Skip to main content
SpringerLink
Log in

Characterization of Pectobacterium carotovorum subsp. carotovorum Bacteriophage PP16 Prospective for Biocontrol of Potato Soft Rot

  • EXPERIMENTAL ARTICLES
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

Phages of the phytopathogenic Pectobacteriaceae species causing black leg and soft rot of potato were investigated. These phages are promising as biocontrol agents to prevent the loss of seed and ware potato tubers. The present work characterizes a new podovirus PP16, infecting a broad range of Pectobacterium carotovorum strains. Based on its genomic composition, phage PP16 was assigned to a separate phylogenetic branch of the genus Phimunavirus, subfamily Autographivirinae. Bacteriophage PP16 efficiently inhibited development of bacterial infection both in vitro and in planta. The field experiment demonstrated a substantial increase of plant germination after the treatment of seed potato with phage PP16.

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. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.

Similar content being viewed by others

REFERENCE

  1. Ackermann H.-W. Basic phage electron microscopy, in Bacteriophages: Methods and Protocols, 2009, vol. 1, pp. 113–126. https://doi.org/10.1007/978-1-60327-164-6

    Google Scholar 

  2. Adeolu, M., Alnajar, S., Naushad, S., and Gupta, R.S., Genome-based phylogeny and taxonomy of the ‘Enterobacteriales’: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Int. J. Syst. Evol. Microbiol., 2016, vol. 66, pp. 5575–5599. https://doi.org/10.1099/ijsem.0.001485

    Article  CAS  PubMed  Google Scholar 

  3. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J., Gapped BLAST and PSI-BLAST: a new generation of protein database search programs, Nucl. Acids Res., 1997, vol. 25, pp. 3389–3402. https://doi.org/10.1093/nar/25.17.3389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Balogh, B., Jones, J.B., Iriarte, F.B., and Momol, M.T., Phage therapy for plant disease control, Curr. Pharm. Biotechnol., 2010, vol. 11, pp. 48–57. https://doi.org/10.2174/138920110790725302

    Article  CAS  PubMed  Google Scholar 

  5. Bankevich, A., Nurk, S., Antipov, D., Gurevich, A.A., Dvorkin, M., Kulikov, A.S., Lesin, V.M., Nikolenko, S.I., Pham, S., Prjibelski, A.D., Pyshkin, A.V., Sirotkin, A.V., Vyahhi, N., Tesler, G., Alekseyev, M.A., and Pevzner, P.A., SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing, J. Computat. Biol., 2012, vol. 19, pp. 455–477. https://doi.org/10.1089/cmb.2012.0021

    Article  CAS  Google Scholar 

  6. Besemer, J., Lomsadze, A., and Borodovsky, M., GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions, Nucl. Acids Res., 2001, vol. 29, pp. 2607–2618. doi: 11410670

  7. Buttimer, C., Lucid, A., Neve, H., Franz, C.M.A.P., O’Mahony, J., Turner, D., Lavigne, R., and Coffey, A., Pectobacterium atrosepticum phage VB_PatP_CB5: a member of the proposed genus “Phimunavirus”, Viruses, 2018, vol. 10. pii: E394. https://doi.org/10.3390/v10080394

    Article  CAS  PubMed  Google Scholar 

  8. Clokie, M.R.J. and Kropinski, A.M., Bacteriophages: Methods and Protocols, vol. 1: Isolation, Characterization, and Interactions, in Methods in Molecular Biology, Humana, 2009. https://doi.org/10.1007/978-1-60327-164-6

  9. Czajkowski, R., Ozymko, Z., de Jager, V., Siwinska, J., Smolarska, A., Ossowicki, A., Narajczyk, M., and Lojkowska, E., Genomic, proteomic and morphological characterization of two novel broad host lytic bacteriophages ΦPD10.3 and ΦPD23.1 infecting pectinolytic Pectobacterium spp. and Dickeya spp., PLoS One, 2015, vol. 10, article e0119812. https://doi.org/10.1371/journal.pone.0119812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Dees, M.W., Lysøe, E., Rossmann, S., Perminow, J., and Brurberg, M.B., Pectobacterium polaris sp. nov., isolated from potato (Solanum tuberosum), Int. J. Syst. Evol. Microbiol., 2017, vol. 67, pp. 5222–5529. https://doi.org/10.1099/ijsem.0.002448

