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Chapter 20 : Polysaccharide-Degrading Phages

Authors: Dean Scholl, Carl Merril
Content Type: Monograph
Publication Year: 2005

Category: Bacterial Pathogenesis; Microbial Genetics and Molecular Biology

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Abstract:

This chapter discusses some of the recent developments and ideas and focuses on phages that possess virion-bound capsule depolymerization activities rather than those that simply bind to surface carbohydrate structures. The best-characterized polysaccharide-degrading phages are those that infect various strains of . Polysaccharide-degrading phages were also isolated from other gram-negative bacteria, and in the case of , a tremendous amount of diversity was found. Probably the most structurally characterized extracellular polysaccharide-degrading phage tail protein is the lysogenic P22 tailspike. The crystal structures of both the catalytic domain and the head-binding domain have been solved. P22, Sf6, and related phages are lysogenic, have very little biological or sequence relationship to the SP6 group, and based on their tail protein structures, may be categorized as their own distinct group. We may find that multispecific phages encoding more than one tail protein are fairly widespread. While much of this work can be done by the use of molecular techniques, phage typing is still a rapid and reliable method for identifying capsular antigens. In a recent study, a phage endosialidase (endo E) was used as an antibacterial to treat infections by 1 strains. Phages have long been known to play a role in bacterial pathogenesis by transducing virulence factors such as toxin genes.

Citation: Scholl D, Merril C. 2005. Polysaccharide-Degrading Phages, p 400-414. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch20

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Polysaccharide-Degrading Phages
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Citation: Scholl D, Merril C. 2005. Polysaccharide-Degrading Phages, p 400-414. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch20
/content/10.1128/9781555816506.chap20.fig20-1
FIGURE 1

Penetration of bacteriophage K29 through the K29 capsule. Phage particles create a channel through the polysaccharide capsule to reach the cell surface. Reprinted from with permission of the publisher.

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10.1128/9781555816506/fig20-1.gif
Image of FIGURE 1
FIGURE 1

Penetration of bacteriophage K29 through the K29 capsule. Phage particles create a channel through the polysaccharide capsule to reach the cell surface. Reprinted from with permission of the publisher.

Citation: Scholl D, Merril C. 2005. Polysaccharide-Degrading Phages, p 400-414. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch20
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FIGURE 2

Electron immunomicroscopy of K1F particles. The incubation of phage with anti-endosialidase resulted in tail-to-tail lattices, indicating that the enzyme is part of the tail structure. Reprinted from with permission.

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10.1128/9781555816506/fig20-2.gif
Image of FIGURE 2
FIGURE 2

Electron immunomicroscopy of K1F particles. The incubation of phage with anti-endosialidase resulted in tail-to-tail lattices, indicating that the enzyme is part of the tail structure. Reprinted from with permission.

Citation: Scholl D, Merril C. 2005. Polysaccharide-Degrading Phages, p 400-414. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch20
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FIGURE 3

Modular genetic organization of the regions carrying the tail genes of members of the SP6 group of phages. In all four phages, these genes are located at one end of the ~40-kb dsDNA genome. Transcription of the tail genes of all four phages is probably initiated from a common SP6-like promoter. Immediately downstream, phages K1-5 and K5 encode a lyase, whereas SP6 encodes the P22-like endorhamnosidase and K1E has a small ORF of unknown function. In the second position downstream, K1-5 and K1E encode an endosialidase, whereas K5 and SP6 have unidentifiable ORFs.All four phages have a common 84- to 85-base intergenic region.

10.1128/9781555816506/fig20-3_thmb.gif
10.1128/9781555816506/fig20-3.gif
Image of FIGURE 3
FIGURE 3

Modular genetic organization of the regions carrying the tail genes of members of the SP6 group of phages. In all four phages, these genes are located at one end of the ~40-kb dsDNA genome. Transcription of the tail genes of all four phages is probably initiated from a common SP6-like promoter. Immediately downstream, phages K1-5 and K5 encode a lyase, whereas SP6 encodes the P22-like endorhamnosidase and K1E has a small ORF of unknown function. In the second position downstream, K1-5 and K1E encode an endosialidase, whereas K5 and SP6 have unidentifiable ORFs.All four phages have a common 84- to 85-base intergenic region.

