Chapter 10 : A Sticky Business: the Extracellular Polymeric Substance Matrix of Bacterial Biofilms

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

A Sticky Business: the Extracellular Polymeric Substance Matrix of Bacterial Biofilms, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817718/9781555818944_Chap10-1.gif /docserver/preview/fulltext/10.1128/9781555817718/9781555818944_Chap10-2.gif


This chapter is divided into two sections. The first section addresses the different types of biopolymers, which represent the primary components of the extracellular polymeric substances (EPS) matrix. The second section discusses the different functions that EPS has shown or suggested to have in biofilm communities. This section describes some of the different biological macromolecules found in EPS. The chapter discusses two classes of proteins that have been suggested to play a biofilm-specific role in the context of EPS. Lectins are usually associated with cell surface structures, such as pili, peptidoglycan, and the outer membrane of gram-negative bacteria. Alginate lyases constitute a large group of enzymes found in several bacterial species. The biological function of these enzymes depends on the organism and is unclear in certain cases. In general, two functions can be carried out by these enzymes. The first is in eps biosynthesis, where these enzymes process the growing polymer and can regulate chain length. The second is in eps utilization. In this case, enzymatic activity is used to break down eps polymers for use as carbon and energy substrates for growth. Where there are electrostatic repulsive interactions, attachment can occur due to van der Waals interactions, H-bonding, hydrophobic interactions, and specific chemical interactions (such as complexation). The interplay between attractive and repulsive forces is governed by thermodynamics and is described by the landmark Derjaguin Landau-Verwey-Overbeek (DLVO) theory. As research of biofilm communities and EPS continues to advance, specific therapies for biofilm infections and biotechnology applications may emerge.

Citation: Starkey M, Parsek M, Gray K, Chang S. 2004. A Sticky Business: the Extracellular Polymeric Substance Matrix of Bacterial Biofilms, p 174-191. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch10
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

A scanning electron microscopic view of VP-6 attached to a glass coverslip at its pole by means of its holdfast. Bar, 1 μm. Reproduced with permission from Langille and Weiner, 1998.

Citation: Starkey M, Parsek M, Gray K, Chang S. 2004. A Sticky Business: the Extracellular Polymeric Substance Matrix of Bacterial Biofilms, p 174-191. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch10
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Comparative scanning confocal micrographs of nonmucoid and mucoid biofilms grown in a flow chamber apparatus. On the left is a nonmucoid wild-type strain of (PAO1) and on the right is a strain bearing a mutation in the gene rendering it mucoid (PDO300). The cells are constitutively tagged with green fluorescent protein. The large micrograph in the upper left of each panel represents a top-down view of the biofilm. A side view of the biofilm is presented below and to the right of each top-down view. Bar, 20 μm. Reprinted with permission from Hentzer et al., 2001.

Citation: Starkey M, Parsek M, Gray K, Chang S. 2004. A Sticky Business: the Extracellular Polymeric Substance Matrix of Bacterial Biofilms, p 174-191. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch10
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

FIGURE 3 Scanning confocal micrographs of smooth (left) and rugrose (right) variants of 01 El Tor. The micrographs above show a top-down view of the biofilm and the micrographs below show side views of the biofilm. Bar, 10 μm. Reproduced with permission from Yildiz and Schoolnik, 1999.

Citation: Starkey M, Parsek M, Gray K, Chang S. 2004. A Sticky Business: the Extracellular Polymeric Substance Matrix of Bacterial Biofilms, p 174-191. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch10
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Aarons, S. J.,, I. W. Sutherland,, A. M. Chakrabarty,, and M. P. Gallagher. 1997. A novel gene, algK, from the alginate biosynthesis cluster of Pseudomonas aeruginosa. Microbiology 143(Part 2): 641 652.
