Skip to main content
SpringerLink
Log in

Site-specific recombination systems in filamentous phages

  • Review
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Since the discovery of the integration mechanism of the filamentous phage CTXϕ of Vibrio cholerae, integrating filamentous phages have been discovered to be more abundant and diverse than previously recognized. However, the integration systems of filamentous phages have not been fully investigated. The present review provides a short overview on the different strategies employed by filamentous bacteriophages for integration into the host chromosome. This is the first review to describe the diversity of site-specific recombination in filamentous phages.

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

Similar content being viewed by others

References

  • Addy HS, Askora A, Kawasaki T, Fujie M, Yamada T (2012) Loss of virulence of the phytopathogen Ralstonia solanacearum through infection by ϕRSM filamentous phages. Phytopathology 105(5). doi:1094/PHYTO-11-11-0319-R

  • Armstrong J, Perham RN, Walker JE (1981) Domain structure of the bacteriophage fd adsorption protein. FEBS Lett 135:167–172

    Article  PubMed  CAS  Google Scholar 

  • Askora A, Kawasaki T, Usami S, Fujie M, Yamada T (2009) Host recognition and integration of filamentous phage ϕRSM in the phytopathogen, Ralstonia solanacearum. Virology 384:69–76

    Article  PubMed  CAS  Google Scholar 

  • Askora A, Kawasaki T, Fujie M, Yamada T (2011) Resolvase-like serine recombinase mediates integration/excision in the bacteriophage ϕRSM. J Biosci Bioeng 111:109–116

    Article  PubMed  CAS  Google Scholar 

  • Barre FX, Sherratt DJS (2002) Xer site-specific recombination: promoting chromosome segregation. In: Craig NL, Craigie R, Gellert M, Lambowitz A (eds) Mobile DNA II, vol 1. American Society of Microbiology, Washington, DC, pp 149–161

    Google Scholar 

  • Bibb LA, Hancox MI, Hatfull GF (2005) Integration and excision by the large serine recombinase ϕRv1 integrase. Mol Microbiol 55:1896–1910

    Article  PubMed  CAS  Google Scholar 

  • Bille E, Zahar JR, Perrin A, Morelle S, Kriz P, Jolley KA, Maiden MCJ, Dervin C, Nassif X, Tinsley CR (2005) A chromosomally integrated bacteriophage in invasive meningococci. J Exp Med 201:1905–1913

    Article  PubMed  CAS  Google Scholar 

  • Biswas T, Aihara H, Radman-Livaja M, Filman D, Landy A, Ellenberger T (2005) A structural basis for allosteric control of DNA recombination by lambda integrase. Nature 435:1059–1066

    Article  PubMed  CAS  Google Scholar 

  • Blakely G, May G, McCulloch R, Arciszewska LK, Burke M, Lovett ST, Sherratt DJ (1993) Two related recombinases are required for site-specific recombination at dif and cer in E. coli K12. Cell 75:351–361

    Article  PubMed  CAS  Google Scholar 

  • Campbell A (1962) Episomes. Adv Genet 11:101–145

    Article  Google Scholar 

  • Campos J, Martinez E, Suzarte E, Rodriguez BL, Marrero K, Silva Y, Ledon T, del Sol R, Fando R (2003) VGJϕ, a novel filamentous phage of Vibrio cholerae, integrates into the same chromosomal site as CTXϕ. J Bacteriol 185:5685–5696

    Article  PubMed  CAS  Google Scholar 

  • Campos J, Martinez E, Izquierdo Y, Fando R (2010) VEJϕ, a novel filamentous phage of Vibrio cholerae able to transduce the cholera toxin genes. Microbiology 156:108–115

    Article  PubMed  CAS  Google Scholar 

  • Colloms SD, Sykora P, Szatmari G, Sherratt DJ (1990) Recombination at ColE1 cer requires the Escherichia coli xerC gene product, a member of the lambda integrase family of site-specific recombinases. J Bacteriol 172:6973–6980

    PubMed  CAS  Google Scholar 

  • Das B, Bischerour J, Val ME, Barre FX (2010) Molecular keys of the tropism of integration of the cholera toxin phage. Proc Natl Acad Sci USA 107:4377–4382