Citation: Scholl D, Merril C. 2005. Polysaccharide-Degrading Phages, p 400-414. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch20
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FIGURE 4

(A) Comparison of the tailspike proteins of phages P22 and SP6.The P22 tailspike has an N-terminal head-binding domain that is very similar to those of the tailspikes from phages HK620, Sf6, ST64T, and APSE-1.The SP6 tailspike lacks this domain but possesses a catalytic domain similar to that of P22. (B) The N terminus of the K1F endosialidase has similarity to the head-binding domain of the T7 tail fiber, which is missing from the K1-5 endosialidase.The C termini of both proteins are involved in folding proteins and are cleaved from the mature protein. Head attachment of the SP6 and K1-5 tailspikes may be mediated through a separate protein (see the text for further details).

10.1128/9781555816506/fig20-4_thmb.gif
10.1128/9781555816506/fig20-4.gif
Image of FIGURE 4
FIGURE 4

(A) Comparison of the tailspike proteins of phages P22 and SP6.The P22 tailspike has an N-terminal head-binding domain that is very similar to those of the tailspikes from phages HK620, Sf6, ST64T, and APSE-1.The SP6 tailspike lacks this domain but possesses a catalytic domain similar to that of P22. (B) The N terminus of the K1F endosialidase has similarity to the head-binding domain of the T7 tail fiber, which is missing from the K1-5 endosialidase.The C termini of both proteins are involved in folding proteins and are cleaved from the mature protein. Head attachment of the SP6 and K1-5 tailspikes may be mediated through a separate protein (see the text for further details).

Citation: Scholl D, Merril C. 2005. Polysaccharide-Degrading Phages, p 400-414. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch20
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References

