The tail-associated depolymerase of Erwinia amylovora phage L1 mediates host cell adsorption and enzymatic capsule removal, which can enhance infection by other phage

Environmental Microbiology

Volumn 16, Issue 7, 2014, Pages 2168-2180

  Born, Yannick ^a,b   Fieseler, Lars ^a,c   Klumpp, Jochen ^a   Eugster, Marcel R ^a   Zurfluh, Katrin ^a   Duffy, Brion ^b   Loessner, Martin J ^a  

^a ETH ZURICH   (Switzerland)

^b AGROSCOPE   (Switzerland)

^c ZURICH UNIVERSITY OF APPLIED SCIENCES   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ERWINIA AMYLOVORA;

AMYLOVORAN; BACTERIAL POLYSACCHARIDE; RECOMBINANT PROTEIN; VIRUS PROTEIN;

ARTICLE; BACTERIOPHAGE; BACTERIUM ADHERENCE; BIOLOGICAL CONTROL AGENT; CHEMISTRY; ENZYMOLOGY; ERWINIA AMYLOVORA; ESCHERICHIA COLI; GENETICS; HOST RANGE; HYDROLYSIS; KINETICS; METABOLISM; MICROBIOLOGY; PH; PROTEIN TERTIARY STRUCTURE; ROSACEAE; ULTRASTRUCTURE; VIRION; VIROLOGY;

BACTERIAL ADHESION; BIOLOGICAL CONTROL AGENTS; ERWINIA AMYLOVORA; ESCHERICHIA COLI; HOST SPECIFICITY; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; KINETICS; PODOVIRIDAE; POLYSACCHARIDES, BACTERIAL; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; ROSACEAE; VIRAL PROTEINS; VIRION;

EID: 84903788662     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12212     Document Type: Article

References (60)