2. Allison, D. G.,, B. Ruiz,, C. San Jose,, A. Jaspe,, and P. Gilbert. 1998. Extracellular products as mediators of the formation and detachment of Pseudomonas fluorescens biofilms. FEMS Microbiol. Lett. 167: 179 184.
3. Anderl, J. N.,, M. J. Franklin,, and P. S. Stewart. 2000. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother. 44: 1818 1824.
4. Beenken, K. E.,, J. S. Blevins,, and M. S. Smeltzer. 2003. Mutation of sarA in Staphylococcus aureaus limits biofilm formation. Infect. Immun. 71: 4206 4211.
5. Bellemann, P.,, and K. Geider. 1992. Localization of transposon insertions in pathogenicity mutants of Erwinia amylovora and their biochemical characterization. J. Gen. Microbiol. 138(Part 5): 931 940.
6. Bomchil, N.,, P., Watnick,, and R. Kolter. 2003. Identification and characterization of a Vibrio cholerae gene, mbaA, involved in maintenance of biofilm architecture. J. Bacteriol. 185: 1384 1390.
7. Bourgeau, G.,, and B. C. McBride. 1976. Dextranmediated interbacterial aggregation between dextran-synthesizing streptococci and Actinomyces viscosus. Infect. Immun. 13: 1228 1234.
8. Boyd, A.,, and A. M. Chakrabarty. 1995. Pseudomonas aeruginosa biofilms: role of the alginate exopolysaccharide. J. Ind. Microbiol. 15: 162 168.
9. Chang, S. I.,, K. A. Gray,, and M. R. Parsek. 2003. Qualitative and quantitative analysis of the extracellular DNA from Pseudomonas aeruginosa biofilms by pyrolysis/GC/MS. . .
10. Christensen, B. B.,, C. Sternberg,, J. B. Andersen,, L. Eberl,, S. Moller,, M. Givskov,, and S. Molin. 1998. Establishment of new genetic traits in a microbial biofilm community. Appl. Environ. Microbiol. 64: 2247 2255.
11. Christensen, B. E. 1989. The role of extracellular polysaccharides in biofilms. J. Biotechnol. 10: 181 182.
12. Christensen, B. E.,, J. Kjosbakken,, and O. Smidsrod. 1985. Partial chemical and physical characterization of two extracellular polysaccharides produced by marine, periphytic Pseudomonas sp. strain NCMB 2021. Appl. Environ. Microbiol. 50: 837 845.
13. Chu, L.,, T. B. May,, A. M. Chakrabarty,, and T. K. Misra. 1991. Nucleotide sequence and expression of the algE gene involved in alginate biosynthesis by Pseudomonas aeruginosa. Gene 107: 1 10.
14. Conlon, K. M.,, H. Humphreys,, and J. P. O’Gara. 2002. icaR encodes a transcriptional repressor involved in environmental regulation of ica operon expression and biofilm formation in Staphylococcus epidermidis. J. Bacteriol. 184: 4400 4408.
15. Costerton, J. W.,, Z. Lewandowski,, D. E. Caldwell,, D. R. Korber,, and H. M. Lappin-Scott. 1995. Microbiol biofilms. Annu. Rev. Microbiol. 49: 711 745.
16. Costerton, J. W.,, P. S. Stewart,, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284: 1318 1322.
17. Cramton, S. E.,, M. Ulrich,, F. Gotz,, and G. Doring. 2001. Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis. Infect. Immun. 69: 4079 4085.
18. Danese, P. N.,, L. A. Pratt,, and R. Kolter. 2000. Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J. Bacteriol. 182: 3593 3596.
19. Davey, M. E.,, N. C. Caiazza,, and G. A. O’Toole. 2003. Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J. Bacteriol. 185: 1027 1036.
20. Deretic, V.,, R. Dikshit,, W. M. Konyecsni,, A. M. Chakrabarty,, and T. K. Misra. 1989. The algR gene, which regulates mucoidy in Pseudomonas aeruginosa, belongs to a class of environmentally responsive genes. J. Bacteriol. 171: 1278 1283.
