Skip to main content

Filamentous Phages Affect Virulence of the Phytopathogen Ralstonia solanacearum

  • Chapter
  • First Online:
Biocommunication of Phages

Abstract

ϕRSS-type filamentous phages are frequently found integrated in Ralstonia solanacearum genomes and affect host virulence after infection. ϕRSS1, a known virulence-enhancing phage, was found to be a truncated form of a larger phage (designated as ϕRSS0; 7288 nt) integrated in strain C319. A 626-nt ϕRSS0 sequence missing in ϕRSS1 DNA contains a nucleotide sequence element attP, corresponding to dif of R. solanacearum. Thus, ϕRSS0 was integrated at a dif site, similarly to CTXϕ of Vibrio cholerae, which uses the host XerC/D recombination system. ϕRSS0 could integrate into both the chromosome and megaplasmid of the host genome. The extra region of ϕRSS0 also contained an open reading frame (ORF13) of 156 amino acids with sequence similarity to DNA-binding phage regulators. The ϕRSS0-attP is located within the ORF13-coding region; therefore, integration results in a truncation of the C-terminus of ORF13. ORF13 may function as a phage repressor for immunity, because strain C319 (a ϕRSS0 lysogen) is resistant to second infection by ϕRSS0. C319 is susceptible to ϕRSS1, thus ϕRSS1 (without ORF13) seems to be an escaped superinfective phage derived from ϕRSS0. The diversity and dynamic rearrangements of ϕRSS-type phages/prophages in R. solanacearum and their effects on host virulence are discussed.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Addy HS, Askora A, Kawasaki T, Fujie M, Yamada T (2012a) Loss of virulence of the phytopathogen Ralstonia solanacearum through infection by ϕRSM filamentous phages. Phytopathology 102:469–477

    Article  CAS  Google Scholar 

  • Addy HS, Askora A, Kawasaki T, Fujie M, Yamada T (2012b) The filamentous phage ϕRSS1 enhances virulence of phytopathogenic Ralstonia solanacearum on tomato. Phytopathology 102:244–251

    Article  Google Scholar 

  • Ahmad AA, Askora A, Kawaski T, Fujie M, Yamada T (2014) The filamentous phage XacF1 causes loss of virulence in Xanthomonas axonopodis pv. citri, the causative agent of citrus canker disease. Front Microbiol 5:321

    Article  Google Scholar 

  • Ahmad AA, Kawabe M, Askora A, Kawasaki T, Fujie M, Yamada T (2017) Dynamic integration and excision of filamentous phage XacF1 in Xanthomonas citri pv. citri, the causative agent of citrus canker disease. FEBS Open Bio 7:1715–1721

    Article  CAS  Google Scholar 

  • Askora A, Yamada T (2015) Two different evolutionary lines of filamentous phages in Ralstonia solanacearum; their effects on bacterial virulence. Front Genet 6:217. https://doi.org/10.3389/fgene.2015.00217

    Article  CAS  PubMed  PubMed Central  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  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Buchen-Osmond C (2003) Inoviridae. In: Oracle AZ (ed) ICTVdB-The Universal Virus Database, version 3. ICTVdB Management, The Earth Institute, Biosphere 2 Center, Columbia University

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Carney BF, Denny TP (1990) A cloned avirulence gene from Pseudomonas solanacearum determines incompatibility on Nicotiana tabacum at the host species level. J Bacteriol 172:4836–4843

    Article  CAS  Google Scholar 

  • Carnoy C, Roten C-A (2009) The dif/Xer recombination systems in Proteobacteria. PLoS ONE 4(9):e6531

    Article  Google Scholar 

  • Dai H, Chiang KS, Kuo TT (1980) Characterization of a new filamentous phage Cf from Xanthomonas citri. J Gen Virol 46:277–289

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Das B, Bischerour J, Barre F-X (2011) VGJϕ integration and excision mechanisms contribute to the genetic diversity of Vibrio cholerae epidemic strains. Proc Natl Acad Sci USA 108:2516–2521

    Article  CAS  Google Scholar 

  • Davis BM, Waldor MK (2003) Filamentous phages linked to virulence of Vibrio cholerae. Curr Opin Microbiol 6:35–42

    Article  CAS  Google Scholar 

  • Denny TP (2006) Plant pathogenic Ralstonia species. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, Amsterdam, pp 573–644

