Skip to main content
SpringerLink
Log in

Lagging strand replication of rolling-circle plasmids in Streptomyces lividans: an RNA polymerase-independent primer synthesis

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

Abstract

The rolling circle (RC) mechanism of DNA replication generating single-stranded DNA (ssDNA) intermediates is common in various high-copy circular plasmids in Streptomyces, and the ssDNA released after leading strand synthesis is converted to its double-stranded form (dsDNA) by the host proteins. The in vivo and in vitro lagging strand syntheses from ssDNA replicative intermediates of RC plasmid pSN22 in Streptomyces lividans was characterized. The presence or absence of the single-strand origin (sso), the replication initiation site of lagging strand synthesis, did not significantly affect the copy numbers of pSN22 derivatives. In vivo lagging strand synthesis was not affected by the rifampicin inhibition of S. lividans RNA polymerase. Likewise, in vitro lagging strand synthesis using cell-free extracts revealedsso-independent, rifampicin-resistant lagging strand synthesis in S. lividans. Although all four dNTPs are usually required for the initiation of such synthesis, the presence of only one NTP was sufficient to carry outlagging strand synthesis in vitro. Interestingly, the cell-free extract of exponential-phase cells required less ATP than that of stationary-phase cells. These results reveal a predominant RNA polymerase-independent priming system in S. lividans that may be a result of the stabilization of RC plasmids lacking sso in S. lividans.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3a,b
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Arai K, Kornberg A (1979) A general priming system employing only dnaB protein and primase for DNA replication. Proc Natl Acad Sci USA 76:4308–4312

    CAS  PubMed  Google Scholar 

  • Arai K, Kornberg A (1981a) Mechanism of dnaB protein action. III. Allosteric role of ATP in the alteration of DNA structure by dnaB protein in priming replication. J Biol Chem 256:5260–5266

    CAS  PubMed  Google Scholar 

  • Arai K, Kornberg A (1981b) Mechanism of dnaB protein action. IV. General priming of DNA replication by dnaB protein and primase compared with RNA polymerase. J Biol Chem 256:5267–5272

    CAS  PubMed  Google Scholar 

  • Arai K, Low RL, Kornberg A (1981) Movement and site selection for priming by the primosome in phage ϕX174 DNA replication. Proc Natl Acad Sci USA 78:707–711

    CAS  PubMed  Google Scholar 

  • Beppu T (1995) Signal transduction and secondary metabolism: prospects for controlling productivity. Trends Biotechnol 13:264–269

    CAS  PubMed  Google Scholar 

  • Birch P, Khan SA (1992) Replication of single-stranded plasmid pT181 DNA in vitro. Proc Natl Acad Sci USA 89:290–294

    CAS  PubMed  Google Scholar 

  • Boe L, Gros MF, te Riele H, Ehrlich SD, Gruss A (1989) Replication origins of single-stranded-DNA plasmid pUB110. J Bacteriol 171:3366–3372

    CAS  PubMed  Google Scholar 

  • Bruand C, Ehrlich SD, Jannière L (1995) Primosome assembly site in Bacillus subtilis. EMBO J 11:2642–2650

    Google Scholar 

  • Conrad SE, Campbell JL (1979) Characterization of an improved in vitro DNA replication system for Escherichia coli plasmids. Nucl Acids Res 6:3289–3303

    CAS  Google Scholar 

  • Dempsey LA, Zhao AC, Khan SA (1995) Localization of the start sites of lagging-strand replication of rolling-circle plasmids from gram-positive bacteria. Mol Microbiol 15:679–687

    CAS  PubMed  Google Scholar 

  • Deng ZT, Kieser T, Hopwood DA (1988) “Strong incompatibility” between derivatives of the Streptomyces multi-copy plasmid pIJ101. Mol Gen Genet 214:286–294

    CAS  PubMed  Google Scholar 

  • Fuller RS, Kaguni JM, Kornberg A (1981) Enzymatic replication of the origin of the Escherichia coli chromosome. Proc Natl Acad Sci USA 78:7370–7374

    CAS  PubMed  Google Scholar 

  • Gruss A, Ehrlich SD (1989) The family of highly interrelated single-stranded deoxyribonucleic acid plasmids. Microbiol Rev 53:231–241

    CAS  PubMed  Google Scholar 

  • Gruss A, Ross HF, Novick RP (1987) Functional analysis of a palindromic sequence required for normal replication of several staphylococcal plasmids. Proc Natl Acad Sci USA 84:2165–2169