21. Deretic, V.,, and W. M. Konyecsni. 1989. Control of mucoidy in Pseudomonas aeruginosa: transcriptional regulation of algR and identification of the second regulator gene, algQ. J. Bacteriol. 171: 3680 3688.
22. Fey, P. D.,, J. S. Ulphani,, F. Gotz,, C. Heilmann,, D. Mack,, and M. E. Rupp. 1999. Characterization of the relationship between polysaccharide intercellular adhesin and hemagglutination in Staphylococcus epidermidis. J. Infect. Dis. 179: 1561 1564.
23. Fiorina, J. C.,, M. Weber,, and J. C. Block. 2000. Occurrence of lectins and hydrophobicity of bacteria obtained from biofilm of hospital catheters and water pipes. J. Appl. Microbiol. 89: 494 500.
24. Fletcher, M.,, and G. D. Floodgate. 1973. An electron-microscopic demonstration of an acidic polysaccharide involved in the adhesion of a marine bacterium to solid surfaces. J. Gen. Microbiol. 74: 325 334.
25. Franklin, M. J.,, C. E. Chitnis,, P. Gacesa,, A. Sonesson,, D. C. White,, and D. E. Ohman. 1994. Pseudomonas aeruginosa AlgG is a polymer level alginate C5-mannuronan epimerase. J. Bacteriol. 176: 1821 1830.
26. Franklin, M. J.,, and D. E. Ohman. 1993. Identification of algF in the alginate biosynthetic gene cluster of Pseudomonas aeruginosa which is required for alginate acetylation. J. Bacteriol. 175: 5057 5065.
27. Franklin, M. J.,, and D. E. Ohman. 1996. Identification of algI and algJ in the Pseudomonas aeruginosa alginate biosynthetic gene cluster which are required for alginate O acetylation. J. Bacteriol. 178: 2186 2195.
28. Franklin, M. J.,, and D. E. Ohman. 2002. Mutant analysis and cellular localization of the AlgI, AlgJ, and AlgF proteins required for O acetylation of alginate in Pseudomonas aeruginosa. J. Bacteriol. 184: 3000 3007.
29. Gerke, C.,, A. Kraft,, R. Sussmuth,, O. Schweitzer,, and F. Gotz. 1998. Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J. Biol. Chem. 273: 18586 18593.
30. Gilboa-Garber, N. 1972. Purification and properties of hemagglutinin from Pseudomonas aeruginosa and its reaction with human blood cells. Biochim. Biophys. Acta 273: 165 173.
31. Gilboa-Garber, N.,, L. Mizrahi,, and N. Garber. 1977. Mannose-binding hemagglutinins in extracts of Pseudomonas aeruginosa. Can. J. Biochem. 55: 975 981.
32. Gilligan, P. H. 1991. Microbiology of airway disease in patients with cystic fibrosis. Clin. Microbiol. Rev. 4: 35 51.
33. Goldberg, J. B.,, and T. Dahnke. 1992. Pseudomonas aeruginosa AlgB, which modulates the expression of alginate, is a member of the NtrC subclass of prokaryotic regulators. Mol. Microbiol. 6: 59 66.
34. Gomez-Suarez, C.,, J. Pasma,, A. J. van der Borden,, J. Wingender,, H. C. Flemming,, H. J. Busscher,, and H. C. van der Mei. 2002. Influence of extracellular polymeric substances on deposition and redeposition of Pseudomonas aeruginosa to surfaces. Microbiology 148: 1161 1169.
35. Gotz, F. 2002. Staphylococcus and biofilms. Mol. Microbiol. 43: 1367 1378.
36. Govan, J. R.,, and V. Deretic. 1996. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60: 539 574.
37. Hanna, A.,, M. Berg,, V. Stout,, and A. Razatos. 2003. Role of capsular colanic acid in adhesion of uropathogenic Escherichia coli. Appl. Environ. Microbiol. 69: 4474 4481.
