Abstract
Soft rot is an economically significant disease in potato and one of the major threats to sustainable potato production. This study aimed at isolating lytic bacteriophages and evaluating methods for and the efficacy of applying phages to control potato soft rot caused by Pectobacterium carotovorum. Eleven bacteriophages isolated from soil and water samples collected in Wuhan, China, were used to infect P. carotovorum host strains isolated from potato tubers showing soft rot symptoms in Nakuru county, Kenya. The efficacy of the phages in controlling soft rot disease was evaluated by applying individual phage strains or a phage cocktail on potato slices and tubers at different time points before or after inoculation with a P. carotovorum strain. The phages could lyse 20 strains of P. carotovorum, but not Pseudomonas fluorescens control strains. Among the 11 phages, Pectobacterium phage Wc5r, interestingly showed cross-activity against Pectobacterium atrosepticum and two phage-resistant P. carotovorum strains. Potato slice assays showed that the phage concentration and timing of application are crucial factors for effective soft rot control. Phage cocktail applied at a concentration of 1 × 109 plaque-forming units per milliliter before or within an hour after bacterial inoculation on potato slices, resulted in ≥ 90% reduction of soft rot symptoms. This study provides a basis for the development and application of phages to reduce the impact of potato soft rot disease.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adriaenssens EM, Van Vaerenbergh J, Vandenheuvel D, Dunon V, Ceyssens P-J, De Proft M, Kropinski AM, Noben J-P, Maes M, Lavigne R (2012) T4-related bacteriophage LIMEstone isolates for the control of soft rot on potato caused by ‘Dickeya solani’. PLoS ONE 7:e33227
Buttimer C, McAuliffe O, Ross RP, Hill C, O’Mahony J, Coffey A (2017) Bacteriophages and bacterial plant diseases. Front Microbiol. https://doi.org/10.3389/fmicb.2017.00034
Chan BK, Abedon ST (2012) Phage therapy pharmacology: phage cocktails. Adv Appl Microbiol 78:1–23
Czajkowski R, Ozymko Z, Lojkowska E (2014) Isolation and characterization of novel soilborne lytic bacteriophages infecting Dickeya spp. biovar 3 (‘D. solani’). Plant Pathol 63:758–772
Darrasse A, Priou S, Kotoujansky A, Bertheau Y (1994) PCR and restriction fragment length polymorphism of a pel gene as a tool to identify Erwinia carotovora in relation to potato diseases. Appl Environ Microbiol 60:1437–1443
Davidson RS (1948) Factors affecting the development of bacterial soft rot of potato tuber initials. Dissertation, University of Minnesota
De Boer S (2008) Managing soft rot and ring rot. In: Johnson DA (ed) Potato health management. APS Press, St Paul, pp 171–181
de Haan EG, Dekker-Nooren TC, van den Bovenkamp GW, Speksnijder AG, van der Zouwen PS, van der Wolf JM (2008) Pectobacterium carotovorum subsp. carotovorum can cause potato blackleg in temperate climates. Eur J Plant Pathol 122:561
del Pilar Marquez-Villavicencio M, Weber B, Witherell RA, Willis DK, Charkowski AO (2011) The 3-hydroxy-2-butanone pathway is required for Pectobacterium carotovorum pathogenesis. PLoS ONE 6:e22974
Ellis EL, Delbrück M (1939) The growth of bacteriophage. J Gen Physiol 22:365–384
FAO STAT (2013) Food and agriculture organization of the United Nations. Statistical database
Fister S, Robben C, Witte AK, Schoder D, Wagner M, Rossmanith P (2016) Influence of environmental factors on phage-bacteria interaction and on the efficacy and infectivity of phage P100. Front Microbiol 7:1152
Frampton RA, Pitman AR, Fineran PC (2012) Advances in bacteriophage-mediated control of plant pathogens. Int J Microbiol 2012:326452
Hadas H, Einav M, Fishov, I, Zaritsky A (1997) Bacteriophage T4 development depends on the physiology of its host Escherichia coli. Microbiology 143:179–185
Iriarte FB, Obradović A, Wernsing MH, Jackson LE, Balogh B, Hong JA, Vallad GE (2012) Soil-based systemic delivery and phyllosphere in vivo propagation of bacteriophages: two possible strategies for improving bacteriophage persistence for plant disease control. Bacteriophage 2(4):e23530
Lim J-A, Jee S, Lee DH, Roh E, Jung K, Oh C, Heu S (2013) Biocontrol of Pectobacterium carotovorum subsp. carotovorum using bacteriophage PP1. J Microbiol Biotechnol 23:1147–1153
Loc-Carrillo C, Abedon ST (2011) Pros and cons of phage therapy. Bacteriophage 1:111–114
Ma B, Hibbing ME, Kim H-S, Reedy RM, Yedidia I, Breuer J, Breuer J, Glasner JD, Perna NT, Kelman A (2007) Host range and molecular phylogenies of the soft rot enterobacterial genera Pectobacterium and Dickeya. Phytopathology 97:1150–1163
Muturi P, Yu J, Li J, Jiang M, Maina AN, Kariuki S, Mwaura FB, Wei H (2018) Isolation and characterization of pectolytic bacterial pathogens infecting potatoes in Nakuru County, Kenya. J Appl Microbiol 124:1580–1588
Onkendi EM, Moleleki LN (2014) Characterization of Pectobacterium carotovorum subsp. carotovorum and brasiliense from diseased potatoes in Kenya. Eur J Plant Pathol 139:557–566
Patil VU, Sharma NN, Chakrabarti SK (2017) High-throughput sequencing of the potato genome. In: Chakrabarti SK, Xie C, Tiwari JK (eds) The potato genome. Springer, Berlin, pp 95–107
Pérombelon M (2002) Potato diseases caused by soft rot erwinias: an overview of pathogenesis. Plant Pathol 51:1–12
Rakhuba D, Kolomiets E, Dey ES, Novik G (2010) Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. Pol J Microbiol 59:145–155
Sulakvelidze A, Alavidze Z, Morris JG (2001) Bacteriophage therapy. Antimicrob Agents Chemother 45:649–659
Toth IK, Bell KS, Holeva MC, Birch PR (2003) Soft rot erwiniae: from genes to genomes. Mol Plant Pathol 4:17–30
Wei C, Liu J, Maina AN, Mwaura FB, Yu J, Yan C, Zhang R, Wei H (2017) Developing a bacteriophage cocktail for biocontrol of potato bacterial wilt. Virol Sin 32:476–484
Acknowledgements
We would like to thank Pei Zhang and An-Na Du from Core Facility and Technical Support, Wuhan Institute of Virology, for their assistance in providing TEM micrographs. This study was supported financially by the Sino-Africa Joint Research Centre (SAJC201605) and the Chinese Academy of Sciences (ZDRW-ZS-2016-4).
Author information
Authors and Affiliations
Contributions
PM, FBM and HPW came up with the concept and designed the experiments. PM, JPY and ANM did the experiments. PM and JPY analysed the data. HPW, SK and FBM guided in developing the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
All the authors declare that they have no conflict of interest.
Animal and Human Rights Statement
This article does not contain any studies with human or animal subjects performed by any of the Authors
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Muturi, P., Yu, J., Maina, A.N. et al. Bacteriophages Isolated in China for the Control of Pectobacterium carotovorum Causing Potato Soft Rot in Kenya. Virol. Sin. 34, 287–294 (2019). https://doi.org/10.1007/s12250-019-00091-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12250-019-00091-7