Skip to content
1887

Abstract

Relatively few phages that infect plant pathogens have been isolated and investigated. The species complex is present in various environments, including plants. It can cause major crop diseases, such as bacterial canker on apricot trees. This study presents a collection of 25 unique phage genomes that infect . These phages were isolated from apricot orchards with bacterial canker symptoms after enrichment with 21 strains of . This collection comprises mostly virulent phages, with only three being temperate. They belong to 14 genera, 11 of which are newly discovered, and 18 new species, revealing great genetic diversity within this collection. Novel DNA packaging systems have been identified bioinformatically in one of the new phage species, but experimental confirmation is required to define the precise mechanism. Additionally, many phage genomes contain numerous potential auxiliary metabolic genes with diversified putative functions. At least three phages encode genes involved in bacterial tellurite resistance, a toxic metalloid. This suggests that viruses could play a role in bacterial stress tolerance. This research emphasizes the significance of continuing the search for new phages in the agricultural ecosystem to unravel novel ecological diversity and new gene functions. This work contributes to the foundation for future fundamental and applied research on phages infecting phytopathogenic bacteria.

Funding
This study was supported by the:
  • INRAE
    • Principle Award Recipient: NotApplicable
  • Avignon Université
    • Principle Award Recipient: NotApplicable
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001990
2024-06-04
2025-04-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/105/6/jgv001990.html?itemId=/content/journal/jgv/10.1099/jgv.0.001990&mimeType=html&fmt=ahah

References

  1. Suttle CA. Marine viruses – major players in the global ecosystem. Nat Rev Microbiol 2007; 5:801–812 [View Article] [PubMed]
    [Google Scholar]
  2. Middelboe M, Brussaard CPD. Marine viruses: key players in marine ecosystems. Viruses 2017; 9:302 [View Article] [PubMed]
    [Google Scholar]
  3. Williamson KE, Fuhrmann JJ, Wommack KE, Radosevich M. Viruses in soil ecosystems: an unknown quantity within an unexplored territory. Annu Rev Virol 2017; 4:201–219 [View Article] [PubMed]
    [Google Scholar]
  4. Mirzaei MK, Maurice CF. Ménage à trois in the human gut: interactions between host, bacteria and phages. Nat Rev Microbiol 2017; 15:397–408 [View Article] [PubMed]
    [Google Scholar]
  5. Blazanin M, Turner PE. Community context matters for bacteria-phage ecology and evolution. ISME J 2021; 15:3119–3128 [View Article] [PubMed]
    [Google Scholar]
  6. Brown TL, Charity OJ, Adriaenssens EM. Ecological and functional roles of bacteriophages in contrasting environments: marine, terrestrial and human gut. Curr Opin Microbiol 2022; 70:102229 [View Article] [PubMed]
    [Google Scholar]
  7. Dong Z, Xing S, Liu J, Tang X, Ruan L et al. Isolation and characterization of a novel phage Xoo-sp2 that infects Xanthomonas oryzae pv. oryzae. J Gen Virol 2018; 99:1453–1462 [View Article] [PubMed]
    [Google Scholar]
  8. Wang X, Wei Z, Yang K, Wang J, Jousset A et al. Phage combination therapies for bacterial wilt disease in tomato. Nat Biotechnol 2019; 37:1513–1520 [View Article] [PubMed]
    [Google Scholar]