38. Hausner, M.,, and S. Wuertz. 1999. High rates of conjugation in bacterial biofilms as determined by quantitative in situ analysis. Appl. Environ. Microbiol. 65: 3710 3713.
39. Heilmann, C.,, O. Schweitzer,, C. Gerke,, N. Vanittanakom,, D. Mack,, and F. Gotz. 1996. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol. Microbiol. 20: 1083 1091.
40. Hentzer, M.,, G. M. Teitzel,, G. J. Balzer,, A. Heydorn,, S. Molin,, M. Givskov,, and M. R. Parsek. 2001. Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J. Bacteriol. 183: 5395 5401.
41. Hershberger, C. D.,, R. W. Ye,, M. R. Parsek,, Z. D. Xie,, and A. M. Chakrabarty. 1995. The algT (algU) gene of Pseudomonas aeruginosa, a key regulator involved in alginate biosynthesis, encodes an alternative sigma factor (sigma E) Proc. Natl. Acad. Sci. USA 92: 7941 7945.
42. Jahn, A.,, and P. H. Nielsen. 1998. Cell biomass and exopolymer composition in sewer biofilms. Water Sci. Technol. 37: 17 24.
43. Jang, A.,, S. M. Kim,, S. Y. Kim,, S. G. Lee,, and I. S. Kim. 2001. Effects of heavy metals (Cu, Pb, and Ni) on the compositions of EPS in biofilms. Water Sci. Technol. 43: 41 48.
44. John, M.,, H. Rohrig,, J. Schmidt,, U. Wieneke,, and J. Schell. 1993. Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase. Proc. Natl. Acad. Sci. USA 90: 625 629.
45. Kao, C. C.,, E. Barlow,, and L. Sequeira. 1992. Extracellular polysaccharide is required for wildtype virulence of Pseudomonas solanacearum. J. Bacteriol. 174: 1068 1071.
46. Karthikeyan, S.,, and T. J. Beveridge. 2002. Pseudomonas aeruginosa biofilms react with and precipitate toxic soluble gold. Environ. Microbiol. 4: 667 675.
47. Kato, J.,, T. K. Misra,, and A. M. Chakrabarty. 1990. AlgR3, a protein resembling eukaryotic histone H1, regulates alginate synthesis in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 87: 2887 2891.
48. Kennedy, L.,, K. R. McDowell,, and I. W. Sutherland. 1992. Alginases from azotobacter species. J. Gen. Microbiol. 138: 2465 2471.
49. Kidambi, S. P.,, G. W. Sundin,, D. A. Palmer,, A. M. Chakrabarty,, and C. L. Bender. 1995. Copper as a signal for alginate synthesis in Pseudomonas syringae pv. syringae. Appl. Environ. Microbiol. 61: 2172 2179.
50. Knobloch, J. K.,, K. Bartscht,, A. Sabottke,, H. Rohde,, H. H. Feucht,, and D. Mack. 2001. Biofilm formation by Staphylococcus epidermidis depends on functional RsbU, an activator of the sigB operon: differential activation mechanisms due to ethanol and salt stress. J. Bacteriol. 183: 2624 2633.
51. Langille, S. E.,, and R. M. Weiner. 1998. Spatial and temporal deposition of hyphomonas strain VP-6 capsules involved in biofilm formation. Appl. Environ. Microbiol. 64: 2906 2913.
52. Lawman, P.,, and A. S. Bleiweis. 1991. Molecular cloning of the extracellular endodextranase of Streptococcus salivarius. J. Bacteriol. 173: 7423 7428.
53. Leid, J. G.,, M. E. Shirtliff,, J. W. Costerton,, and A. P. Stoodley. 2002. Human leukocytes adhere to, penetrate, and respond to Staphylococcus aureus biofilms. Infect. Immun. 70: 6339 6345.
54. Ma, M.,, and J. W. Eaton. 1992. Multicellular oxidant defense in unicellular organisms. Proc. Natl. Acad. Sci. USA 89: 7924 7928.
