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Environmental microbiology
Mar, 2025;27 (3): e70076.

Impact of Phage Therapy on Pseudomonas syringae pv. syringae and Plant Microbiome Dynamics Through Coevolution and Field Experiments.

Matevz Papp-Rupar, Emily R Grace, Naina Korotania, Maria-Laura Ciusa, Robert W Jackson, Mojgan Rabiey
Author Information
  1. Matevz Papp-Rupar: NIAB EMR, West Malling, UK. ORCID
  2. Emily R Grace: School of Biosciences and the Birmingham Institute of Forest Research, University of Birmingham, Edgbaston, UK. ORCID
  3. Naina Korotania: School of Biosciences and the Birmingham Institute of Forest Research, University of Birmingham, Edgbaston, UK. ORCID
  4. Maria-Laura Ciusa: School of Biosciences and the Birmingham Institute of Forest Research, University of Birmingham, Edgbaston, UK. ORCID
  5. Robert W Jackson: School of Biosciences and the Birmingham Institute of Forest Research, University of Birmingham, Edgbaston, UK. ORCID
  6. Mojgan Rabiey: School of Biosciences and the Birmingham Institute of Forest Research, University of Birmingham, Edgbaston, UK. ORCID
PMID: 40075541 DOI: 10.1111/1462-2920.70076

Abstract

Bacteriophages (phages) are viruses that infect and lyse bacteria and have the potential for controlling bacterial diseases. Isolation of phages targeting the cherry pathogen Pseudomonas syringae pv. syringae (Pss) led to five distinct phage genotypes. Building on previous in vitro coevolution experiments, the coevolution of the five phages (individually and as a cocktail) with Pss on cherry leaves was conducted in glasshouse and field experiments. Phages effectively reduced Pss numbers on detached leaves, with no evidence of phage resistance emerging in the bacterial population. Field application of phages in a cherry orchard in Southeast England evaluated phage survival, viability and impact on bacterial populations and the microbial community. The bacterial population and phages persisted in the leaf and shoot environment as long as the bacterial host was present. In contrast to in vitro studies, the plant environment constrained the emergence of phage resistant Pss populations. Application of phage cocktail in the orchard did not affect the cherry leaf microbiome. These observations provide essential knowledge for using phage treatments to control bacterial diseases while minimising the impact on the plant microbiome, highlighting phages' potential to safely control bacterial diseases in trees.