1. Adams, M.H., and Park, B.H. (1956) An enzyme produced by a phage-host cell system. II. The properties of the polysaccharide depolymerase. Virology 2: 719-736.
2. Barbirz, S., Müller, J.J., Uetrecht, C., Clark, A.J., Heinemann, U., and Seckler, R. (2008) Crystal structure of Escherichia coli phage HK620 tailspike: podoviral tailspike endoglycosidase modules are evolutionarily related. Mol Microbiol 69: 303-316.
3. Bartell, P.F., and Orr, T.E. (1969) Distinct slime polysaccharide depolymerases of bacteriophage-infected Pseudomonas aeruginosa: evidence of close association with the structured bacteriophage particle. J Virol 4: 580-584.
4. Bayer, M.E., Thurow, H., and Bayer, M.H. (1979) Penetration of the polysaccharide capsule of Escherichia coli (Bi161/42) by bacteriophage K29. Virology 94: 95-118.
5. Bellemann, P., Bereswill, S., Berger, S., and Geider, K. (1994) Visualization of capsule formation by Erwinia amylovora and assays to determine amylovoran synthesis. Int J Biol Macromol 16: 290-296.
6. Bernheimer, H.P., and Tiraby, J.G. (1976) Inhibition of phage infection by Pneumococcus capsule. Virology 73: 308-309.
7. Bessler, W., Freund-Molbert, E., Knufermann, H., Rudolph, C., Thurow, H., and Stirm, S. (1973) A bacteriophage-induced depolymerase active on Klebsiella K11 capsular polysaccharide. Virology 56: 134-151.
8. Billing, E. (1960) An association between capsulation and phage sensitivity in Erwinia amylovora. Nature 186: 819-820.
9. Bonn, W.G., and van der Zwet, T. (2000) Distribution and economic importance of fire blight. In Fire Blight: The Disease and Its Causative Agent, Erwinia amylovora. Vanneste, J.L. (ed.). Wallingford, CT, USA: CAB International, pp. 37-53.
10. Born, Y., Fieseler, L., Marazzi, J., Lurz, R., Duffy, B., and Loessner, M.J. (2011) Novel virulent and broad-host-range Erwinia amylovora bacteriophages reveal a high degree of mosaicism and a relationship to Enterobacteriaceae phages. Appl Environ Microbiol 77: 5945-5954.
11. Boulé, J., Sholberg, P.L., Lehman, S.M., O'Gorman, D.T., and Svircev, A.M. (2011) Isolation and characterization of eight bacteriophages infecting Erwinia amylovora and their potential as biological control agents in British Columbia, Canada. Can J Plant Pathol 33: 308-317.
12. Bugert, P., and Geider, K. (1995) Molecular analysis of the ams operon required for exopolysaccharide synthesis of Erwinia amylovora. Mol Microbiol 15: 917-933.
13. Casjens, S.R. (2005) Comparative genomics and evolution of the tailed-bacteriophages. Curr Opin Microbiol 8: 451-458.
14. Casjens, S.R., and Molineux, I.J. (2012) Short noncontractile tail machines: adsorption and DNA delivery by podoviruses. Adv Exp Med Biol 726: 143-179.
15. Castillo, F.J., and Bartell, P.F. (1976) Localization and functional role of the Pseudomonas bacteriophage 2 depolymerase. J Virol 18: 701-708.
16. Cornelissen, A., Ceyssens, P.J., T'Syen, J., Van Praet, H., Noben, J.P., Shaburova, O.V., etal. (2011) The T7-related Pseudomonas putida phage φ15 displays virion-associated biofilm degradation properties. PLoS ONE 6: e18597.
17. Cornelissen, A., Ceyssens, P.J., Krylov, V.N., Noben, J.P., Volckaert, G., and Lavigne, R. (2012) Identification of EPS-degrading activity within the tail spikes of the novel Pseudomonas putida phage AF. Virology 434: 251-256.
18. Duffy, B., Schärer, H.-J., Bünter, M., Klay, A., and Holliger, E. (2005) Regulatory measures against Erwinia amylovora in Switzerland. EPPO Bulletin 35: 239-244.
19. Erskine, J.M. (1973) Characteristics of Erwinia amylovora bacteriophage and its possible role in the epidemiology of fire blight. Can J Microbiol 19: 837-845.
20. Flachowsky, H., Richter, K., Kim, W.S., Geider, K., and Hanke, M.V. (2008) Transgenic expression of a viral EPS-depolymerase is potentially useful to induce fire blight resistance in apple. Ann Appl Biol 153: 345-355.
21. Geider, K. (2000) Exopolysaccharides of Erwinia amylovora: structure, biosynthesis, regulation, role in pathogenicity of amylovoran and levan. In Fire Blight: The Disease and Its Causative Agent, Erwinia Amylovora. Vanneste, J.L. (ed.). Wallingford, CT, USA: CABI, pp. 117-140.
22. Gill, J.J., Svircev, A.M., Smith, R., and Castle, A.J. (2003) Bacteriophages of Erwinia amylovora. Appl Environ Microbiol 69: 2133-2138.
23. Gutierrez, D., Martinez, B., Rodriguez, A., and Garcia, P. (2010) Isolation and characterization of bacteriophages infecting Staphylococcus epidermidis. Curr Microbiol 61: 601-608.
24. Hatfull, G.F. (2008) Bacteriophage genomics. Curr Opin Microbiol 11: 447-453.
25. Hendry, A.T., Carpenter, J.A., and Garrard, E.H. (1967) Bacteriophage studies of isolates from fire blight sources. Can J Microbiol 13: 1357-1364.
26. Hughes, K.A., Sutherland, I.W., Clark, J., and Jones, M.V. (1998a) Bacteriophage and associated polysaccharide depolymerases - novel tools for study of bacterial biofilms. J Appl Microbiol 85: 583-590.
27. Hughes, K.A., Sutherland, I.W., and Jones, M.V. (1998b) Biofilm susceptibility to bacteriophage attack: the role of phage-borne polysaccharide depolymerase. Microbiology 144: 3039-3047.
28. Johnson, K.B., and Stockwell, V.O. (1998) Management of fire blight: a case study in microbial ecology. Annu Rev Phytopathol 36: 227-248.
29. Kassa, T., and Chhibber, S. (2012) Thermal treatment of the bacteriophage lysate of Klebsiella pneumoniae B5055 as a step for the purification of capsular depolymerase enzyme. J Virol Methods 179: 135-141.
30. Kim, W.-S., and Geider, K. (2000) Characterization of a viral EPS-depolymerase, a potential tool for control of fire blight. Phytopathology 90: 1263-1268.