    Article  CAS  PubMed  Google Scholar 

  11. Eriksson, H., Maciejewska, B., Latka, A., Majkowska-Skrobek, G., Hellstrand, M., Melefors, Ö., Wang, J.-T., Kropinski, A.M., Drulis-Kawa, Z., and Nilsson, A.S., A suggested new bacteriophage genus, ‘Kp34likevirus’, within the Autographivirinae subfamily of Podoviridae, Viruses, 2015, vol. 7, pp. 1804–1822. https://doi.org/10.3390/v7041804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Finn, R.D., Clements, J., and Eddy, S.R., HMMER web server: interactive sequence similarity. searching, Nucl. Acids Res., 2011, vol. 39, suppl. 2. https://doi.org/10.1093/nar/gkr367

  13. Gardan, L., Gouy, C., Christen, R., and Samson, R., Elevation of three subspecies of Pectobacterium carotovorum to species level: Pectobacterium atrosepticum sp. nov., Pectobacterium betavasculorum sp. nov. and Pectobacterium wasabiae sp. nov., Int. J. Syst. Evol. Microbiol., 2003, vol. 53, pp. 381–391. https://doi.org/10.1099/ijs.0.02423-0

    Article  CAS  PubMed  Google Scholar 

  14. Hirata, H., Kashihara, M., Horiike, T., Suzuki, T., Dohra, H., Netsu, O., and Tsuyumu, S., Genome sequence of Pectobacterium Carotovorum phage PPWS1, isolated from Japanese horseradish [Eutrema Japonicum (Miq.) Koidz] showing soft-rot symptoms, Genome Announc., 2016, vol. 4, no. 2. pii: e01625-15. https://doi.org/10.1128/genomeA.01625-15

    Article  PubMed  PubMed Central  Google Scholar 

  15. Humphris, S.N., Cahill, G., Elphinstone, J.G., Kelly, R., Parkinson, N.M., Pritchard, L., Toth, I.K., and Saddler, G.S., Detection of the bacterial potato pathogens Pectobacterium and Dickeya spp. using conventional and real-time PCR, in Methods in Molecular Biology, Clifton, NJ, 2015, pp. 1–16. https://doi.org/10.1007/978-1-4939-2620-6_1

  16. Lavigne, R., Sun, W.D., and Volckaert, V., PHIRE, a deterministic approach to reveal regulatory elements in bacteriophage genomes, Bioinformatics, 2004, vol. 20, pp. 629–635. https://doi.org/10.1093/bioinformatics/btg456

    Article  CAS  PubMed  Google Scholar 

  17. Lavigne, R., Seto, D., Mahadevan, P., Ackermann, H.-W., and Kropinski, A.M., Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools, Res. Microbiol., 2008, vol. 159, pp. 406–414. https://doi.org/10.1016/j.resmic.2008.03.005

    Article  CAS  PubMed  Google Scholar 

  18. Lim, J.A., Heu, S., Park, J., and Roh, E., Genomic characterization of bacteriophage VB_PcaP_PP2 infecting Pectobacterium carotovorum subsp. carotovorum, a new member of a proposed genus in the subfamily Autographivirinae, Arch. Virol., 2017, vol. 162, pp. 2441–2444. https://doi.org/10.1007/s00705-017-3349-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P., Dow, M., Verdier, V., Beer, S.V., Machado, M.A., Toth, I., Salmond, G., and Foster, G.D., Top 10 plant pathogenic bacteria in molecular plant pathology, Mol. Plant Pathol., 2012, vol. 13, pp. 614–629. https://doi.org/10.1111/j.1364-3703.2012.00804.x

    Article  PubMed  PubMed Central  Google Scholar 

  20. Martin, B., Humbert, O., Camara, M., Guenzi, E., Walker, J., Mitchell, T., Andrew, P., Prudhomme, M., Alloing, G., Hakenbeck, R., Morrison, D.A., Boulnois, G.J., and Claverys, J.-P., A highly conserved repeated DNA element located in the chromosome of Streptococcus pneumoniae, Nucl. Acids Res., 1992, vol. 20, pp. 3479–3483. https://doi.org/10.1093/nar/20.13.3479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Meier-Kolthoff, J.P. and Göker, M., VICTOR: Genome-based phylogeny and classification of prokaryotic viruses, Bioinformatics, 2017, vol. 33, pp. 3396–3404. https://doi.org/10.1093/bioinformatics/btx440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Pérombelon, M.C.M., Potato diseases caused by soft rot erwinias: an overview of pathogenesis, Plant Pathol., 2002, vol. 51, pp. 1–12. https://doi.org/10.1046/j.0032-0862.2001

