Polysaccharases in Biofilms — Sources — Action — Consequences!

  • Ian W. Sutherland


As such a large proportion of the structure of biofilms is composed of polysaccharides secreted by the constituent micro-organisms, the presence of enzymes (polysaccharases) acting on these polymers will inevitably have a very marked effect on the structure and on the integrity of the biofilm. It is also possible that glycosidases capable of cleaving exposed terminal monosaccharide residues may modify both polysaccharides and glycoproteins present in biofilms. Enzymes will derive from a variety of sources and may well differ considerably in their effects. It has also to be remembered that in multi-species biofilms, the collective action of several different enzymes may result in the degradation or alteration of polysaccharides which are resistant to discrete enzymes. Thus, the growth of different enzyme-secreting species in close proximity with intimate cell:cell contact may permit synergistic action of the enzyme mixture within the confines of the biofilm. The effects of polysaccharases may well be moderated if a mixture of polysaccharides is present and removal of one polymer leaves others with similar physical properties intact. The presence of other chemical compounds absorbed to the polysaccharides may also have a moderating influence on enzyme action. Thus simultaneous release of biosurfactants could well affect enzyme activity either positively (enhancing degradation) or negatively (inhibiting destruction of the substrate).


Phage Polysaccharase Polysaccharide lyase 


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  1. Aereboe M, Parolis H, Parolis, LAS (1993) Klebsiella K43 capsular polysaccharide:primary structure and depolymerisation by a viral borne endoglycanase. Carbohydr Res 248: 213–223CrossRefGoogle Scholar
  2. Altmann F, Kwiatkowski B, Stirm S (1986) A bacteriophage associated glycanase cleaving β-pyranosidic linkages of 3-deoxy-D-amnno-2-octulosonic acid (KDO). Biochem Biophys Res Commun 136: 329–335CrossRefGoogle Scholar
  3. Altmann F, Maerz L, Stirm S, Unger FM (1987) Two additional phage-associated glycan hydrolases cleaving ketosidic bonds of 3-deoxy-D-manno-octulosonic acid in capsular polysaccharides of Escherichia coli. FEBS Lett 221: 145–149CrossRefGoogle Scholar
  4. Baxa U, Steinbacher S, Miller S, Weintraub A, Huber R, Seckler R (1996) Interactions of phage P22 tails with their cellular receptor, Salmonella O-antigen polysaccharide. Biophys J 71: 2040–2048CrossRefGoogle Scholar
  5. Bayer ME, Thurow H, Bayer MH (1979) Penetration of the polysaccharide capsule of Escherichia coli (Bi161/42) by bacteriophage K29. Virol 94: 95–118CrossRefGoogle Scholar
  6. Boyd A, Chakrabarty AM (1994) Role of alginate lyase in cell detachment of Pseudomonas aeruginosa. Appl Environ Microbiol 60: 2355–2359Google Scholar
  7. Burne RA, Schilling K, Bowen WH, Yasbin RE (1987) Expression, purification and characterization of an exo-(3-D-fructosidase of Streptococcus mutans. J Bacteriol 169: 4507–4517Google Scholar
  8. Cadmus MC, Jackson LK, Burton KA, Plattner RD, Slodki ME (1982) Biodegradation of xanthan gum by Bacillus sp. Appl Environ Microbiol 44: 5–11Google Scholar
  9. Cescutti P, Paoletti S (1994) On the specificity of a bacteriophage borne endoglycanase for the native capsular polysaccharide produced by Klebsiella pneumoniae SK1 and its derived polymers. Biochem Biophys Res Commun 198: 1128–1134CrossRefGoogle Scholar
  10. Chakraborty AK (1985) Depolymerization of capsular polysaccharide by glycanase activity of Klebsiella bacteriophage 51. Ind J Biochem 22: 22–26Google Scholar