31. Klumpp, J., Dorscht, J., Lurz, R., Bielmann, R., Wieland, M., Zimmer, M., etal. (2008) The terminally redundant, nonpermuted genome of Listeria bacteriophage A511: a model for the SPO1-like myoviruses of Gram-positive bacteria. J Bacteriol 190: 5753-5765.
32. Labrie, S.J., Samson, J.E., and Moineau, S. (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8: 317-327.
33. Loessner, M.J., Kramer, K., Ebel, F., and Scherer, S. (2002) C-terminal domains of Listeria monocytogenes bacteriophage murein hydrolases determine specific recognition and high-affinity binding to bacterial cell wall carbohydrates. Mol Microbiol 44: 335-349.
34. McManus, P.S., Stockwell, V.O., Sundin, G.W., and Jones, A.L. (2002) Antibiotic use in plant agriculture. Annu Rev Phytopathol 40: 443-465.
35. Maes, M., Orye, K., Bobev, S., Devreese, B., Van Beeumen, J., De Bruyn, A., etal. (2001) Influence of amylovoran production on virulence of Erwinia amylovora and a different amylovoran structure in E.amylovora isolates from Rubus. Eur J Plant Pathol 107: 839-844.
36. Malnoy, M., Faize, M., Venisse, J.S., Geider, K., and Chevreau, E. (2005) Expression of viral EPS-depolymerase reduces fire blight susceptibility in transgenic pear. Plant Cell Rep 23: 632-638.
37. Maneval, W.E. (1941) Staining bacteria and yeasts with acid dyes. Stain Technol 16: 13-19.
38. Müller, I., Kube, M., Reinhardt, R., Jelkmann, W., and Geider, K. (2011a) Complete genome sequences of three Erwinia amylovora phages isolated in North America and a bacteriophage induced from an Erwinia tasmaniensis strain. J Bacteriol 193: 795-796.
39. Müller, I., Lurz, R., Kube, M., Quedenau, C., Jelkmann, W., and Geider, K. (2011b) Molecular and physiological properties of bacteriophages from North America and Germany affecting the fire blight pathogen Erwinia amylovora. Microb Biotechnol 4: 735-745.
40. Nagy, J.K., Kiraly, L., and Ildiko, S. (2012) Phage therapy for plant disease control with a focus on fire blight. Cent Eur J Biol 7: 1-12.
41. Nimtz, M., Mort, A., Domke, T., Wray, V., Zhang, Y., Qiu, F., etal. (1996) Structure of amylovoran, the capsular exopolysaccharide from the fire blight pathogen Erwinia amylovora. Carbohydr Res 287: 59-76.
42. Ohshima, Y., Schumacherperdreau, F., Peters, G., and Pulverer, G. (1988) The role of capsule as a barrier to bacteriophage adsorption in an encapsulated Staphylococcus simulans strain. Med Microbiol Immunol 177: 229-233.
43. Petter, J.G., and Vimr, E.R. (1993) Complete nucleotide sequence of the bacteriophage K1F tail gene encoding endo-N-acylneuraminidase (endo-N) and comparison to an endo-N homolog in bacteriophage PK1E. J Bacteriol 175: 4354-4363.
44. Ritchie, D.F., and Klos, E.J. (1977) Isolation of Erwinia amylovora bacteriophage from aerial parts of apple trees. Phytopathology 67: 101-104.
45. Ritchie, D.F., and Klos, E.J. (1979) Some properties of Erwinia amylovora bacteriophages. Phytopathology 69: 1078-1083.
46. Schnabel, E.L., and Jones, A.L. (2001) Isolation and characterization of five Erwinia amylovora bacteriophages and assessment of phage resistance in strains of Erwinia amylovora. Appl Environ Microbiol 67: 59-64.
47. Scholl, D., Rogers, S., Adhya, S., and Merril, C.R. (2001) Bacteriophage K1-5 encodes two different tail fiber proteins, allowing it to infect and replicate on both K1 and K5 strains of Escherichia coli. J Virol 75: 2509-2515.
48. Scholl, D., Adhya, S., and Merril, C. (2005) Escherichia coli K1's capsule is a barrier to bacteriophage T7. Appl Environ Microbiol 71: 4872-4874.
49. Schwarczinger, I., Kiss, E., Süle, S., Tóth, M., and Hevesi, M. (2011) Control of fire blight by bacteriophages on apple flowers. Acta Hortic 896: 457-462.
50. Steven, A.C., Trus, B.L., Maizel, J.V., Unser, M., Parry, D.A.D., Wall, J.S., etal. (1988) Molecular substructure of a viral receptor-recognition protein - the gp17 tail-fiber of bacteriophage T7. J Mol Biol 200: 351-365.
51. Stirm, S. (1968) Escherichia coli K bacteriophages. I. Isolation and introductory characterization of five Escherichia coli K bacteriophages. J Virol 2: 1107-1114.
52. Stockwell, V.O., and Duffy, B. (2012) Use of antibiotics in plant agriculture. Rev Sci Tech 31: 199-210.
53. Stummeyer, K., Schwarzer, D., Claus, H., Vogel, U., Gerardy-Schahn, R., and Muhlenhoff, M. (2006) Evolution of bacteriophages infecting encapsulated bacteria: lessons from Escherichia coli K1-specific phages. Mol Microbiol 60: 1123-1135.
54. Sutherland, I.W., and Wilkinson, J.F. (1965) Depolymerases for bacterial exopolysaccharides obtained from phage-infected bacteria. J Gen Microbiol 39: 373-383.
55. Thomson, S.V. (2000) Epidemiology of fire blight. In Fire Blight: The Disease and Its Causative Agent, Erwinia Amylovora. Vanneste, J.L. (ed.). Wallingford, CT, USA: CAB International, pp. 9-36.
56. Vandenbergh, P.A., and Cole, R.L. (1986) Cloning and expression in Escherichia coli of the polysaccharide depolymerase associated with bacteriophage-infected Erwinia amylovora. Appl Environ Microbiol 51: 862-864.
57. Vandenbergh, P.A., Wright, A.M., and Vidaver, A.K. (1985) Partial purification and characterization of a polysaccharide depolymerase associated with phage infected Erwinia amylovora. Appl Environ Microbiol 49: 994-996.
58. Wilkinson, B.J., and Holmes, K.M. (1979) Staphylococcus aureus cell surface: capsule as a barrier to bacteriophage adsorption. Infect Immun 23: 549-552.
59. Yurewicz, E.C., Ghalambor, M.A., Duckworth, D.H., and Heath, E.C. (1971) Catalytic and molecular properties of a phage-induced capsular polysaccharide depolymerase. J Biol Chem 246: 5607-5616.
60. Zhang, Y., and Geider, K. (1997) Differentiation of Erwinia amylovora strains by pulsed-field gel electrophoresis. Appl Environ Microbiol 63: 4421-4426.