    Chapter  Google Scholar 

  • Gonzalez MD, Lichtensteiger CA, Caughlan R, Vimr ER (2002) Conserved filamentous prophage in Escherichia coli O18:K1:H7 and Yersinia pestis biovar. orientalis. J Bacteriol 184:6050–6055

    Article  CAS  Google Scholar 

  • Hayward AC (2000) Ralstonia solanacearum. In: Lederberg J (ed) Encyclopedia of microbiology, vol 4. Academic, San Diego, pp 32–42

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kang Y, Liu H, Genin S, Schell MA, Denny TP (2002) Ralstonia solanacearum requires type 4 pili to adhere to multiple surfaces and for natural transformation and virulence. Mol Microbiol 46:427–437

    Article  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

    Google Scholar 

  • Kuo TT, Chao YS, Lin YH, Lin BY, Liu LF, Feng TY (1987a) Integration of the DNA of filamentous bacteriophage Cf1t into the chromosomal DNA of its host. J Virol 61:60–65

    Article  CAS  Google Scholar 

  • Kuo TT, Lin YH, Huang CM, Chang SF, Dai D, Feng TY (1987b) The lysogenic cycle of the filamentous phage Cf1t from Xanthomonas campestris pv. citri. Virology 156:305–312

    Article  CAS  Google Scholar 

  • Kuo TT, Tan MS, Su MT, Yang MK (1991) Complete nucleotide sequence of filamentous phage Cf1c from Xanthomonas campestris pv. citri. Nucleic Acids Res 19:2498

    Article  CAS  Google Scholar 

  • Lin NT, Chang RY, Lee SJ, Tseng YH (2000) Plasmids carrying cloned fragments of RF DNA from the filamentous phage ϕLF can be integrated into the host chromosome via site-specific integration and homologous recombination. Mol Genet Genom 266:425–435

    Article  Google Scholar 

  • Moyer KE, Kimsey HH, Waldor MK (2001) Evidence for a rolling-circle mechanism of phage DNA synthesis from both replicative and integrated forms of CTXϕ. Mol Microbiol 41:311–323

    Article  CAS  Google Scholar 

  • Negishi H, Yamada T, Shiraishi T, Oku H, Tanaka H (1993) Pseudomonas solanacearum plasmid pJTPS1 mediates a shift from the pathogenic to nonpathogenic phenotype. Mol Plant-Microbe Interact 6:203–209

    Article  CAS  Google Scholar 

  • Simpson AJ, Reinach FC, Arruda P, Abreu FA, Acencio M, Alvarenga R et al (2000) The genome sequence of the plant pathogen Xylella fastidiosa. Nature 406:151–157

    Article  CAS  Google Scholar 

  • Vasse J, Genin S, Frey P, Boucher C, Brito B (2000) The hrpB and hrpG regulatory genes of Ralstonia solanacearum are required for different stages of the tomato root infection process. Mol Plant-Microbe Interact 13:259–267

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Yamada T (2013) Filamentous phages of Ralstonia solanacearum: double-edged swords for pahogenic bacteria. Front Microbiol 4:325. https://doi.org/10.3389/fmicb.2013.00325

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamada T, Kawasaki T, Nagata S, Fujiwara A, Usami S, Fujie M (2007) New bacteriophages that infect the phytopathogen Ralstonia solanacearum. Microbiology 153:2630–2639

    Article  CAS  Google Scholar 

  • Yamada T, Sato S, Ishikawa H, Fujiwara A, Kawasaki T, Fujie M, Ogata, H (2010) A jumbo phage infecting the phytopathogen Ralstonia solanacearumdefines a new lineage of the Myovirus family. Virology 398:135–147

    Google Scholar 

  • Yao J, Allen C (2007) The plant pathogen Ralstonia solanacearum needs aerotaxis for normal biofilm formation and interactions with its tomato host. J Bacteriol 189:6415–6424

    Article  CAS  Google Scholar 

  • Zinder ND, Horiuchi K (1985) Multiregulatory element of filamentous bacteriophages. Microbiol Rev 49:101–106

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takashi Yamada .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Tasaka, Y., Kawasaki, T., Yamada, T. (2020). Filamentous Phages Affect Virulence of the Phytopathogen Ralstonia solanacearum. In: Witzany, G. (eds) Biocommunication of Phages. Springer, Cham. https://doi.org/10.1007/978-3-030-45885-0_11

Download citation

Publish with us

Policies and ethics