/content/book/10.1128/9781555816506.chap20
1. Aalto, J.,, S. Pelkonen,, H. Kalimo,, and J. Finne. 2001. Mutant bacteriophage with non-catalytic endosialidase binds to both bacterial and eukaryotic polysialic acid and can be used as a probe for its detection. Glycoconj. J. 18: 751– 758.
2. Adams, M. H.,, and B. H. Park. 1956. An enzyme produced by a phage-host cell system. II. The properties of the polysaccharide depolymerase. Virology 2: 719– 736.
3. Albert, J. M.,, N. A. Bhuiyan,, A. Rahman,, A. N. Ghosh,, K. Hultenby,, A. Weintraub,, S. Nahar,, A. K. M. G. Kibriya,, M. Ansaruzzaman,, and T. Shimada. 1996. Phage specific for Vibrio cholerae O139 Bengal. J. Clin. Microbiol. 34: 1843– 1845.
4. Altmann, F.,, B. Kwiatkowski,, and S. Stirm. 1986. A bacteriophage-associated glycanase cleaving β-pyranosidic linkages of 3-deoxy-D-mannose-2-octulosonic acid. Biochem. Biophys. Res.Commun. 136: 329– 335.
5. Baker, J. R.,, S. Dong,, and D. G. Pritchard. 2002. The hyaluronan lyase of Streptococcus pyogenes bacteriophage H4489A. Biochem. J. 365: 317– 322.
6. Barnet, Y. M.,, and B. Humphry. 1975. Exopolysaccharide depolymerases induced by Rhizobium bacteriophage. Can. J. Microbiol. 21: 1647– 1650.
7. Barrow, P. A.,, and J. S. Soothill. 1997. Bacteriophage therapy and prophylaxis: rediscovery and renewed assessment of potential. Trends Microbiol. 5: 268– 271.
8. Bartell, P. E.,, G. K. H. Lam,, and T. E. Orr. 1968. Purification and properties of polysaccharide depolymerase associated with phage-infected Pseudomonas aeruginosa. J. Biol. Chem. 243: 2077– 2080.
9. Bayer, M. E.,, H. Thurow,, and M. H. Bayer. 1979. Penetration of the polysaccharide capsule of Escherichia coli (Bi161/42) by bacteriophage K29. Virology 94: 95– 118.
10. Bernheimer, H. P.,, and J.-G. Tiraby. 1976. Inhibition of phage infection by Pneumococcus capsule. Virology 73: 308– 309.
11. Bessler, W.,, E. Freund-Molbert,, H. Knufermann,, C. Rudolph,, H. Thurow,, and S. Stirm. 1973. A bacteriophage-induced depolymerase active on Klebsiella K11 capsular polysaccharide. Virology 56: 134– 151.
12. Botstein, D. 1980. A theory of modular evolution for bacteriophages. Ann. N.Y. Acad. Sci. 354: 484– 490.
13. Boyd, A.,, and A. M. Chakrabarty. 1995. Pseudomonas aeruginosa biofilms: role of alginate exopolysaccharide. J. Ind. Microbiol. 15: 162– 168.
14. Cescutti, P.,, R. Toffanin,, P. Pollesello,, and I. W. Sutherland. 1999. Structural determination of the acidic exopolysaccharide produced by a Pseudomonas sp. strain 1.15. Carbohydr. Res. 315: 159– 168.
15. Chua, J. E. H.,, P.A. Manning,, and R. Morona. 1999. The Shigella flexneri bacteriophage Sf6 tailspike protein (TSP)/endorhamnosidase is related to the bacteriophage P22 TSP and has a motif common to exo- and endoglycanases, and C-5 epimerases. Microbiology 145: 1649– 1659.
16. Clark, A. J.,, W. Inwood,, T. Cloutier,, and T. S. Dhillon. 2001. Nucleotide sequence of coliphage HK620 and the evolution of lambdoid phages. J. Mol. Biol. 311: 657– 679.
17. Clarke, B. R.,, F. Esumeh,, and I. S. Roberts. 2000. Cloning, expression, and purification of the K5 capsular polysaccharide lyase (KflA) from coliphage K5: evidence for two distinct K5 lyase enzymes. J. Bacteriol. 182: 3761– 3766.
18. Costerton, J. W.,, K.-J. Cheng,, G. G. Geesey,, T. I. Ladd,, J. C. Nickel,, M. Dasgupta,, and T. J. Marrie. 1987. Bacterial biofilms in nature and disease. Annu. Rev. Microbiol. 41: 435– 464.
19. Danese, P. N.,, L. A. Pratt,, and R. Kolter. 2000. Exopolysaccharide production is required for development of E. coli K-12 biofilm architecture. J. Bacteriol. 182: 3593– 3596.
20. Donlan, R. M.,, and J. W. Costerton. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15: 167– 193.