  11. Conti E, Flaibani A, O’Regan M, Sutherland IW (1994) Alginate from Pseudomonas fluorescens and Pseudomonas putida: production and properties. Microbiology 140: 1128–1132CrossRefGoogle Scholar
  12. Davidson IW, Lawson CJ, Sutherland IW (1977) An alginate lyase from Azotobacter vinelandii phage. J Gen Microbiol 98: 223–229Google Scholar
  13. DiFabio JL, Dutton GGS, Parolis H (1984) Preparation of a branched heptasaccharide by bacteriophage depolymerization of Klebsiella K60 capsular polysaccharide. Carbohydr Res 126: 261–269CrossRefGoogle Scholar
  14. Dutton GGS, Merrifield EH (1982) Acylated oligosaccharides from Klebsiella K63 capsular polysaccharide: depolymerization by partial hydrolysis by bacteriophage-borne enzymes. Carbohydr Res 103: 107–128CrossRefGoogle Scholar
  15. Dutton GGS, Lam Z, Lim AVS (1988) N-acety1–13-D-galactosaminidase activity of E. coli phage 44 and the sequencing of E. coli K44 capsular polysaccharide by mass spectrometry. Carbohydr Res 183: 123–125CrossRefGoogle Scholar
  16. Eichholtz H, Freund-Mölbert E, Stirm S (1975) Escherichia coli capsule bacteriophages. J Virol 15: 985–993Google Scholar
  17. Elsässer-Beile U, Stirm S (1981) Substrate specificity of the glycanase activity associated with particles of Klebsiella bacteriophage no 6. Carbohydr Res 88: 315–322CrossRefGoogle Scholar
  18. Fehmel F, Feige U, Niemann H, Stirm S (1975) Escherichia coli capsule bacteriophages VII. Bacteriophage 29-host capsular polysaccharide interactions. J Virol 16: 591–601Google Scholar
  19. Frølund B, Griebe T, Nielsen PH (1995) Enzymatic activity in the activated sludge floc matrix. Appl Microbiol Biotechnol 43: 755–761CrossRefGoogle Scholar
  20. Gilbert HJ, Hazlewood GP (1993) Bacterial cellulases and xylanases. J Gen Microbiol 139: 187–194Google Scholar
  21. Gilkes NR, Claeyssens M, Aebersold R, Henrissat B, Meinke A (1991) Structural and functional relationships in two families of β-1,4-glycanases. Eur J Biochem 202: 367–377CrossRefGoogle Scholar
  22. Glucksman MA, Reuber TL, Walker GC (1993) Genes needed for the modification, polymerization, export and processing of succinoglycan by Rhizobium meliloti: a model for succinoglycan biosynthesis. J Bacteriol 175: 7045–7055Google Scholar
  23. Grimmeke H-D, Knirel YA, Kiesel B, Voges M, Rietschel ET (1994a) Structure of the Acetobacter methanolicus MB 129 capsular polysaccharide and of oligosaccharides resulting from degradation by bacteriophage Acm. Carbohydr Res 259: 45–58CrossRefGoogle Scholar
  24. Grimmeke H-D, Knirel YA, Shashkov AS, Kiesel B, Lauk W, Voges M (1994b) Structure of the capsular polysaccharide and the 0-side chain of the lipolysaccharide from Acetobacter methanolicus. Carbohydr Res 253: 277–282CrossRefGoogle Scholar
  25. Hallenbeck PC, Vimr ER, Yu F, Bassler B, Troy FA (1987) Purification and properties of a bacteriophage-induced endo-N-acetylneuraminidase. J Biol Chem 262: 3553–3561Google Scholar
  26. Hänfling P, Shashkov AS, Jann B, Jann K (1996) Analysis of the enzymatic cleavage (β-elimination) of the capsular K5 polysaccharide of E. coli by the K5-specific coliphage: a re-examination. J Bacteriol 178: 4747–4750Google Scholar
  27. Hou CT, Barnabe N, Greaney K (1986) Biodegradation of xanthan by salt-tolerant aerobic micro-organisms. J Ind Microbiol 1: 31–37CrossRefGoogle Scholar
  28. Hughes KA (1997) Bacterial biofilms and their exopolysaccharides. PhD thesis, Edinburgh UniversityGoogle Scholar