  9. Frampton RA, Taylor C, Holguín Moreno AV, Visnovsky SB, Petty NK et al. Identification of bacteriophages for biocontrol of the kiwifruit canker phytopathogen Pseudomonas syringae pv. actinidiae. Appl Environ Microbiol 2014; 80:2216–2228 [View Article] [PubMed]
    [Google Scholar]
  10. Vu NT, Kim H, Lee S, Hwang IS, Kwon C-T et al. Bacteriophage cocktail for biocontrol of soft rot disease caused by Pectobacterium species in Chinese cabbage. Appl Microbiol Biotechnol 2023; 108:11 [View Article] [PubMed]
    [Google Scholar]
  11. Twort FW. An investigation on the nature of ultra-microscopic viruses. The Lancet 1915; 186:1241–1243 [View Article]
    [Google Scholar]
  12. D’Herelle F. On an invisible microbe antagonistic toward dysenteric bacilli: brief note by Mr. F. D’Herelle, presented by Mr. Roux. 1917. Res Microbiol 2007; 158:553–554 [View Article] [PubMed]
    [Google Scholar]
  13. Mallmann WL, Hemstreet C. Isolation of an inhibitory substance from plants; 1924 https://naldc.nal.usda.gov/download/IND43966880/PDF accessed 22 August 2022
  14. Coons GH, Kotila JE. The transmissible lytic principle (Bacteriophage) in relation to plant pathogens. Phytopathology 1925; 15:357–370
    [Google Scholar]
  15. Berge O, Monteil CL, Bartoli C, Chandeysson C, Guilbaud C et al. A user’s guide to A data base of the diversity of Pseudomonas syringae and its application to classifying strains in this phylogenetic complex. PLoS One 2014; 9:e105547 [View Article] [PubMed]
    [Google Scholar]
  16. Morris CE, Monteil CL, Berge O. The life history of Pseudomonas syringae: linking agriculture to earth system processes. Annu Rev Phytopathol 2013; 51:85–104 [View Article] [PubMed]
    [Google Scholar]
  17. Córdova P, Rivera-González JP, Rojas-Martínez V, Fiore N, Bastías R et al. Phytopathogenic Pseudomonas syringae as a threat to agriculture: perspectives of a promising biological control using bacteriophages and microorganisms. Horticulturae 2023; 9:712 [View Article]
    [Google Scholar]
  18. Lamichhane JR, Varvaro L, Parisi L, Audergon J-M, Morris CE. Disease and frost damage of woody plants caused by Pseudomonas syringae. In Sparks DL. ed Advances in Agronomy Academic Press; pp 235–295
    [Google Scholar]
  19. Karimi-Kurdistani G, Harighi B. Phenotypic and molecular properties of Pseudomonas syringae pv. syringae the causal agent of bacterial canker of stone fruit trees in Kurdistan province. J Plant Pathol 2008; 90:81–86
    [Google Scholar]
  20. Donmez MF, Karlidag H, Esitken A. Identification of resistance to bacterial canker (Pseudomonas syringae pv. syringae) disease on apricot genotypes grown in Turkey. Eur J Plant Pathol 2010; 126:241–247 [View Article]
    [Google Scholar]
  21. Ivanova L. First occurrence of apricot blast disease caused by Psеudomonas syringae in the north-eastern part of bulgaria. Acta Hortic 2009149–152 [View Article]
    [Google Scholar]
  22. Giovanardi D, Ferrante P, Scortichini M, Stefani E. Characterisation of Pseudomonas syringae isolates from apricot orchards in north-eastern Italy. Eur J Plant Pathol 2018; 151:901–917 [View Article]
    [Google Scholar]
  23. Parisi L, Morgaint B, Blanco‐Garcia J, Guilbaud C, Chandeysson C et al. Bacteria from four phylogroups of the Pseudomonas syringae complex can cause bacterial canker of apricot. Plant Pathology 2019; 68:1249–1258 [View Article]
    [Google Scholar]
