Abstract
Bacteriophages are often considered as possible agents of biological control of unwanted bacterial populations in medicine, agriculture and food industry. Although the virulent phages can efficiently kill the infected host cells but at the population level phage attack not always leads to the host population collapse but may result in establishment of a more or less stable co-existence. The mechanism of the long-term stabilization of the mixed phage-host cultures is poorly understood. Here we describe bacteriophages VyarbaL and Hena2, the members of the Molineuxvirinae and the Ounavirinae subfamilies, respectively, that are able to form the pseudolysogenic associations (PA) with their host Erwinia amylovora 1/79Sm on solid media. These PAs were stable through multiple passages. The phenomenon of the PA formation between a bacterial culture and bacteriophages decreases the effectiveness of bacteriophage-mediated biological control agents based on lytic bacteriophages.
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All data that support the findings of the phage and bacterial culture associations study are included within this paper and its Supplementary Information files.
References
Abedon ST (2009) Disambiguating bacteriophage pseudolysogeny: an historical analysis of lysogeny, pseudolysogeny, and the phage carrier state. In: Adams HT (ed) Contemporary Trends in Bacteriophage Research. Nova Science Publishers, UK
Alattas H (2015) Isolation and Characterization of Host mutations that Supress the Bacteriophage Lambda (λ) Rex Phenotype. Waterloo, Ontario Canada A thesis presented to the University of Waterloo in fulfillment of the thesis requirement for the degree of Master of Science in Pharmacy.
Batinovic S, Wassef F, Knowler SA et al (2019) Bacteriophages in natural and artificial environments. Pathogens 8(3):100. https://doi.org/10.3390/pathogens8030100
Bellemann P, Bereswill S, Berger S et al (1994) Visualization of capsule formation by Erwinia amylovora and assays to determine amylovoran synthesis. Int J Biol Macromol 16:290–296
Besarab NV, Golomidova AK, Letarova MA, Lagonenko AL, Kulikov EE, Letarov AV, Evtushenkov AN (2021) Characterization of Erwinia amylovora bacteriophages, isolated in Belarus. Micro Biotechnol Fund Appl Asp. 13:8–20. https://doi.org/10.47612/2226-3136-2021-13-8-20
Besarab NV, Letarov AV, Babenko VV et al. (2022) Biodiversity of bacteriophages isolated using the indicator bacterial culture Erwinia amylovora 1/79Sm/Abstract book of the 11th International Conference Achievements & Challenges in Biology devoted to 120th anniversary of professor Mirali Akhundov 13-14 October, 2022, Baku State University, Baku, Azerbaijan. 86-88
Bonn WG, van der Zwet T (2000) Distribution and Economic Importance of Fire Blight. In: Vanneste JL (ed) Fire Blight: The Disease and Its Causative Agent. CABI Publishing Erwinia Amylovora, UK
Boulé J, Sholberg PL, Lehman SM et al (2011) Isolation and characterization of eight bacteriophages infecting Erwinia amylovora and their potential as biological control agents in British Columbia. Canad Canad J Plant Pathol 33(3):308–317. https://doi.org/10.1080/07060661.2011.588250
Brives C, Pourraz J (2020) Phage therapy as a potential solution in the fight against AMR: obstacles and possible futures. Palgrave Commun 6:100. https://doi.org/10.1057/s41599-020-0478-4
Composition and method for preventing infections of vegetable tissues caused by Erwinia amylovora. Patent WO2014177996A1.
D'Herelle F. (1935) Bacteriophage and phenomena of recovery. Tiflis. (In Russian)
EPPO Datasheet: Erwinia amylovora https://gd.eppo.int/taxon/ERWIAM/datasheet. Accessed 19 Dec 2022.
Erskine JM (1973) Characteristics of Erwinia amylovora bacteriophage and its possible role in the epidemology of fire blight. Can J Microbiol 19(7):837–845. https://doi.org/10.1139/m73-134
Erwinia amylovora (fireblight) https://www.cabi.org/isc/datasheet/21908. Accessed 14 May 2022.