  29. Iwashita S, Kanegasaki S (1976) Deacetylation reaction catalyzed by Salmonella phage. J Biol Chem 251: 5361–5365Google Scholar
  30. Jass J, Costerton JW, Lappin-Scott HM (1995) Assessment of a chemostat-coupled modified Robbins device to study biofilms. J Ind Microbiol 15: 283–289CrossRefGoogle Scholar
  31. Johansen C, Falholt P, Gram L (1997) Enzymatic removal and disinfection of bacterial bio-films. Appl Environ Microbiol 63: 3724–3728Google Scholar
  32. Kennedy L, McDowell K, Sutherland IW (1992) Alginases from Azotobacter species. J Gen Microbiol 138: 2465–2471Google Scholar
  33. Koval SF, Bayer ME (1997) Bacterial capsules–no barrier against Bdellovibrio. Microbiol 143: 749–753CrossRefGoogle Scholar
  34. Kwiatkowski B, Boschek B, Thiele H, Stirm S (1983) Substrate specificity of two bacteriophage associated endo-N-acetylneuraminidases. J Virol 45: 367–374Google Scholar
  35. Lawman P, Bleiweis AW (1991) Molecular cloning of the extracellular endodextranase of Streptococcus salivarius. J Bacteriol 173: 495–504Google Scholar
  36. Legoux R, Lelong P, Jourde C, Feuillerat C, Capdeville J, Sure V, Ferran E, Kaghad M, Delpech B, Shire D, Ferrara P, Loisin G, Salomé M (1996) N-acetyl-heparosan lyase of E. coli K5: gene:gene cloning and expression. J Bacteriol 178: 7260–7264Google Scholar
  37. Long GS, Bryant JM, Taylor PW, Luzio JP (1995) Complete nucleotide sequence of the gene encoding bacteriophage E endosialidase: implications for K1E endosialidase structure and function. Biochem J 309: 43–55Google Scholar
  38. Matthysse AG, White S, Lightfoot R (1995) Genes required for cellulose synthesis in Agrobacterium tumefaciens. J Bacteriol 177: 1069–1075Google Scholar
  39. McNeil M, Darvill J, Darvill AG, Albersheim P, van Veen R, Hooykas P, Schilepoort R, Dell A (1986) The discernible, structural features of the acidic polysaccharides secreted by different Rhizobium species are the same. Carbohydr Res 146: 307–326CrossRefGoogle Scholar
  40. Mishra C, Robbins PW (1995) Specific beta-glucanases as tools for polysaccharide structure determination. Glycobiology 5: 645–654CrossRefGoogle Scholar
  41. Niemann H, Birch-Andersen A, Kjems E, Mansa B, Stirm S (1976) Streptococcal bacteria-phage 12/12-borne hyaluronidase and its characterization as a lyase. Acta Pathol Microbiol Scand 84: 145–153Google Scholar
  42. Niemann H, Kwiatkowski B, Westphal, U, Stirm S (1977) Klebsiella serotype-13 capsular polysaccharide: primary structure and depolymerization by a bacteriophage-borne glycanase. J Bacteriol 130: 366–374Google Scholar
  43. Nimmich W (1997) Degradation studies on Escherichia coli capsular polysaccharides by bacteriophages. FEMS Microbiol Lett 153: 105–110CrossRefGoogle Scholar
  44. Osman SF, Fett WF, Irwin PL, Bailey DG, Parris N, O’Connor JV (1993) Isolation and characterization of an exopolysaccharide depolymerase from Pseudomonas marginalis HTO41B. Curr Microbiol 26: 299–304CrossRefGoogle Scholar
  45. Oyaizu H, Komagata K, Amemura A, Harada T (1982) A succinoglycan-decomposing bacterium, Cytophaga arvensicola sp. nov. J Gen Appl Microbiol 28: 369–388CrossRefGoogle Scholar
  46. Pecina A, Paneque A (1994) Detection of alginate lyase by activity staining after SDS PAGE and subsequent renaturation. Anal Biochem 217: 124–127CrossRefGoogle Scholar
  47. Prehm P, Jann K (1976) Enzymatic action of coliphage 8 and its possible role in infection. J Virol 19: 940–949Google Scholar
  48. Ravenscroft N, Jackson GE, Joao H, Stephen AM (1988) Spectroscopic analysis of oligosaccharides produced by bacteriophage-borne enzyme action on Klebsiella K36 polysaccharide. S Afr J Chem 41: 42Google Scholar