  24. Vasebi Y, Khakvar R, Tian L, Moubarak P, Valentini F et al. Phenotypic characterization and phylogenetic analysis of Pseudomonas syringae strains associated with canker disease on apricot in Iran within the context of the global genetic diversity of the P. syringae complex. Eur J Plant Pathol 2020; 158:545–560 [View Article]
    [Google Scholar]
  25. Skliros D, Papazoglou P, Gkizi D, Paraskevopoulou E, Katharios P et al. In planta interactions of a novel bacteriophage against Pseudomonas syringae pv. tomato. Appl Microbiol Biotechnol 2023; 107:3801–3815 [View Article] [PubMed]
    [Google Scholar]
  26. Warring SL, Malone LM, Jayaraman J, Easingwood RA, Rigano LA et al. A lipopolysaccharide-dependent phage infects a pseudomonad phytopathogen and can evolve to evade phage resistance. Environ Microbiol 2022; 24:4834–4852 [View Article] [PubMed]
    [Google Scholar]
  27. Crummett LT, Puxty RJ, Weihe C, Marston MF, Martiny JBH. The genomic content and context of auxiliary metabolic genes in marine cyanomyoviruses. Virology 2016; 499:219–229 [View Article] [PubMed]
    [Google Scholar]
  28. Sun M, Yuan S, Xia R, Ye M, Balcázar JL. Underexplored viral auxiliary metabolic genes in soil: Diversity and eco-evolutionary significance. Environ Microbiol 2023; 25:800–810 [View Article] [PubMed]
    [Google Scholar]
  29. Tamura K, Stecher G, Kumar S. MEGA11: Molecular evolutionary genetics analysis version 11. Mol Biol Evol 2021; 38:3022–3027 [View Article] [PubMed]
    [Google Scholar]
  30. King EO, Ward MK, Raney DE. Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 1954; 44:301–307 [PubMed]
    [Google Scholar]
  31. Fortier L-C, Moineau S. Phage production and maintenance of stocks, including expected stock lifetimes. In Clokie MRJ, Kropinski AM. eds Bacteriophages Totowa, NJ: Humana Press; pp 203–219 [View Article]
    [Google Scholar]
  32. Kropinski AM, Mazzocco A, Waddell TE, Lingohr E, Johnson RP. Enumeration of bacteriophages by double agar overlay plaque assay. Methods Mol Biol 2009; 501:69–76 [View Article] [PubMed]
    [Google Scholar]
  33. Ackermann H-W. Basic phage electron microscopy. In Clokie MRJ, Kropinski AM. eds Bacteriophages: Methods and Protocols, Volume 1: Isolation, Characterization, and Interactions Totowa, NJ: Humana Press; pp 113–126 [View Article]
    [Google Scholar]
  34. The Galaxy Community The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2022 update. Nucleic Acids Res 2022; 50:W345–W351 [View Article] [PubMed]
    [Google Scholar]
  35. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  36. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  37. Garneau JR, Depardieu F, Fortier L-C, Bikard D, Monot M. PhageTerm: a tool for fast and accurate determination of phage termini and packaging mechanism using next-generation sequencing data. Sci Rep 2017; 7:8292 [View Article] [PubMed]
    [Google Scholar]
  38. Lopes A, Tavares P, Petit M-A, Guérois R, Zinn-Justin S. Automated classification of tailed bacteriophages according to their neck organization. BMC Genomics 2014; 15:1027 [View Article] [PubMed]
    [Google Scholar]
  39. Tynecki P, Guziński A, Kazimierczak J, Jadczuk M, Dastych J et al. PhageAI - bacteriophage life cycle recognition with machine learning and natural language processing. bioRxiv 2020 [View Article]
    [Google Scholar]
  40. Moraru C, Varsani A, Kropinski AM. VIRIDIC — a novel tool to calculate the intergenomic similarities of prokaryote-infecting viruses. Viruses 2020; 12:1268 [View Article] [PubMed]
    [Google Scholar]