21. Forde, A.,, and G. F. Fitzgerald. 2003. Molecular organization of exopolysaccharide (EPS) encoding genes on the lactococcal bacteriophage adsorption blocking plasmid, pCI658. Plasmid 49: 130– 142.
22. Freiberg, A.,, R. Morona,, L. Van Den Bosch,, C. Jung,, J. Behlke,, N. Carlin,, R. Seckler,, and U. Baxa. 2003. The tailspike protein of Shigella phage Sf6. J. Biol. Chem. 278: 1542– 1548.
23. Gerardy-Schahn, R.,, A. Bethe,, T. Brennecke,, M. Muhlenhoff,, M. Eckhardt,, S. Zeising,, F. Lottspeich,, and M. Frosch. 1995. Molecular cloning and functional expression of bacteriophage PK1E-encoded endoneuraminidase Endo NE. Mol. Microbiol. 16: 441– 450.
24. Greenberg, M.,, J. Dunlap,, and R. Villafane. 1995. Identification of the tailspike protein from the Salmonella newington phage epsilon 34 and partial characterization of its phage-associated properties. J. Struct. Biol. 115: 283– 289.
25. Gross, R. J.,, T. Cheasty,, and B. Rowe. 1977. Isolation of bacteriophages specific for the K1 polysaccharide antigen of E. coli. J. Clin. Microbiol. 6: 548– 550.
26. Gupta, D. S.,, B. Jann,, and K. Jann. 1983. Enzymatic degradation of the capsular K5-antigen of E. coli by coliphage K5. FEMS Microbiol. Lett. 16: 13– 17.
27. Hallenbeck, P. C.,, E. R. Vimr,, F. Yu,, B. Bassler,, and F. A. Troy. 1987. Purification and properties of a bacteriophage-induced endo- N-acetylneuraminidase specific for poly-alpha-2,8-sialosyl carbohydrate units. J. Biol. Chem. 262: 3553– 3561.
28. Hana, A.,, M. Berg,, V. Stout,, and A. Razatos. 2003. Role of capsular colanic acid in the adhesion of uropathogenic E. coli. Appl. Environ. Microbiol. 69: 4474– 4481.
29. Hanfling, P.,, A. S. Shashkov,, B. Jann,, and K. Jann. 1996. Analysis of the enzymatic cleavage (β elimination) of the capsular K5 polysaccharide of E. coli by the K5-specific coliphage: a reexamination. J. Bacteriol. 178: 4747– 4750.
30. Hanlon, G. W.,, S. P. Denyer,, C. J. Olliff,, and L. J. Ibrahim. 2001. Reduction in exopolysaccharide viscosity as an aid to bacteriophage penetration through Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 67: 2746– 2753.
31. Ho, K. 2001. Bacteriophage therapy for bacterial infections. Perspect. Biol. Med. 44: 1– 16.
32. Hughes, K. A.,, I. W. Sutherland,, and M. V. Jones. 1998. Biofilm susceptibility to bacteriophage attack: the role of phage-borne polysaccharide depolymerase. Microbiology 144: 3039– 3047.
33. Hughes, K. A.,, I. W. Sutherland,, J. Clark,, and M. V. Jones. 1998. Bacteriophage and associated polysaccharide depolymerases—novel tools for the study of bacterial biofilms. J.Appl. Microbiol. 85: 583– 590.
34. Humphries, J. C. 1948. Enzymatic activity of bacteriophage culture lysates: a capsule lysin active against Klebsiella pneumoniae type A. J. Bacteriol. 56: 683– 693.
35. Iwashita, S.,, and S. Kanegasaki. 1973. Smooth specific phage adsorption: endorhamnosidase activity of tail parts of P22. Biochem. Biophys. Res. Commun. 55: 403– 409.
36. Juhala, R. J.,, M. E. Ford,, R. L. Duda,, A. Youltan,, G. F. Hatfull,, and R. W. Hendrix. 2000. Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J. Mol. Biol. 299: 27– 51.
37. Kwiatkowski, B.,, H. Beilharz,, and S. Stirm. 1975. Disruption of Vi bacteriophage III and localization of its deacetylase activity. J. Gen. Virol. 29: 267– 280.
38. Kwiatkowski, B.,, B. Boschek,, H. Thiele,, and S. Stirm. 1982. Endo- N-acetylneuraminidase associated with bacteriophage particles. J. Virol. 43: 697– 704.
39. Kwiatkowski, B.,, B. Boschek,, H. Thiele,, and S. Stirm. 1983. Substrate specificity of two bacteriophage-associated endo- N-acetylneuraminidases. J.Virol. 45: 367– 374.
40. Leggate, D. R.,, J. M. Bryant,, M. B. Redpath,, D. Head,, P. W. Taylor,, and J. P. Luzio. 2002. Expression, mutagenesis, and kinetic analysis of the recombinant K1E endosialidase to define the site of proteolytic processing and requirements for catalysis. Mol. Microbiol. 44: 749– 760.