Garneau JR, Depardieu F, Fortier L-C et al (2017) PhageTerm: a tool for fast and accurate determination of phage termini and packaging mechanism using next-generation sequencing data. Sci Rep 7(1):8292. https://doi.org/10.1038/s41598-017-07910-5
Gerami E, Hassanzadeh N, Abdollahi H et al (2013) Evaluation of some bacterial antagonists for biological control of fire blight disease. Journal of Plant Pathology 95(1):127–134
Gilchrist CLM, Chooi Y-H (2020) Automatic generation of gene cluster comparison figures. Bioinformat. https://doi.org/10.1093/bioinformatics/btab007
Gill J, Abedon ST (2003) Bacteriophage ecology and plants. Apsnet Features, Online. https://doi.org/10.1094/APSnetFeature-2003-1103
Grant JR, Stothard P (2008) The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Res 36(2):W181–W184
Hasan M, Ahn J (2022) Evolutionary dynamics between phages and bacteria as a possible approach for designing effective phage therapies against antibiotic-resistant bacteria. Antibiotics (basel) 11(7):915. https://doi.org/10.3390/antibiotics11070915
Knecht LE, Veljkovic M, Fieseler L (2020) Diversity and function of phage encoded depolymerases. Front Microbiol 10:2949. https://doi.org/10.3389/fmicb.2019.02949
Knecht LE, Born Y, Pelludat C et al (2022) Spontaneous resistance of Erwinia amylovora against bacteriophage Y2 affects infectivity of multiple phages. Front Microbiol 13:908346. https://doi.org/10.3389/fmicb.2022.908346
Koczan JM, McGrath MJ, Zhao Y, Sundin GW (2009) Contribution of Erwinia amylovora exopolysaccharides amylovoran and levan to biofilm formation: implications in pathogenicity. Phytopathology 99(11):1237–1244. https://doi.org/10.1094/PHYTO-99-11-1237
Kulikov EE, Golomidova AK, Letarova MA et al (2014) Genomic sequencing and biological characteristics of a novel Escherichia coli bacteriophage 9g, a putative representative of a new Siphoviridae genus. Viruses 6(12):5077–5092. https://doi.org/10.3390/v6125077
Kulikov EE, Golomidova AK, Prokhorov NS et al (2019) High-throughput LPS profiling as a tool for revealing of bacteriophage infection strategies. Scient Rep. 9:2958. https://doi.org/10.1038/s41598-019-39590-8
Laslett D, Canback B (2004) ARAGORN, a program for the detection of transfer RNA and transfer-messenger RNA genes in nucleotide sequences. Nucleic Acids Res 32:11–16
Latino L, Midoux C, Hauck Y et al (2016) Pseudolysogeny and sequential mutations build multiresistance to virulent bacteriophages in Pseudomonas aeruginosa. Microbiology 162(5):748–763. https://doi.org/10.1099/mic.0.000263
Letarov AV (2019) Modern observations of the biology of bacteriophages. Moscow: TD DeLi. 384. (In Russian)
Letarov AV, Kulikov EE (2018) Determination of the bacteriophage host range: culture-based approach. Methods Mol Biol 1693:75–84. https://doi.org/10.1007/978-1-4939-7395-8_7
Letarova MA, Kulikov EE, Golomidova AK et al (2013) Metastable associations formed in the phage–host system isolated from the horse feces. Vestnik Ulyanovskoi Gosudarstvennoi Selskokhozyaistvennoi Akademii 3:57–61
Loc-Carrillo C, Abedon ST (2011) Pros and cons of phage therapy. Bacteriophage 1(2):111–114. https://doi.org/10.4161/bact.1.2.14590
Łoś M, Węgrzyn G (2012) Pseudolysogeny. Adv Virus Res 82:339–349. https://doi.org/10.1016/B978-0-12-394621-8.00019-4
Lowe TM, Chan PP (2016) tRNAscan-SE On-line: search and contextual analysis of transfer RNA genes. Nucl Acids Res 44:W54-57
Maniatis T, Fritsch E, Sambrook J (1984) Methods of genetic engineering. Molecular Cloning: Transl. from English. 11:479
Mann RA, Smits TH, Bühlmann A, Blom J, Goesmann A, Frey JE, Plummer KM, Beer SV, Luck J, Duffy B, Rodoni B (2013) Comparative genomics of 12 strains of Erwinia amylovora identifies a pan-genome with a large conserved core. PLoS ONE 8(2):55644. https://doi.org/10.1371/journal.pone.0055644