  41. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  42. Arndt D, Grant JR, Marcu A, Sajed T, Pon A et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 2016; 44:W16–21 [View Article] [PubMed]
    [Google Scholar]
  43. Cook R, Brown N, Redgwell T, Rihtman B, Barnes M et al. INfrastructure for a PHAge reference database: identification of large-scale biases in the current collection of cultured phage genomes. PHAGE 2021; 2:214–223 [View Article] [PubMed]
    [Google Scholar]
  44. Ceyssens P-J, Lavigne R. Bacteriophages of Pseudomonas. Future Microbiol 2010; 5:1041–1055 [View Article] [PubMed]
    [Google Scholar]
  45. De Smet J, Hendrix H, Blasdel BG, Danis-Wlodarczyk K, Lavigne R. Pseudomonas predators: understanding and exploiting phage-host interactions. Nat Rev Microbiol 2017; 15:517–530 [View Article] [PubMed]
    [Google Scholar]
  46. Rabiey M, Roy SR, Holtappels D, Franceschetti L, Quilty BJ et al. Phage biocontrol to combat Pseudomonas syringae pathogens causing disease in cherry. Microb Biotechnol 2020; 13:1428–1445 [View Article] [PubMed]
    [Google Scholar]
  47. Morris CE, Sands DC, Vanneste JL, Montarry J, Oakley B et al. Inferring the evolutionary history of the plant pathogen Pseudomonas syringae from its biogeography in headwaters of rivers in North America, Europe, and New Zealand. mBio 2010; 1:e00107-10 [View Article] [PubMed]
    [Google Scholar]
  48. Monteil CL, Lafolie F, Laurent J, Clement J-C, Simler R et al. Soil water flow is a source of the plant pathogen Pseudomonas syringae in subalpine headwaters. Environ Microbiol 2014; 16:2038–2052 [View Article] [PubMed]
    [Google Scholar]
  49. Turner D, Kropinski AM, Adriaenssens EM. A roadmap for genome-based phage taxonomy. Viruses 2021; 13:506 [View Article] [PubMed]
    [Google Scholar]
  50. Silva EC, Rodrigues LMR, Vila MMDC, Balcão VM. Newly isolated phages preying on Pseudomonas syringae pv. garcae: In vitro and ex vivo inactivation studies in coffee plant leafs. Enzyme Microb Technol 2023; 171:110325 [View Article] [PubMed]
    [Google Scholar]
  51. Rocha EPC, Danchin A. Base composition bias might result from competition for metabolic resources. Trends Genet 2002; 18:291–294 [View Article] [PubMed]
    [Google Scholar]
  52. Backman T, Latorre SM, Symeonidi E, Muszyński A, Bleak E et al. A weaponized phage suppresses competitors in historical and modern metapopulations of pathogenic bacteria. bioRxiv 2024 [View Article] [PubMed]
    [Google Scholar]
  53. López-Leal G, Camelo-Valera LC, Hurtado-Ramírez JM, Verleyen J, Castillo-Ramírez S et al. Mining of thousands of prokaryotic genomes reveals high abundance of prophages with a strictly narrow host range. mSystems 2022; 7:e0032622 [View Article] [PubMed]
    [Google Scholar]
  54. Baltrus DA, Weaver S, Krings L, Nguyen AE. Genomic correlates of tailocin sensitivity in Pseudomonas syringae. Microbiology 2023 [View Article]
    [Google Scholar]
  55. Shen A, Millard A. Phage genome annotation: where to begin and end. PHAGE 2021; 2:183–193 [View Article] [PubMed]
    [Google Scholar]
  56. Young R. Phage lysis: three steps, three choices, one outcome. J Microbiol 2014; 52:243–258 [View Article] [PubMed]
    [Google Scholar]
  57. Berry J, Summer EJ, Struck DK, Young R. The final step in the phage infection cycle: the Rz and Rz1 lysis proteins link the inner and outer membranes. Mol Microbiol 2008; 70:341–351 [View Article] [PubMed]
    [Google Scholar]
  58. Bailly-Bechet M, Vergassola M, Rocha E. Causes for the intriguing presence of tRNAs in phages. Genome Res 2007; 17:1486–1495 [View Article] [PubMed]