41. Lindberg, A. A., 1977. Bacterial surface carbohydrates and bacteriophage adsorption, p. 289– 356. In I. Sutherland (ed.), Surface Carbohydrates of the Prokaryotic Cell. Academic Press, London, United Kingdom.
42. Long, G. S.,, J. M. Bryant,, P. W. Taylor,, and J. P. Luzio. 1995. Complete nucleotide sequence of the gene encoding bacteriophage E endosialidase: implications for K1E endosialidase structure and function. Biochem. J. 309: 543– 550.
43. Machida, Y.,, K. Miyake,, K. Hattori,, S. Yamamoto,, M. Kawase,, and S. Iijima. 2000. Structure and function of a novel coliphageassociated sialidase. FEMS Microbiol. Lett. 182: 333– 337.
44. Merril, C. R.,, D. Scholl,, and S. Adhya. 2003. The prospect for phage therapy in Western medicine. Nat. Rev. Drug. Discov. 2: 489– 497.
45. Mmolawa, P. T.,, H. Schmieger,, C. P. Tucker,, and M. W. Heuzenroeder. 2003. Genomic structure of the Salmonella enterica serovar Typhimurium DT bacteriophage ST64T: evidence for modular genetic architecture. J. Bacteriol. 185: 3473– 3475.
46. Mühlenhoff, M.,, K. Stummeyer,, M. Grove,, M. Seuerborn,, and R. Gerardy-Schahn. 2003. Proteolytic processing and oligomerization of bacteriophage-derived endosialidases. J. Biol. Chem. 278: 12634– 12644.
47. Mushtaq, N.,, M. B. Redpath,, J. P. Luzio,, and P. W. Taylor. 2004. Prevention and cure of systemic Escherichia coli K1 infection by modification of the bacterial phenotype. Antimicrob. Agents Chemother. 48: 1503– 1508.
48. Nimmich, W.,, G. Schmidt,, and U. Krallmann-Wenzel. 1991. Two different E. coli capsular depolymerases each associated with one of the coliphage ΦK5 and ΦK20. FEMS Microbiol. Lett. 82: 137– 142.
49. Nimmich, W.,, U. Krallmann-Wenzel,, B. Muller,, and G. Schmidt. 1992. Isolation and characterization of bacteriophages specific for capsular antigens K3, K7, K12, and K13 of E. coli. Zentbl. Bakteriol. 276: 213– 220.
50. Nimmich, W. 1994. Detection of Escherichia coli K95 strains by bacteriophages. J. Clin. Microbiol. 32: 2843– 2845.
51. Nimmich, W.,, U. Krallman-Wenzel,, and G. Schmidt. 1994. Bacteriophages specifically recognizing the lipopolysaccharide antigens O4, O5, O6, and O7 of E. coli. Zentbl. Bakteriol. 281: 406– 414.
52. Nimmich, W. 1997. Degradation studies on Escherichia coli capsular polysaccharides. FEMS Microbiol. Lett. 153: 105– 110.
53. Park, B. H. 1956. An enzyme produced by a phage-host system. I.The properties of a Klebsiella phage. Virology 2: 711– 718.
54. Pelkonen, S. 1990. Capsular sialyl chains of E. coli K1 mutants resistant to K1 phage. Curr. Microbiol. 21: 23– 28.
55. Pelkonen, S.,, J. Aalto,, and J. Finne. 1992. Differential activities of bacteriophage depolymerase on bacterial polysaccharide: binding is essential but degradation is inhibitory in phage infection of K1- defective Escherichia coli. J. Bacteriol. 174: 7757– 7761.
56. Petter, J. G.,, and E. R. Vimr. 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.
57. Rieger-Hug, D.,, and S. Stirm. 1981. Comparative study of host capsule depolymerases associated with Klebsiella bacteriophages. Virology 113: 363– 378.
58. Roberts, I. S. 1995. Bacterial polysaccharides in sickness and in health. Microbiology 141: 2023– 2031.
59. Rutishaueser, U.,, M. Watanabe,, J. Silver,, F.A. Troy,, and E. R. Vimr. 1985. Specific alteration of NCAM-mediated cell adhesion by an endoneuraminidase. J. Cell Biol. 101: 1842– 1849.
60. Saxelin, M.-L.,, E.-L. Murmiaho,, M. P. Korhola,, and V. Sundman. 1979. Partial characterization of a new C3-type capsule-dissolving phage of Streptococcus cremoris. Can. J. Microbiol. 25: 1182– 1187.
61. Scholl, D.,, S. Rogers,, S. Adhya,, and C. Merril. 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.
