Streptomyces griseus mutants constructed and kept in our laboratory. During this study, macrorestriction analysis of AseI and DraI fragments of mutant 402-2 suggested a large chromosomal inversion. The junctions of chromosomal inversion were cloned and sequenced and compared with the corresponding target sequences in the parent strain 2247. Consequently, a transposon-involved mechanism was revealed. Namely, a transposon originally located at the left target site was replicatively transposed to the right target site in an inverted direction, which generated a second copy and at the same time caused a 2.5-Mb chromosomal inversion. The involved transposon named TnSGR was grouped into a new subfamily of the resolvase-encoding Tn3 family transposons based on its gene organization. At the end, terminal diversity of S. griseus chromosomes is discussed by comparing the sequences of strains 2247 and IFO13350.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bentley SD, Chater KF, Cerdeno-Tarraga AM et al (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147

    Article  PubMed  Google Scholar 

  • Brown NL, Misra TK, Winnie JN, Schmidt A, Seiff M, Silver S (1986) The nucleotide sequence of the mercuric resistance operons of plasmid R100 and transposon Tn501: further evidence for mer genes which enhance the activity of the mercuric ion detoxification system. Mol Gen Genet 202:143–151

    Article  PubMed  CAS  Google Scholar 

  • Chen CW, Huang CH, Lee HH, Tsai HH, Kirby R (2002) Once the circle has been broken: dynamics and evolution of Streptomyces chromosomes. Trends Genet 18:522–529

    Article  PubMed  CAS  Google Scholar 

  • Delic V, Hopwood DA, Friend EJ (1970) Mutagenesis by N-methyl-N’-nitro-N-nitrosoguanidine (NTG) in Streptomyces coelicolor. Mutat Res 9:167–182

    Article  PubMed  CAS  Google Scholar 

  • Fischer G, Decaris B, Leblond P (1997) Occurrence of deletions, associated with genetic instability in Streptomyces ambofaciens, is independent of the linearity of the chromosomal DNA. J Bacteriol 179:4553–4558

    PubMed  CAS  Google Scholar 

  • Fischer G, Wenner T, Decaris B, Leblond P (1998) Chromosomal arm replacement generates a high level of intraspecific polymorphism in the terminal inverted repeats of the linear chromosomal DNA of Streptomyces ambofaciens. Proc Natl Acad Sci USA 95:14296–14301

    Article  PubMed  CAS  Google Scholar 

  • Goshi K, Uchida T, Lezhava A, Yamasaki M, Hiratsu K, Shinkawa H, Kinashi H (2002) Cloning and analysis of the telomere and terminal inverted repeat of the linear chromosome of Streptomyces griseus. J Bacteriol 184:3411–3415

    Article  PubMed  CAS  Google Scholar 

  • Grindley ND (2002) The movement of Tn3-like elements: transposition and cointegrate resolution. In: Mobile DNA II, ASM Press, Washington, DC, pp 272–302

  • Heffron F, McCarthy BL, Ohtsubo H, Ohtsubo E (1979) DNA sequence analysis of the transposon Tn3: three genes and three sites involved in transposition of Tn3. Cell 18:1153–1163

    Article  PubMed  CAS  Google Scholar 

  • Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, Sakaki Y, Hattori M, Omura S (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21:526–531

    Article  PubMed  Google Scholar 

  • Inoue S, Higashiyama K, Uchida T, Hiratsu K, Kinashi H (2003) Chromosomal circularization in Streptomyces griseus by nonhomologous recombination of deletion ends. Biosci Biotechnol Biochem 67:1101–1108

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa J, Hotta K (1999) FramePlot: a new implementation of the frame analysis for predicting protein-coding regions in bacterial DNA with a high G + C content. FEMS Microbiol Lett 174:251–253

    Article  PubMed  CAS  Google Scholar 

  • Kameoka D, Lezhava A, Zenitani H, Hiratsu K, Kawamoto M, Goshi K, Inada K, Shinkawa H, Kinashi H (1999) Analysis of fusion junctions of circularized chromosomes in Streptomyces griseus. J Bacteriol 181:5711–5717

    PubMed  CAS  Google Scholar 

  • Kinashi H (2008) Antibiotic production, linear plasmids and linear chromosomes in Streptomyces. Actinomycetol 22:20–29