55. Ma, S.,, D. J. Wozniak,, and D. E. Ohman. 1997. Identification of the histidine protein kinase KinB in Pseudomonas aeruginosa and its phosphorylation of the alginate regulator algB. J. Biol. Chem. 272: 17952 17960.
56. Mack, D.,, W. Fisher,, A. Krokotsch,, K. Leopold,, R. Hartmann,, H. Egge,, and R. Laufs. 1996. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J. Bacteriol. 178: 175 183.
57. Mack, D. J.,, Riedewald, , H. Rohde, , T. Magnus, , H. H. Feucht, , H. A. Elsner, , R. Laufs, , and M. E. Rupp. 1999. Essential functional role of the polysaccharide intercellular adhesin of Staphylococcus epidermidis in hemagglutination. Infect. Immun. 67: 1004 1008.
58. Maharaj, R.,, T. B. May,, S. K. Wang,, and A. M. Chakrabarty. 1993. Sequence of the alg8 and alg44 genes involved in the synthesis of alginate by Pseudomonas aeruginosa. Gene 136: 267 269.
59. May, T. B.,, and A. M. Chakrabarty. 1994. Pseudomonas aeruginosa: genes and enzymes of alginate synthesis. Trends Microbiol. 2: 151 157.
60. Mayer, C.,, R. Moritz,, C. Kirschner,, W. Borchard,, R. Maibaum,, J. Wingender,, and H. C. Flemming. 1999. The role of intermolecular interactions: studies on model systems for bacterial biofilms. Int. J. Biol. Macromol. 26: 3 16.
61. Mejia-Ruiz, H.,, J. Guzman,, S. Moreno,, G. Soberon-Chavez,, and G. Espin. 1997. The Azotobacter vinelandii alg8 and alg44 genes are essential for alginate synthesis and can be transcribed from an algD-independent promoter. Gene 199: 271 277.
62. Meluleni, G. J.,, M. Grout,, D. J. Evans,, and G. B. Pier. 1995. Mucoid Pseudomonas aeruginosa growing in a biofilm in vitro are killed by opsonic antibodies to the mucoid exopolysaccharide capsule but not by antibodies produced during chronic lung infection in cystic fibrosis patients. J. Immunol. 155: 2029 2038.
63. Mitchell, E.,, C. Houles,, D. Sudakevitz,, M. Wimmerova,, C. Gautier,, S. Perez,, A. M. Wu,, N. Gilboa-Garber,, and A. Imberty. 2002. Structural basis for oligosaccharide-mediated adhesion of Pseudomonas aeruginosa in the lungs of cystic fibrosis patients. Nat. Struct. Biol. 9: 918 921.
64. Monday, S. R.,, and N. L. Schiller. 1996. Alginate synthesis in Pseudomonas aeruginosa: the role of AlgL (alginate lyase) and AlgX. J. Bacteriol. 178: 625 632.
65. Nichols, W. W.,, S. M. Dorrington,, M. P. Slack,, and H. L. Walmsley. 1988. Inhibition of tobramycin diffusion by binding to alginate. Antimicrob. Agents Chemother. 32: 518 523.
66. Nichols, W. W.,, M. J. Evans,, M. P. Slack,, and H. L. Walmsley. 1989. The penetration of antibiotics into aggregates of mucoid and nonmucoid Pseudomonas aeruginosa. J. Gen. Microbiol. 135(Part 5): 1291 1303.
67. Nickel, J. C.,, I. Ruseska,, J. B. Wright,, and J. W. Costerton. 1985. Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrob. Agents Chemother. 27: 619 624.
68. Nielsen, P. H.,, A. Jahn,, and R. Palmgren. 1997. Conceptual model for production and composition of exopolymers in biofilms. Water Sci. Technol. 36: 11 19.