62. Scholl, D.,, S. Adhya,, and C. Merril. 2002. Bacteriophage SP6 is closely related to phages K1-5, K5, and K1E but encodes a tail protein very similar to that of the distantly related P22. J. Bacteriol. 184: 2833– 2836.
63. Scholl, D.,, J. Kieleczawa,, P. Kemp,, J. Rush,, C. C. Richardson,, C. Merril,, S. Adhya,, and I. J. Molineux. 2004. Genomic analysis of bacteriophages SP6 and K1-5, an estranged subgroup of the T7 supergroup. J. Mol. Biol. 335: 1151– 1171.
64. Sertic, V. 1929. Experiments on bacteriophages that produce lysin zones. 1. The structure of bacteriophage colonies. Zentbl. Bakteriol. Parasitenkd.Abt. II 110: 125– 139.
65. Silver, R. P.,, and E. R. Vimr. 1990. Polysialic acid capsule of E. coli K1, p. 39– 60. In The Bacteria, vol. 11. Academic Press, Inc., New York, N.Y.
66. Smith, H. W.,, and M. B. Huggins. 1982. Successful treatment of experimental E. coli infections in mice using phage: its general superiority over antibiotics. J. Gen. Microbiol. 128: 307– 318.
67. Steinbacher, S.,, S. Miller,, U. Baxa,, N. Budisa,, A. Weintraub,, R. Seckler,, and R. Huber. 1997. Phage P22 tailspike protein: crystal structure of the head-binding domain at 2.3 Å, fully refined structure of the endorhamnosidase at 1.56 Å resolution, and the molecular basis of O-antigen recognition and cleavage. J. Mol. Biol. 267: 865– 880.
68. Stirm, S. 1968. E. coli K bacteriophages. I. Isolation and introductory characterization of five E. coli K bacteriophages. Virology 2: 1107– 1114.
69. Stirm, S.,, and E. Freund-Molbert. 1971. E. coli capsule bacteriophages. II. Morphology. J. Virol. 8: 330– 342.
70.Stirm S., W. Bessler, F. Fehmel, and E. Freund-Molbert. 1971. Isolation of spike-formed particles from bacteriophage lysates. Virology 45: 303– 308.
71. Stirm, S.,, W. Bessler,, F. Fehmel,, E. Freun-Molbert,, and H. Thurow. 1974. On a bacteriophage-induced colanic acid depolymerase. Zentbl. Bakteriol. 226: 26– 35.
72. Sutherland, I. W.,, and J. F. Wilkinson. 1965. Depolymerases for bacterial exopolysaccharides obtained from phage-infected bacteria. J. Gen. Microbiol. 39: 373– 383.
73. Sutherland, I. W. 1966. Phage-induced fucosidases hydrolysing the exopolysaccharide of Klebsiella aerogenes type 54 [A3 (SI)]. Biochem. J. 104: 278– 285.
74. Thurow, H.,, H. Niemann,, C. Rudolph,, and S. Stirm. 1974. Host capsule depolymerase activity of bacteriophage particles active on Klebsiella K20 and K24 strains. Virology 58: 306– 309.
75. Tomlinson, S.,, and P. W. Taylor. 1985. Neuraminidase associated with coliphage E that specifically depolymerizes the Escherichia coli K1 capsular polysaccharide. J. Virol. 55: 374– 378.
76. Vandenbergh, P. A.,, and R. L. Cole. 1986. Cloning and expression in E. coli of the polysaccharide depolymerase associated with bacteriophage-infected Erwinia amylovora. Appl. Environ. Microbiol. 51: 862– 864.
77. van der Ley, P.,, P. De Graaff,, and J. Tommassen. 1986. Shielding of Escherichia coli outer membrane proteins as receptors for bacteriophages and colicins by O-antigenic chains of lipopolysaccharide. J. Bacteriol. 168: 449– 451.
78. van der Wilk, F.,, A. M. Dullemans,, M. Verbeck,, and J. F. Heuvel. 1999. Isolation and characterization of APSE-1, a bacteriophage infecting the secondary endosymbiont of Acyrthosiphon pisum. Virology 262: 104– 113.
79. Whitfield, C.,, and I. S. Roberts. 1999. Structure, assembly, and regulation of expression of capsules in E. coli. Mol. Microbiol. 31: 1307– 1319.
80. Wilson, J. W.,, M. J. Schurr,, C. L. LeBlanc,, R. Ramamurthy,, K. L. Buchanan,, and C. A. Nickerson. 2002. Mechanisms of bacterial pathogenicity. Postgrad. Med. J. 78: 216– 224.
81. Yurewicz, E. C.,, M. A. Ghalambor,, and E. C. Heath. 1971. The structure of Aerobacter aerogenes capsular polysaccharide. J. Biol. Chem. 246: 5596– 5606.

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