    CAS  PubMed  Google Scholar 

  • Hagège J, Pernodet JL, Friedmann A, Guérineau M (1993) Mode and origin of replication of pSAM2, a conjugative integrating element of Streptomyces ambofaciens. Mol Microbiol 10:799–812

    PubMed  Google Scholar 

  • Hopwood DA, Bibb MJ, Chater KF, Kieser T, Bruton CJ, Kieser HM, Lydiate DJ, Smith CP, Ward JM, Schrempf H (1985) Genetic manipulation of Streptomyces: a laboratory manual. The John Innes Foundation, Norwich, UK

    Google Scholar 

  • Inuzuka M, Helinski DR (1978) Replication of antibiotic resistance plasmid R6K DNA in vitro. Biochemistry 17:2567–2573

    CAS  PubMed  Google Scholar 

  • Jannière L, Gruss A, Ehrlich SD (1993) Plasmids. In: Sonenshein AL, Losick R, Hoch JA (eds) Bacillus subtilis and other gram positive bacteria: biochemistry, physiology, and molecular genetics. American Society for Microbiology, Washington DC, pp 625–644

  • Kaguni JM, Kornberg A (1982) The ρ subunit of RNA polymerase holoenzyme confers specificity in priming M13 viral DNA replication. J Biol Chem 257: 5437–5443

    CAS  PubMed  Google Scholar 

  • Kataoka M, Seki T, Yoshida, T (1991) Five genes involved in self-transmission of pSN22, a Streptomyces plasmid. J Bacteriol 173:4220–4228

    CAS  PubMed  Google Scholar 

  • Kataoka M, Kiyose YM, Michisuji Y, Horiguchi T, Seki T, Yoshida T (1994a) Complete nucleotide sequence of the Streptomyces plasmid, pSN22; genetic organization and correlation with genetic properties. Plasmid 32:55–69

    Article  CAS  PubMed  Google Scholar 

  • Kataoka M, Kuno N, Horiguchi T, Seki T, Yoshida T (1994b) Replication of the Streptomyces plasmid pSN22 through single-stranded intermediates. Mol Gen Genet 242:130–136

    CAS  PubMed  Google Scholar 

  • Katz E, Thompson CJ, Hopwood, DA (1983) Cloning and expression of the tyrosinase gene from Streptomyces antibioticus in Streptomyces lividans. J Gen Microbiol 129:2703–2714

    CAS  PubMed  Google Scholar 

  • Khan SA (1997) Rolling-circle replication of bacterial plasmids. Microbiol Mol Biol Rev 61:442–455

    CAS  PubMed  Google Scholar 

  • Kieser T, Hopwood DA, Wright HM, Thompson CJ (1982) pIJ101, a multi-copy broad host-range Streptomyces plasmid: functional analysis and development of DNA cloning vectors. Mol Gen Genet 185:223–238

    CAS  PubMed  Google Scholar 

  • Kornberg A, Baker TA (1992) DNA replication, 2nd edn. WH Freeman & Co, New York

  • Kramer MG, Khan SA, Espinosa M (1997) Plasmid rolling circle replication: identification of the RNA polymerase-directed primer RNA and requirement for DNA polymerase I for lagging strand synthesis. EMBO J. 16:5784–5795

    Google Scholar 

  • Kramer MG, Espinosa M, Misra TK, Khan SA (1998) Lagging strand replication of rolling-circle plasmids: specific recognition of the ssoA-type origins in different gram-positive bacteria. Proc Natl Acad Sci USA 95:10505–10510

    Article  CAS  PubMed  Google Scholar 

  • Leenhouts KJ, Tolner B, Bron S, Kok J, Venema G, Seegers JFML (1991) Nucleotide sequence and characterization of the broad-host-range lactococcal plasmid pWVO1. Plasmid 26:55–66

    CAS  PubMed  Google Scholar 

  • Muth G, Farr M, Hartmann V, Wohlleben W (1995) Streptomyces ghanaensis plasmid pSG5: nucleotide sequence analysis of the self-transmissible minimal replicon and characterization of the replication mode. Plasmid 33:113–126

    Article  CAS  PubMed  Google Scholar 

  • Novick RP (1989) Staphylococcal plasmids and their replication. Annu Rev Microbiol 43:537–565

    Article  CAS  PubMed  Google Scholar 

  • Pigac J, Vujaklija D, Toman Z, Gamulin V, Schrempf H (1988) Structural instability of a bifunctional plasmid pZG1 and single-stranded DNA formation in Streptomyces. Plasmid 19:222–230

    CAS  PubMed  Google Scholar 

  • te Riele H, Michel B, Ehrlich SD (1986a) Single-stranded plasmid DNA in Bacillus subtilis and StaphylococcuStaphylococcus aureus. Proc Natl Acad Sci USA 83:2541–2545