Mäntynen S, Laanto E, Oksanen HM et al (2021) Black box of phage-bacterium interactions: exploring alternative phage infection strategies. Open Biol 11(9):210188. https://doi.org/10.1098/rsob.210188
Müller I, Lurz R, Kube M et al (2011) Molecular and physiological properties of bacteriophages from North America and Germany affecting the fire blight pathogen Erwinia amylovora. Microb Biotechnol 4(6):735–745. https://doi.org/10.1111/j.1751-7915.2011.00272.x
Nagy JK, Király L, Schwarczinger I (2012) Phage therapy for plant disease control with a focus on fire blight. Cent Eur J Biol 7:1–12. https://doi.org/10.2478/s11535-011-0093-x
Phillips ZN, Tram G, Seib KL, Atack JM (2019) Phase-variable bacterial loci: how bacteria gamble to maximise fitness in changing environments. Biochem Soc Trans 47(4):1131–1141. https://doi.org/10.1042/BST20180633
Ripp S, Miller RV (1997) The role of pseudolysogeny in bacteriophage–host interactions in a natural freshwater environment. Virology 143(6):2065–2070
Roach DR, Sjaarda DR, Castle AJ et al (2013) Host exopolysaccharide quantity and composition impact Erwinia amylovora bacteriophage pathogenesis. Appl Environ Microbiol 79(10):3249–3256. https://doi.org/10.1128/AEM.00067-13
Roach DR, Sjaarda DR, Sjaarda CP, Ayala CJ, Howcroft B, Castle AJ, Svircev AM (2015) Absence of lysogeny in wild populations of Erwinia amylovora and Pantoea agglomerans. Microb Biotechnol 8(3):510–518. https://doi.org/10.1111/1751-7915.12253
Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
Schwarczinger I, Nagy JK, Künstler A et al (2017) Characterization of Myoviridae and Podoviridae family bacteriophages of Erwinia amylovora from Hungary – potential of application in biological control of fire blight. Eur J Plant Pathol 149(3):639–652. https://doi.org/10.1007/s10658-017-1214-9
Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30(14):2068–2069
Seibold A, Viehrig M, Jelkmann W (2006) Yeasts as antagonists against Erwinia amylovora. Proc Intl. https://doi.org/10.17660/ActaHortic.2006.704.56
Shabbir MAB, Hao H, Shabbir MZ et al (2016) Bacteria vs bacteriophages: parallel evolution of immune arsenals. Front Microbiol 7:1292. https://doi.org/10.3389/fmicb.2016.01292
Stone E, Campbell K, Grant I et al (2019) Understanding and exploiting phage-host interactions. Viruses 11(6):567. https://doi.org/10.3390/v11060567
Turkington CJR, Morozov A, Clokie MRJ, Bayliss CD (2019) Phage-resistant phase-variant sub-populations mediate herd immunity against bacteriophage invasion of bacterial meta-populations. Front Microbiol 10:1473. https://doi.org/10.3389/fmicb.2019.01473
van der Woude MW, Bäumler AJ (2004) Phase and antigenic variation in bacteria. Clin Microbiol Rev 17(3):581–611. https://doi.org/10.1128/CMR.17.3.581-611.2004
Vanneste JL (2000) What is Fire Blight? Who is Erwinia amylovora? How to Control It? In: Vanneste JL (ed) Fire Blight: The Disease and Its Causative Agent. CABI Publishing. UK, Erwinia Amylovora
Williamson SJ, McLaughlin MR, Paul JH (2001) Interaction of the PhiHSIC virus with its host: lysogeny or pseudolysogeny? Appl Environ Microbiol 67(4):1682–1688. https://doi.org/10.1128/AEM.67.4.1682-1688.2001
Zrelovs N, Dislers A, Kazaks A (2020) Novel Erwinia persicina infecting phage midgardsormr38 within the context of temperate Erwinia phages. Front Microbiol 11:1245. https://doi.org/10.3389/fmicb.2020.01245
Funding
The work of N.V. Besarab, A.L. Lagonenko and A.N. Evtushenkov was partially supported by Ministry of education of Belarus (project no. 20211371).
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Besarab, N.V., Letarova, M.A., Babenko, V.V. et al. The metastable associations of bacteriophages and Erwinia amylovora. Arch Microbiol 205, 214 (2023). https://doi.org/10.1007/s00203-023-03550-8
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DOI: https://doi.org/10.1007/s00203-023-03550-8