    Article  PubMed  CAS  Google Scholar 

  • de Mello Varani A, Souza RC, Nakaya HI, de Lima WC, de Almeid P, Watabnabe-Kitajima E, Chen J, Civerelo E, Vasconceliss ATR, Van Sluys MA (2008) Origins of the Xylella fastidiosa prophage-like regions and their impact in genome differentiation. PLoS ONE 3(12):e4059

    Article  PubMed  Google Scholar 

  • Deng LW, Malik P, Perham PN (1999) Interaction of the globular domains of pIII protein of filamentous bacteriophage fd with the F-pilus of Escherichia coli. Virology 253:271–277

    Article  PubMed  CAS  Google Scholar 

  • Gabriel K, Schmid H, Schmidt U, Rausch H (1995) The actinophage RP3 DNA integrates site-specifically into the putative tRNA (Arg) (AGG) gene of Streptomyces rimosus. Nucleic Acid Res 23:58–63

    Article  PubMed  CAS  Google Scholar 

  • Grindley NDF, Whiteson KL, Rice PA (2006) Mechanisms of site-specific recombination. Annu Rev Biochem 75:567–605

    Article  PubMed  CAS  Google Scholar 

  • Hatfull GF, Grindley NDF (1988) Resolvases and DNA invertases: a family of enzymes active in site-specific recombination. In: Kucherlapati R, Smith S (eds) Genetic recombination. ASM Press, Washington, DC, pp 357–396

    Google Scholar 

  • Hill DF, Short J, Perharm NR, Petersen GB (1991) DNA sequence of the filamentous bacteriophage Pf1. J Mol Biol 218:349–364

    Article  PubMed  CAS  Google Scholar 

  • Huber KE, Waldor MK (2002) Filamentous phage integration requires the host recombinases XerC and XerD. Nature 417:656–659

    Article  PubMed  CAS  Google Scholar 

  • Jacobson A (1972) Role of F pili in the penetration of bacteriophage fl. J Virol 10:835–843

    PubMed  CAS  Google Scholar 

  • Kawai M, Uchiyama I, Kobayashi I (2005) Genomic comparison in silico in Neisseria suggests integration of filamentous bacteriophages by their own transposase. DNA Res 12:389–401

    Article  PubMed  CAS  Google Scholar 

  • Kawasaki T, Nagata S, Fujiwara A, Satsuma H, Fujie M, Usami S, Yamada T (2007) Genomic characterization of the filamentous integrative bacteriophage ϕRSS1 and ϕRSM1, which infect Ralstonia solanacearum. J Bacteriol 189:5792–5802

    Article  PubMed  CAS  Google Scholar 

  • Kitts P, Richet E, Nash HA (1984) Lambda integrative recombination: supercoiling, synapsis, and strand exchange. Cold Spring Harb Symp Quant Biol 49:735–744

    Article  PubMed  CAS  Google Scholar 

  • Lesterlin C, Barre FX, Cornet F (2004) Genetic recombination and the cell cycle: what we have learned from chromosome dimers. Mol Microbiol 54:1151–1160

    Article  PubMed  CAS  Google Scholar 

  • Marvin DA (1998) Filamentous phage structure, infection and assembly. Curr Opin Struc Biol 8:150–158

    Article  CAS  Google Scholar 

  • McLeod SM, Waldor MK (2004) Characterization of XerC- and XerD-dependent CTX phage integration in Vibrio cholerae. Mol Microbiol 54:935–947

    Article  PubMed  CAS  Google Scholar 

  • Model P, Russel M (1988) Filamentous bacteriophages. In: Calendar R (ed) The bacteriophages, vol 2. Plenum Press, New York, pp 375–456

    Chapter  Google Scholar 

  • Mooij MJ, Drenkard E, Llamas MA, Vandenbroucke-Grauls CMJE, Savelkoul PHM, Ausubel FM, Bitter W (2007) Characterization of the integrated filamentous phage Pf5 and its involvement in small-colony formation. Microbiology 153:1790–1798