Keywords

Pseudomonas syringae bacteriophage biocontrol cherry canker microbiome

References

  1. Front Genet. 2019 Sep 25;10:904 [PMID: 31608125]
  2. Evol Lett. 2023 Nov 11;8(2):253-266 [PMID: 38525025]
  3. Plants (Basel). 2021 Apr 30;10(5): [PMID: 33946244]
  4. New Phytol. 2018 Jul;219(2):672-696 [PMID: 29726587]
  5. Elife. 2022 Feb 21;11: [PMID: 35188102]
  6. Nucleic Acids Res. 2014 Jan;42(Database issue):D633-42 [PMID: 24288368]
  7. Gut Microbes. 2019;10(1):92-99 [PMID: 29913091]
  8. Viruses. 2022 May 18;14(5): [PMID: 35632829]
  9. Front Microbiol. 2018 Sep 18;9:2176 [PMID: 30283415]
  10. Microbiol Mol Biol Rev. 2023 Dec 20;87(4):e0006323 [PMID: 37947420]
  11. Sci Rep. 2022 Jun 24;12(1):10725 [PMID: 35750797]
  12. Plant Dis. 2003 Aug;87(8):949-954 [PMID: 30812801]
  13. Viruses. 2022 Aug 13;14(8): [PMID: 36016392]
  14. Curr Microbiol. 2020 Aug;77(8):1438-1447 [PMID: 32193605]
  15. Microb Biotechnol. 2020 Sep;13(5):1428-1445 [PMID: 32383813]
  16. Genomics Inform. 2019 Mar;17(1):e6 [PMID: 30929407]
  17. J Lab Clin Med. 1954 Aug;44(2):301-7 [PMID: 13184240]
  18. Genome Biol. 2014;15(12):550 [PMID: 25516281]
  19. Genes (Basel). 2023 Jul 31;14(8): [PMID: 37628619]
  20. Annu Rev Phytopathol. 2018 Aug 25;56:161-180 [PMID: 29856934]
  21. Mol Ecol Resour. 2023 Apr;23(3):539-548 [PMID: 36330663]
  22. Nat Methods. 2013 Oct;10(10):996-8 [PMID: 23955772]
  23. F1000 Biol Rep. 2012;4:17 [PMID: 22991582]
  24. Mol Ecol. 1993 Apr;2(2):113-8 [PMID: 8180733]
  25. Microb Ecol. 2001 Apr;41(3):252-263 [PMID: 11391463]
  26. Curr Microbiol. 2021 Mar;78(3):1026-1033 [PMID: 33537885]
  27. Nat Biotechnol. 2019 Dec;37(12):1513-1520 [PMID: 31792408]
  28. Nat Commun. 2022 Jun 30;13(1):3776 [PMID: 35773283]
  29. Genome Biol. 2010;11(10):R106 [PMID: 20979621]
  30. Antimicrob Agents Chemother. 2012 Dec;56(12):6235-42 [PMID: 23006754]
  31. Antibiotics (Basel). 2022 Aug 18;11(8): [PMID: 36009986]
  32. Protein Cell. 2021 May;12(5):315-330 [PMID: 32394199]
  33. Appl Environ Microbiol. 2007 Mar;73(6):1704-11 [PMID: 17259361]
  34. Bioinformatics. 2015 Nov 1;31(21):3476-82 [PMID: 26139637]
  35. Nat Rev Microbiol. 2009 Nov;7(11):828-36 [PMID: 19834481]
  36. Front Microbiol. 2016 Mar 15;7:279 [PMID: 27014204]
  37. Mol Ecol. 2017 Apr;26(7):1790-1801 [PMID: 28207977]
  38. Evolution. 2019 Dec;73(12):2461-2475 [PMID: 31433508]
  39. PLoS One. 2013;8(2):e56329 [PMID: 23457551]
  40. FEMS Microbiol Rev. 2014 Sep;38(5):916-31 [PMID: 24617569]
  41. Microbiol Spectr. 2023 Jun 15;11(3):e0056323 [PMID: 37102867]
  42. New Phytol. 2023 Feb;237(3):959-973 [PMID: 36285389]
  43. J Virol Methods. 2018 Sep;259:18-24 [PMID: 29859196]
  44. Mol Ecol. 2013 Nov;22(21):5271-7 [PMID: 24112409]
  45. Food Chem. 2023 Jun 15;411:135442 [PMID: 36652885]
  46. Annu Rev Phytopathol. 2007;45:245-62 [PMID: 17386003]
  47. Nutrients. 2019 Mar 20;11(3): [PMID: 30897686]
  48. Nat Rev Microbiol. 2018 May;16(5):316-328 [PMID: 29479077]
  49. Environ Microbiol. 2022 Oct;24(10):4834-4852 [PMID: 35912527]

Grants

  1. /The University of Warwick start-up fund
  2. BB/T010568/1/Plant Bacterial Diseases programme
  3. /JABBS Foundation
  4. /Applied Microbiology International
  5. /East Malling Trust
  6. /Worshipful Company of Fruiterers
  7. BB/S019669/1/Biotechnology and Biological Sciences Research Council
  8. BB/X019683/1/Biotechnology and Biological Sciences Research Council
  9. /University of Birmingham

MeSH Term

Pseudomonas syringae
Plant Diseases
Microbiota
Plant Leaves
Phage Therapy
Pseudomonas Phages
Bacteriophages
Prunus avium
England
Biological Coevolution
Journal Article

Word Cloud

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