69. Nimtz, M.,, A. Mort,, T. Domke,, V. Wray,, Y. Zhang,, F. Qui,, D. Coplin,, and K. Geider. 1996. Structure of amylovoran, the capsular exopolysaccharide from the fire blight pathogen Erwinia amylovora. Carbohydr. Res. 287: 59 76.
70. Nivens, D. E.,, D. E. Ohman,, J. Williams,, and M. J. Franklin. 2001. Role of alginate and its O acetylation in formation of Pseudomonas aeruginosa microcolonies and biofilms. J. Bacteriol. 183: 1047 1057.
71. Ofek, I.,, D. L. Hasty,, and R. J. Doyle(ed.). 2003. Bacterial Adhesion to Animal Cells and Tissues. ASM Press, Washington, D.C.
72. Ott, C. M.,, D. F. Day,, D. W. Koenig,, and D. L. Pierson. 2001. The release of alginate lyase from growing Pseudomonas syringae pathovar phaseolicola. Curr. Microbiol. 42: 78 81.
73. Parad, R. B.,, C. J. Gerard,, D. Zurakowski,, D. P. Nichols,, and G. B. Pier. 1999. Pulmonary outcome in cystic fibrosis is influenced primarily by mucoid Pseudomonas aeruginosa infection and immune status and only modestly by genotype. Infect. Immun. 67: 4744 4750.
74. Picout, D. R.,, and S. B. Ross-Murphy. 2003. Rheology of biopolymer solutions and gels. Sci. World J. 3: 105 121.
75. Pratten, J.,, S. J. Foster,, P. F. Chan,, M. Wilson,, and S. P. Nair. 2001. Staphylococcus aureus accessory regulators: expression within biofilms and effect of adhesion. Microbes Infect. 3: 633 637.
76. Rachid, S.,, K. Ohlsen,, U. Wallner,, J. Hacker,, M. Hecker,, and W. Ziebuhr. 2000. Alternative transcription factor sigma(B) is involved in regulation of biofilm expression in a Staphylococcus aureus mucosal isolate. J. Bacteriol. 182: 6824 6826.
77. Rehm, B. H.,, and S. Valla. 1997. Bacterial alginates: biosynthesis and applications. Appl. Microbiol. Biotechnol. 48: 281 288.
78. Reverchon, S.,, and J. Robert-Baudouy. 1987. Regulation of expression of pectate lyase genes pe1A, pe1D, and pe1E in Erwinia chrysanthemi. J. Bacteriol. 169: 2417 2423.
79. Rickard, A. H.,, S. A. Leach,, C. M. Buswell,, N. J. High,, and P. S. Handley. 2000. Coaggregation between aquatic bacteria is mediated by specific-growth-phase-dependent lectin-saccharide interactions. Appl. Environ. Microbiol. 66: 431 434.
80. Roychoudhury, S.,, T. B. May,, J. F. Gill,, S. K. Singh,, D. S. Feingold,, and A. M. Chakrabarty. 1989. Purification and characterization of guanosine diphospho-D-mannose dehydrogenase. A key enzyme in the biosynthesis of alginate by Pseudomonas aeruginosa. J. Biol. Chem. 264: 9380 9385.
81. Rupp, M. E.,, P. D. Fey,, C. Heilmann,, and F. Gotz. 2001. Characterization of the importance of Staphylococcus epidermidis autolysin and polysaccharide intercellular adhesin in the pathogenesis of intravascular catheter-associated infection in a rat model. J. Infect. Dis. 183: 1038 1042.
82. Rupp, M. E.,, J. S. Ulphani,, P. D. Fey,, K. Bartscht,, and D. Mack. 1999a. Characterization of the importance of polysaccharide intercellular adhesin/hemagglutinin of Staphylococcus epidermidis in the pathogenesis of biomaterial-based infection in a mouse foreign body infection model. Infect. Immun. 67: 2627 2632.