    Article  CAS  Google Scholar 

  • Lezhava A, Mizukami T, Kajitani T, Kameoka D, Redenbach M, Shinkawa H, Nimi O, Kinashi H (1995) Physical map of the linear chromosome of Streptomyces griseus. J Bacteriol 177:6492–6498

    PubMed  CAS  Google Scholar 

  • Lezhava A, Kameoka D, Sugino H, Goshi K, Shinkawa H, Nimi O, Horinouchi S, Beppu T, Kinashi H (1997) Chromosomal deletions in Streptomyces griseus that remove the afsA Iocus. Mol Gen Genet 253:478–483

    Article  PubMed  CAS  Google Scholar 

  • Ohnishi Y, Ishikawa J, Hara H, Suzuki H, Ikenoya M, Ikeda H, Yamashita A, Hattori M, Horinouchi S (2008) Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO13359. J Bacteriol 190:4050–4060

    Article  PubMed  CAS  Google Scholar 

  • Pandza S, Biukovic G, Paravic A, Dadbin AJ, Cullum J, Hranueli D (1998) Recombination between the linear plasmid pPZG101 and the linear chromosome of Streptomyces rimosus can lead to exchange of ends. Mol Microbiol 28:1165–1176

    Article  PubMed  CAS  Google Scholar 

  • Qin Z, Cohen SN (2002) Survival mechanism for Streptomyces linear replicons after telomere damage. Mol Microbiol 45:785–794

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, NY

    Google Scholar 

  • Shinkawa H, Sugiyama M, Hatada Y, Ohuchi T, Udagawa M, Mini O (1991) Silence of streptomycin 6-phosphotransferase gene derived by incubation at a high temperature in Streptomyces griseus. Biotechnol Lett 13:537–542

    Article  CAS  Google Scholar 

  • Sugiyama M, Nimi O (1990) Streptomycin biosynthesis and self-resistance mechanism in streptomycin-producing Streptomyces griseus. Actinomycetol 4:15–22

    Article  Google Scholar 

  • Suwa M, Sugino H, Sasaoka A, Mori E, Fujii S, Shinkawa H, Nimi O, Kinashi H (2000) Identification of two polyketide synthase gene clusters on the linear plasmid pSLA2-L in Streptomyces rochei. Gene 246:123–131

    Article  PubMed  CAS  Google Scholar 

  • Uchida T, Miyawaki M, Kinashi H (2003) Chromosomal arm replacement in Streptomyces griseus. J Bacteriol 185:1120–1124

    Article  PubMed  CAS  Google Scholar 

  • Uchida T, Ishihara N, Zenitani H, Hiratsu K, Kinashi H (2004) Circularized chromosome with a large palindromic structure in Streptomyces griseus mutants. J Bacteriol 186:3313–3320

    Article  PubMed  CAS  Google Scholar 

  • Volff JN, Altenbuchner J (1998) Genetic instability of the Streptomyces chromosome. Mol Microbiol 27:239–246

    Article  PubMed  CAS  Google Scholar 

  • Wei JR, Tsai YH, Horng YT, Soo PC, Hsieh SC, Hsueh PR, Horng JT, Williams P, Lai HC (2006) A mobile quorum-sensing system in Serratia marcescens. J Bacteriol 188:1518–1525

    Article  PubMed  CAS  Google Scholar 

  • Widenbrant EM, Tsai HH, Chen CW, Kao CM (2007) Streptomyces coelicolor undergoes spontaneous chromosomal end replacement. J Bacteriol 189:9117–9121

    Article  PubMed  CAS  Google Scholar 

  • Yamasaki M, Kinashi H (2004) Two chimeric chromosomes of Streptomyces coelicolor A3(2) generated by single crossover of the wild-type chromosome and linear plasmid SCP1. J Bacteriol 186:6553–6559

    Article  PubMed  CAS  Google Scholar 

  • Yin X, Zabriskie TM (2006) The enduracidin biosynthetic gene cluster from Streptomyces fungicidicus. Microbiology 152:2969–2983

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Grant-in-Aid for Scientific Research on Priority Areas (C) “Genome Biology” from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to H. Kinashi.

Additional information

Communicated by Jan-Luc Pernodet.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Murata, M., Uchida, T., Yang, Y. et al. A large inversion in the linear chromosome of Streptomyces griseus caused by replicative transposition of a new Tn3 family transposon. Arch Microbiol 193, 299–306 (2011). https://doi.org/10.1007/s00203-010-0674-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-010-0674-5

Keywords

Navigation