    Article  Google Scholar 

  23. Prokhorov, N.S., Riccio, C., Zdorovenko, E.L., Shneider, M.M., Browning, C., Knirel, Y.A., Leiman, P.G., and Letarov, A.V., Function of bacteriophage G7C esterase tailspike in host cell adsorption, Mol. Microbiol., 2017, vol. 105, pp. 385–398. https://doi.org/10.1111/mmi.13710

    Article  CAS  PubMed  Google Scholar 

  24. Roucourt, B. and Lavigne, R., The role of interactions between phage and bacterial proteins within the infected cell: a diverse and puzzling interactome, Environ. Microbiol., 2009, vol. 11, pp. 2789–2805. https://doi.org/10.1111/j.1462-2920.2009.02029.x

    Article  CAS  PubMed  Google Scholar 

  25. Sambrook, J., Fritsch, E.F., and Maniatis, T., Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, 1989.

    Google Scholar 

  26. Sarfraz, S., Riaz, K., Oulghazi, S., Cigna, J., Sahi, S.T., Khan, S.H., and Faure, D., Pectobacterium punjabense sp. nov., isolated from blackleg symptoms of potato plants in Pakistan, Int. J. Syst. Evol. Microbiol., 2018, vol. 68, pp. 3551–3556. https://doi.org/10.1099/ijsem.0.003029

    Article  CAS  PubMed  Google Scholar 

  27. Shirshikov, F.V., Korzhenkov, A.A., Miroshnikov, K.K., Kabanova, A.P., Barannik, A.P., Ignatov, A.N., and Miroshnikov, K.A., Draft genome sequences of new genomospecies “Candidatus Pectobacterium maceratum” strains, which cause soft rot in plants, Genome Announc., 2018, vol. 6, article e00260-18. https://doi.org/10.1128/genomeA.00260-18

    Article  PubMed  PubMed Central  Google Scholar 

  28. Waleron, M., Misztak, A., Waleron, M., Franczuk, M., Wielgomas, B., and Waleron, K., Transfer of Pectobacterium carotovorum subsp. carotovorum strains isolated from potatoes grown at high altitudes to Pectobacterium peruviense sp. nov., Syst. Appl. Microbiol., 2018, vol. 41, pp. 85–93. https://doi.org/10.1016/J.SYAPM.2017.11.005

    Article  PubMed  Google Scholar 

  29. Yagodin, B.A., Zhukov, Yu.P., and Kobzarenko, V.I., Agrokhimiya (Agochemistry), Moscow: Kolos, 2002.

    Google Scholar 

  30. Young, R., Phage lysis: three steps, three choices, one outcome, J. Microbiol., 2014, vol. 52, pp. 243–258. https://doi.org/10.1007/s12275-014-4087-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

The research, except for the study of bacteriophage morphology, was supported by the grant of the Russian Science Foundation no. 16-16-00073.

Author information

Authors and Affiliations

  1. PhytoEngineering Research Center, 141880, Rogachevo, Moscow region, Russia

    M. V. Voronina, E. N. Bugaeva, D. M. Vasiliev, A. P. Kabanova, A. N. Ignatov & K. A. Miroshnikov

  2. Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997, Moscow, Russia

    A. P. Kabanova, A. P. Barannik, M. M. Shneider & K. A. Miroshnikov

  3. Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences, 119071, Moscow, Russia

    E. E. Kulikov & S. V. Toschakov

  4. Kant Baltic Federal University, 236041, Kaliningrad,, Russia

    A. A. Korzhenkov & S. V. Toschakov

  5. Kurchatov Institute, 123098, Moscow, Russia

    A. A. Korzhenkov

Authors
  1. M. V. Voronina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. N. Bugaeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. M. Vasiliev
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. P. Kabanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. P. Barannik
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. M. Shneider
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. E. E. Kulikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. A. A. Korzhenkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. S. V. Toschakov
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. A. N. Ignatov
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. K. A. Miroshnikov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. A. Miroshnikov.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by E. Makeeva

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Voronina, M.V., Bugaeva, E.N., Vasiliev, D.M. et al. Characterization of Pectobacterium carotovorum subsp. carotovorum Bacteriophage PP16 Prospective for Biocontrol of Potato Soft Rot. Microbiology 88, 451–460 (2019). https://doi.org/10.1134/S0026261719040118

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261719040118

Keywords:

Search

Navigation