83. Rupp, M. E.,, J. S. Ulphani,, P. D. Fey,, and D. Mack. 1999b. Characterization of Staphylococcus epidermidis polysaccharide intercellular adhesin/ hemagglutinin in the pathogenesis of intravascular catheter-associated infection in a rat model. Infect. Immun. 67: 2656 2659.
84. Sabra, W.,, A. P. Zeng,, and W. D. Deckwer. 2001. Bacterial alginate: physiology, product quality and process aspects. Appl. Microbiol. Biotechnol. 56: 315 325.
85. Schembri, M. A.,, L. Hjerrild,, M. Gjermansen,, and P. Klemm. 2003. Differential expression of the Escherichia coli autoaggregation factor antigen 43. J. Bacteriol. 185: 2236 2242.
86. Schlictman, D.,, M. Kubo,, S. Shankar,, and A. M. Chakrabarty. 1995. Regulation of nucleoside diphosphate kinase and secretable virulence factors in Pseudomonas aeruginosa: roles of algR2 and algH. J. Bacteriol. 177: 2469 2474.
87. Schurr, M. J.,, H. Yu,, J. C. Boucher,, N. S. Hibler,, and V. Deretic. 1995. Multiple promoters and induction by heat shock of the gene encoding the alternative sigma factor AlgU (sigma E) which controls mucoidy in cystic fibrosis isolates of Pseudomonas aeruginosa. J. Bacteriol. 177: 5670 5679.
88. Schurr, M. J.,, H. Yu,, J. M. Martinez-Salazar,, J. C. Boucher,, and V. Deretic. 1996. Control of AlgU, a member of the sigma E-like family of stress sigma factors, by the negative regulators MucA and MucB and Pseudomonas aeruginosa conversion to mucoidy in cystic fibrosis. J. Bacteriol. 178: 4997 5004.
89. Shigeta, M.,, G. Tanaka,, H. Komatsuzawa,, M. Sugai,, H. Suginaka,, and T. Usui. 1997. Permeation of antimicrobial agents through Pseudomonas aeruginosa biofilms: a simple method. Chemotherapy 43: 340 345.
90. Skjak-Braek, G. 1992. Alginates: biosyntheses and some structure-function relationships relevant to biomedical and biotechnological applications. Biochem. Soc. Trans. 20: 27 33.
91. Sundin, G. W.,, S. Shankar,, S. A. Chugani,, B. A. Chopade,, A. Kavanaugh-Black,, and A. M. Chakrabarty. 1996. Nucleoside diphosphate kinase from Pseudomonas aeruginosa: characterization of the gene and its role in cellular growth and exopolysaccharide alginate synthesis. Mol. Microbiol. 20: 965 979.
92. Sutherland, I. 2001. Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147: 3 9.
93. Sutherland, I. W. 1999. Polysaccharases for microbial exopolysaccharides. Carbohydr. Polym. 38: 319 328.
94. Sutherland, I. W. 1995. Polysaccharide lyases. FEMS Microbiol. Rev. 16: 323 347.
95. Teitzel, G. M.,, and M. R. Parsek. 2003. Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl. Environ. Microbiol. 69: 2313 2320.
96. Vrany, J. D.,, P. S. Stewart,, and P. A. Suci. 1997. Comparison of recalcitrance to ciprofloxacin and levofloxacin exhibited by Pseudomonas aeruginosa biofilms displaying rapid-transport characteristics. Antimicrob. Agents Chemother. 41: 1352 1358.
97. Vuong, C.,, H. L. Saenz,, F. Gotz,, and M. Otto. 2000. Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. J. Infect. Dis. 182: 1688 1693.
98. Walters, M. C., III,, F. Roe, , A. Bugnicourt, , M. J. Franklin, , and P. S. Stewart. 2003. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob. Agents Chemother. 47: 317 323.
99. Webb, J. S.,, L. S. Thompson,, S. James,, T. Charlton,, T. Tolker-Nielsen,, B. Koch,, M. Givskov,, and S. Kjelleberg. 2003. Cell death in Pseudomonas aeruginosa biofilm development. J. Bacteriol. 185: 4585 4592.