    [Google Scholar]
  59. Taslem Mourosi J, Awe A, Guo W, Batra H, Ganesh H et al. Understanding bacteriophage tail fiber interaction with host surface receptor: the key “blueprint” for reprogramming phage host range. Int J Mol Sci 2022; 23:12146 [View Article] [PubMed]
    [Google Scholar]
  60. Meyer JR, Dobias DT, Medina SJ, Servilio L, Gupta A et al. Ecological speciation of bacteriophage lambda in allopatry and sympatry. Science 2016; 354:1301–1304 [View Article] [PubMed]
    [Google Scholar]
  61. de Leeuw M, Baron M, Ben David O, Kushmaro A. Molecular insights into bacteriophage evolution toward its host. Viruses 2020; 12:1132 [View Article] [PubMed]
    [Google Scholar]
  62. Ohlendorf DH, Tronrud DE, Matthews BW. Refined structure of Cro repressor protein from bacteriophage λ suggests both flexibility and plasticity. J Mol Biol 1998; 280:129–136 [View Article] [PubMed]
    [Google Scholar]
  63. Ramesh N, Archana L, Madurantakam Royam M, Manohar P, Eniyan K. Effect of various bacteriological media on the plaque morphology of Staphylococcus and Vibrio phages. Access Microbiology 2019; 1:e000036 [View Article]
    [Google Scholar]
  64. Millard A, Clokie MRJ, Shub DA, Mann NH. Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc Natl Acad Sci USA 2004; 101:11007–11012 [View Article] [PubMed]
    [Google Scholar]
  65. Zheng X, Jahn MT, Sun M, Friman V-P, Balcazar JL et al. Organochlorine contamination enriches virus-encoded metabolism and pesticide degradation associated auxiliary genes in soil microbiomes. ISME J 2022; 16:1397–1408 [View Article] [PubMed]
    [Google Scholar]
  66. Pérez-Arellano I, Rubio V, Cervera J. Dissection of Escherichia coli glutamate 5-kinase: functional impact of the deletion of the PUA domain. FEBS Lett 2005; 579:6903–6908 [View Article] [PubMed]
    [Google Scholar]
  67. Ping D, Wang T, Fraebel DT, Maslov S, Sneppen K et al. Hitchhiking, collapse, and contingency in phage infections of migrating bacterial populations. ISME J 2020; 14:2007–2018 [View Article] [PubMed]
    [Google Scholar]
  68. Sharon I, Alperovitch A, Rohwer F, Haynes M, Glaser F et al. Photosystem I gene cassettes are present in marine virus genomes. Nature 2009; 461:258–262 [View Article] [PubMed]
    [Google Scholar]
  69. Mann NH, Cook A, Millard A, Bailey S, Clokie M. Bacterial Photosynthesis genes in a virus. Nature 2003; 424:741 [View Article] [PubMed]
    [Google Scholar]
  70. Clokie MRJ, Shan J, Bailey S, Jia Y, Krisch HM et al. Transcription of a “photosynthetic” T4-type phage during infection of a marine cyanobacterium. Environ Microbiol 2006; 8:827–835 [View Article] [PubMed]
    [Google Scholar]
  71. Taylor DE. Bacterial tellurite resistance. Trends Microbiol 1999; 7:111–115 [View Article] [PubMed]
    [Google Scholar]
  72. Peng W, Wang Y, Fu Y, Deng Z, Lin S et al. Characterization of the tellurite-resistance properties and identification of the core ufnction genes for tellurite resistance in Pseudomonas citronellolis SJTE-3. Microorganisms 2022; 10:95 [View Article] [PubMed]
    [Google Scholar]
  73. Mazor Y, Greenberg I, Toporik H, Beja O, Nelson N. The evolution of photosystem I in light of phage-encoded reaction centres. Philos Trans R Soc Lond B Biol Sci 2012; 367:3400–3405 [View Article]
    [Google Scholar]
/content/journal/jgv/10.1099/jgv.0.001990
Loading
/content/journal/jgv/10.1099/jgv.0.001990
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error