  49. Schiller NL, Monday SR, Boyd C, Keen NT, Ohman DE (1993) Characterization of the Pseudomonas alginate lyase gene (algL): cloning, sequencing and expression in E. coli. J Bacteriol 175: 780–789Google Scholar
  50. Sengha SS, Anderson, AJ, Hacking AJ, Dawes E. (1989) The production of alginate by Pseudomonas mendocina in batch and continuous culture. J Gen Microbiol 135: 795–804Google Scholar
  51. Shabtai Y, Gutnick DL (1985) Exocellular esterase and emulsan release from the cell surface of Acinetobacter calcoaceticus. J Bacteriol 161: 1176–1181Google Scholar
  52. Shaldee PN, Glaser, JH, Conrad HE (1985) A sulfatase specific for glucuronic acid 2-sulfate residues in glycosaminoglycans. J Biol Chem 260: 9146–9149Google Scholar
  53. Shevchik VE, Hugouvieux-Cotte-Pattat N (1997) Identification of a bacterial pectin acetyl esterase in Erwinia chrysanthemi 3937. Mol Microbiol 24: 1285–1301CrossRefGoogle Scholar
  54. Smith ARW, Zamze SE, Hignett RC (1994) Morphology and hydrolytic activity of A7, a typing phage of Pseudomonas syringae pv. morsprunorum. Microbiol 140: 905–913CrossRefGoogle Scholar
  55. Standal R, Iversen T, Coucheron DH, Fjaervik E, Blatny JM, Valla S (1994) A new gene required for cellulose production and a gene encoding cellulolytic activity in Acetobacter xylinum are colocalised with the bcs operon. J Bacteriol 176: 665–672Google Scholar
  56. Steinbacher S, Mille S, Baxa U, Budisa N, Weintraub A, Seckler R, Huber R (1997) Phage P22 tailspike protein–crystal structure of the head-binding domain at 2.3 angstrom, fully refined structure of the endorhamnosidase at 1.56 angstrom resolution, and the molecular basis of O-antigen recognition and cleavage. J Mol Biol 267: 865–880CrossRefGoogle Scholar
  57. Stirm S, Freund-Moelbert E (1971) Escherichia coli capsule bacteriophages II. Morphology. J Virol 8: 330–342Google Scholar
  58. Sutherland IW (1995) Polysaccharide lyases. FEMS Microbiol Rev 16: 323–347CrossRefGoogle Scholar
  59. Sutherland IW (1997) Microbial exopolysaccharides-structural subtleties and their consequences. Pure Appl Chem 69: 1911–1917CrossRefGoogle Scholar
  60. Sutherland IW, Kennedy L (1996) Polysaccharide lyases from gellan-producing Sphingomonas spp. Microbiol 142: 867–872CrossRefGoogle Scholar
  61. Tait MI, Sutherland IW (1989) Synthesis and properties of a mutant type of xanthan. J Appl Bacteriol 66: 457–460CrossRefGoogle Scholar
  62. van Dam JEG, Halbeek H, Kamerling JP, Vliegenhart JFG, Snippe H, Jansze M, Willers JMN (1985) A bacteriophage-associated lyase acting on Klebsiella serotype K5 capsular polysaccharide. Carbohydr Res 142: 338–343CrossRefGoogle Scholar
  63. Voepel KC, Buller CS (1990) Formation of an extracellular energy reserve by Cellulomonas flavigena strain KU. J Ind Microbiol 5: 131–138CrossRefGoogle Scholar
  64. Xun L, Mah RA, Boone DR (1990) Appl Environ Microbiol 56: 3693–3698Google Scholar
  65. Yamazaki M, Thorne L, Mikolajczak MJ, Armentrout RW, Pollock TJ (1996) Linkage of genes essential for synthesis of a polysaccharide capsule in Sphingomonas Strain S88. J Bacteriol 178: 2676 - X2687Google Scholar
  66. Yurewicz EC, Ghalambor MA, Duckworth DH, Heath EC (1971) Catalytic and molecular properties of a phage induced capsular polysaccharide depolymerase. J Biol Chem 246: 5607–5616Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1999

Authors and Affiliations

  • Ian W. Sutherland
    • 1
  1. 1.Institute of Cell and Molecular BiologyEdinburgh UniversityEdinburghUK

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