100. Whitchurch, C. B.,, R. A. Alm,, and J. S. Mattick. 1996. The alginate regulator AlgR and an associated sensor FimS are required for twitching motility in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 93: 9839 9843.
101. Whitchurch, C. B.,, T. Tolker-Nielsen,, P. C. Ragas,, and J. S. Mattick. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295: 1487.
102. Whiteley, M.,, M. G. Bangera,, R. E. Bumgarner,, M. R. Parsek,, G. M. Teitzel,, S. Lory,, and E. P. Greenberg. 2001. Gene expression of Pseudomonas aeruginosa biofilms. Nature 413: 860 864.
103. Winzer, K.,, C. Falconer,, N. C. Garber,, S. P. Diggle,, M. Camara,, and P. Williams. 2000. The Pseudomonas aeruginosa lectins PA-IL and PAIIL are controlled by quorum sensing and by RpoS. J. Bacteriol. 182: 6401 6411.
104. Worlitzsch, D.,, R. Tarran,, M. Ulrich,, U. Schwab,, A. Cekici,, K. C. Meyer,, P. Birrer,, G. Bellon,, J. Berger,, T. Weiss,, K. Botzenhart,, J. R. Yankaskas,, S. Randell,, R. C. Boucher,, and G. Doring. 2002. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J. Clin. Invest. 109: 317 325.
105. Wozniak, D. J.,, T. J. Wyckoff,, M. Starkey,, R. Keyser,, P. Azadi,, G. A. O’Toole,, and M. R. Parsek. 2003. Alginate is not a significant component of the extracellular polysaccharide matrix of PA14 and PAO1 Pseudomonas aeruginosa biofilms. Proc. Natl. Acad. Sci. USA 100: 7907 7912.
106. Xie, Z. D.,, C. D. Hershberger,, S. Shankar,, R. W. Ye,, and A. M. Chakrabarty. 1996. Sigma factor-anti-sigma factor interaction in alginate synthesis: inhibition of AlgT by MucA. J. Bacteriol. 178: 4990 4996.
107. Yildiz, F. H.,, and G. K. Schoolnik. 1999. Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc. Natl. Acad. Sci. USA 96: 4028 4033.
108. Yu, H.,, M. Mudd,, J. C. Boucher,, M. J. Schurr,, and V. Deretic. 1997. Identification of the algZ gene upstream of the response regulator algR and its participation in control of alginate production in Pseudomonas aeruginosa. J. Bacteriol. 179: 187 193.
109. Zheng, Z.,, and P. S. Stewart. 2002. Penetration of rifampin through Staphylococcus epidermidis biofilms. Antimicrob. Agents Chemother. 46: 900 903.
110. Ziebuhr, W.,, K. Dietrich,, M. Trautmann,, and M. Wilhelm. 2000. Chromosomal rearrangements affecting biofilm production and antibiotic resistance in a Staphylococcus epidermidis strain causing shunt-associated ventriculitis. Int. J. Med. Microbiol. 290: 115 120.
111. Ziebuhr, W.,, V. Krimmer,, S. Rachid,, I. Lossner,, F. Gotz,, and J. Hacker. 1999. A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256. Mol. Microbiol. 32: 345 356.
112. Ziebuhr, W.,, I. Lossner,, S. Rachid,, K. Dietrich,, F. Gotz,, and J. Hacker. 2000. Modulation of the polysaccharide intercellular adhesin (PIA) expression in biofilm forming Staphylococcus epidermidis. Analysis of genetic mechanisms. Adv. Exp. Med. Biol. 485: 151 157.
113. Zielinski, N. A.,, A. M., Chakrabarty,, and A. Berry. 1991. Characterization and regulation of the Pseudomonas aeruginosa algC gene encoding phosphomannomutase. J. Biol. Chem. 266: 9754 9763.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error