    Article  PubMed  CAS  Google Scholar 

  • Mumm JP, Landy A, Gelles J (2006) Viewing single lambda site-specific recombination events from start to finish. EMBO J 25:4586–4595

    Article  PubMed  CAS  Google Scholar 

  • Nash HA (1996) Site-specific recombination: integration, excision, resolution and inversion of defined DNA segments. In: Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella. ASM Press, Washington, DC, pp 2363–2376

    Google Scholar 

  • Nunes-Düby SE, Kwon HJ, Tirumalai RS, Ellenberger T, Landy A (1998) Similarities and differences among 105 members of the Int family of site-specific recombinases. Nucleic Acids Res 26:391–406

    Article  PubMed  Google Scholar 

  • Russel M, Model P (1989) Genetic analysis of the filamentous bacteriophage packaging signal and the proteins that interact with it. J Virol 63:3284–3295

    PubMed  CAS  Google Scholar 

  • Sadowski PD (1993) Site-specific genetic recombination: hops, flips, and flops. FASEB J 7:760–767

    PubMed  CAS  Google Scholar 

  • Segall AM, Craig NL (2005) New wrinkles and folds in site-specific recombination. Mol Cell 19:433–435

    Article  PubMed  CAS  Google Scholar 

  • Sherratt DJ, Arciszewska LK, Blakely G, Colloms S, Grant K, Leslie N, McCulloch R (1995) Site-specific recombination and circular chromosome segregation. Phil Trans R Soc Lond (B) 347:37–42

    Article  CAS  Google Scholar 

  • Smith MC, Thorpe HM (2002) Diversity in the serine recombinases. Mol Microbiol 44:299–307

    Article  PubMed  CAS  Google Scholar 

  • Stark WM, Boocock MR, Sherrat DJ (1992) Catalysis by site-specific recombinases. Trends Genet 8:432–439

    Article  PubMed  CAS  Google Scholar 

  • Sun X, Mierke DF, Biswas T, Lee SY, Landy A, Radman-Livaja M (2006) Architecture of the 99 bp DNA-six-protein regulatory complex of the lambda att site. Mol Cell 24:569–580

    Google Scholar 

  • Val ME, Bouvier M, Campos J, Sherratt D, Cornet F, Mazel D, Barre FX (2005) The single-stranded genome of phage CTX is the form used for integration into the genome of Vibrio cholerae. Mol Cell 19:559–565

    Article  PubMed  CAS  Google Scholar 

  • Waldor MK, Mekalanos JJ (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:1910–1914

    Article  PubMed  CAS  Google Scholar 

  • Warren D, Lee SY, Landy A (2005) Mutations in the amino-terminal domain of lambda-integrase have differential effects on integrative and excisive recombination. Mol Microbiol 55:1104–1112

    Article  PubMed  CAS  Google Scholar 

  • Webb JS, Lau M, Kjelleberg S (2004) Bacteriophage and phenotypic variation in Pseudomonas aeruginosa biofilm development. J Bacteriol 186:8066–8073

    Article  PubMed  CAS  Google Scholar 

  • Yamada T (2012) Bacteriophages of Ralstonia solanacearum: their diversity and utilization as biocontrol agents in agriculture. In: Kurtboke I (ed) Bacteriophages. InTech Open Access Publisher, Croatia, pp 113–139

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany, Faculty of Science, Zagazig University, Zagazig, 44519, Egypt

    Ahmed Askora & M. E. F. Abdel-Haliem

  2. Department of Molecular Biotechnology, Graduate School of Advanced Sciences of Matter, Hiroshima University, Higashi-Hiroshima, 739-8530, Japan

    Takashi Yamada

Authors
  1. Ahmed Askora
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. E. F. Abdel-Haliem
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takashi Yamada
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ahmed Askora.

Additional information

Communicated by A. Aguilera.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Askora, A., Abdel-Haliem, M.E.F. & Yamada, T. Site-specific recombination systems in filamentous phages. Mol Genet Genomics 287, 525–530 (2012). https://doi.org/10.1007/s00438-012-0700-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-012-0700-1

Keywords

Search

Navigation