    PubMed  Google Scholar 

  • te Riele, H, Michel B, Ehrlich SD (1986b) Are single-stranded circular intermediates involved in plasmid DNA replication? EMBO J 5:631–637

    PubMed  Google Scholar 

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

    Google Scholar 

  • Seegers JFML, Zhao AC, Meijer WJJ, Khan SA, Venema G, Bron S (1995) Structural and functional analysis of the single-strand origin of replication from the lactococcal plasmid pWVO1. Mol Gen Genet 249:43–50

    CAS  PubMed  Google Scholar 

  • Servín-González L, Sampieri AIII, Cabello J, Galván L, Juárez V, Castro C (1995) Sequence and functional analysis of the Streptomyces phaeochromogenes plasmid pJV1 reveals a modular organization of Streptomyces plasmid that replicate by rolling circle. Microbiol 141:2499–2510

    CAS  PubMed  Google Scholar 

  • del Solar GH, Moscoso M, Espinosa M. (1993) Rolling-circle replicating plasmids from gram-positive and gram-negative bacteria: a wall falls. Mol Microbiol 8:789–796

    PubMed  Google Scholar 

  • Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517

    CAS  PubMed  Google Scholar 

  • Studier FW, Moffatt BA (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189:113–130

    PubMed  Google Scholar 

  • Suzuki I, Kataoka M, Seki T, Yoshida T (1997a) Three single strand origins located on both strands of the Streptomyces rolling circle plasmid pSN22. Plasmid 37:51–64

    Article  CAS  PubMed  Google Scholar 

  • Suzuki I, Seki T, Yoshida T (1997b) Nucleotide sequence of a nicking site of the Streptomyces plasmid pSN22 replicating by the rolling circle mechanism. FEMS Microbiol Lett 150:283–288

    Article  CAS  PubMed  Google Scholar 

  • Thompson J, Cundliffe E (1981) Purification and properties of an RNA methylase produced by Streptomyces azureus and involved in resistance to thiostrepton. J Gen Microbiol 124:291–297

    CAS  Google Scholar 

  • Thompson CJ, Ward JM, Hopwood DA (1982) Cloning of antibiotic resistance and nutritional genes in Streptomycetes. J Bacteriol 151:668–677

    CAS  PubMed  Google Scholar 

  • Thompson J, Rae S, Cundliffe E (1984) Coupled transcription-translation in extracts of Streptomyces lividans. Mol Gen Genet 195:39–43

    CAS  PubMed  Google Scholar 

  • Yanisch-Perron C, Vieira J, Messing J (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119

    PubMed  Google Scholar 

  • Yokoyama E, Doi K, Kimura M, Ogata S (1996) Detection of the single-stranded DNA of Streptomyces plasmid pSA1.1 and a binding histone-like protein. FEMS Microbiol Lett 138:197–200

    Article  CAS  PubMed  Google Scholar 

  • Zaman S, Radnedge L, Richards H, Ward, JM (1993) Analysis of the site for second-strand initiation during replication of the Streptomyces plasmid pIJ101. J Gen Microbiol 139:669–676

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We greatly thank to Drs. T. Kieser, H. Araki and T. Ito for valuable discussions; Dr E. Ko-Mitamura for editorial suggestions and manuscript corrections; and Dr H. Masai for valuable comments on the general priming of E. coli.

Author information

Author notes

  1. Ichiro Suzuki

    Present address: Department of Chemical Engineering Science, Graduate School of Engineering, Yokohama National University, 79-5 Tokiwadai, Hodogaya, Yokohama, 240-8501, Japan

Authors and Affiliations

  1. The International Center for Biotechnology, Osaka University, 2-1 Yamada-oka, Suita, Osaka, 565-0871, Japan

    Ichiro Suzuki, Masakazu Kataoka, Toshiomi Yoshida & Tatsuji Seki

  2. Department of Environmental Science and Technology, Faculty of Engineering, Shinshu University, Wakasato 4-17-1, Nagano, 380-8553, Japan

    Masakazu Kataoka

Authors
  1. Ichiro Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masakazu Kataoka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Toshiomi Yoshida
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tatsuji Seki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Masakazu Kataoka.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Suzuki, I., Kataoka, M., Yoshida, T. et al. Lagging strand replication of rolling-circle plasmids in Streptomyces lividans: an RNA polymerase-independent primer synthesis. Arch Microbiol 181, 305–313 (2004). https://doi.org/10.1007/s00203-004-0656-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-004-0656-6

Keywords

Search

Navigation