Structural and functional characteristics of bacterial biofilms

Microbiology

Volumn 79, Issue 4, 2010, Pages 413-423

  Smirnova, T A ^a   Didenko, L V ^a   Azizbekyan, R R ^b   Romanova, Yu M ^a  

^a INSTITUTE OF BIOMEDICAL CHEMISTRY   (Russian Federation)

^b STATE RESEARCH INSTITUTE OF GENETICS AND SELECTION OF INDUSTRIAL MICROORGANISMS   (Russian Federation)

Author keywords

bacteria; biofilms; flagella; matrix; microscopy; pili; spores

Indexed keywords

BACTERIA (MICROORGANISMS);

EID: 77955786884     PISSN: 00262617     EISSN: None     Source Type: Journal    
DOI: 10.1134/S0026261710040016     Document Type: Review

References (74)

1. Miller, M. B. and Bassler, B. L., Quorum Sensing in Bacteria, Annu. Rev. Microbiol., 2001, vol. 55, pp. 165-199.
2. Gintsburg, A. L., Il'ina, T. S., and Romanova, Yu. M., Quorum Sensing or Social Behavior in Bacteria, Zh. Mikrobiol. Epidemiol. Immunol., 2003, no. 5, pp. 86-93.
3. Costerton, J. W., Stewart, P. S., and Greenberg, E. P., Bacterial Biofilm: a Common Cause of Persistent Infections, Science, 1999, pp. 318-322.
4. Zapata, M., Silva, F., Luza, F., Wilkens, M., and Riquelme, C., The Inhibitory Effect of Biofilm Produced by Wild Bacterial Isolates to the Larval Settlement of the Fouling Ascidia Ciona intenstinalis and Pyura praeputalis, Biofilms, 2007, vol. 10, no. 1, pp. 1-4.
5. Bais, H. B., Fall, R., and Vivanco, J. M., Biocontrol of Bacillus subtilis against Infection of Arabidopsis Root by Pseudomonas syringae Is Facilated by Biofilm Formation and Surfactin Production, Plant. Physiol., 2004, vol. 134, pp. 307-319.
6. Davey, M. E. and O'Tool, G. A., Microbial Biofilm: From Ecology to Molecular Genetics, Microbiol. Mol. Biol. Rev., 2000, vol. 64, no. 4, pp. 847-867.
7. Donlan, R. M., Biofilms: Microbial Life on Surfaces, Emerg. Infect. Dis, 2002, vol. 8, pp. 1-20.
8. Il'ina, T. S., Romanova, Yu. M., and Gintsburg, A. L., Biofilms as a Mode of Existence of Bacteria in External Environment and Host Body: The Phenomenon, Genetic Control, and Regulation Systems of Development, Genetika, 2004, vol. 40, no. 11, pp. 1445-1456 [Russ. J. Genet. (Engl. Transl.), vol. 40, no. 11, pp. 1189-1198].
9. Nikolaev, Yu. A. and Plakunov, V. K., Biofilm-"City of Microbes" or an Analogue of Multicellular Organisms?, Mikrobiologiya, 2007, vol. 76, no. 2, pp. 149-163 [Microbiology (Engl. Transl.), vol. 76, no. 2, pp. 125-138].
10. Monroe, D., Looking for Chinks in the Armor of Bacterial Biofilm, Plos Biol, 2007, vol. 5, pp. 1-4.
11. Lemon, K. P., Earl, A. M., Vlamakis, H. C., Aguilar, C., and Kolter, R., Biofilm Development with an Emphasis on Bacillus subtilis, Curr. Top Microbiol. Immunol., 2008, vol. 322, pp. 1-16.
12. O'Toole, G. A. and Kolter, R., Flagellar and Twitching Motility Are Necessary for Pseudomonas aeruginosa Biofilm Development, Mol. Microbiol., 1998, vol. 30, pp. 295-304.
13. Romanova, Yu. M., Alekseeva, N. V., Smirnova, T. A., Andreev, A. L., Didenko, L. V., and Gintsburg, A. L., Capacity for Biofilm Formation in Artificial Systems in Different Salmonella typhimurium Strains, Zh. Mikrobiol. Epidemiol. Immunol., 2006, no. 4, pp. 38-42.
14. Jiron, A. G., Torres, A. G., Freer, E., and Kaper, J. B., The Flagella of Enteropathogenic Escherichia coli Mediate Adherence to Epithelial Cells, Mol. Microbiol., 2002, vol. 44, pp. 361-379.
15. Zvyagintsev, D. G., Vzaimodeistvie mikroorganizmov s tverdymi poverkhnostyami (Interaction of Microorganisms with Solid Surfaces), Moscow: Mosk. Gos. Univ., 1973.
16. Dalin, M. V. and Fish, N. G., Adhesion of Microorganisms, Itogi Nauki I Tekhniki. VINITI. Mikrobiologiya, 1985, vol. 16, pp. 3-107.
17. Dunny, M. W., Bacterial Adhesion: Seen Any Good Biofilm Lately?, Clin. Microbiol. Rev., 2002, vol. 15, pp. 155-166.
18. Severina, L. O., Bacterial S Layers, Mikrobiologiya, 1995, vol. 64, no. 6, pp. 725-733.
19. Nuccio, S.-P. and Braumer, A. J., Evolution of the Chaperone/Usher Assembly Pathway: Fimbrial Classification Goes Greek, Microbiol. Mol. Biol. Rev., 2007, vol. 71, no. 4, pp. 551-573.
20. Chapman, M. R., Robinson, L. S., Pinkner, S. J., Roth, R., Heuser, J., Hammar, M., Normark, S., and Hultgren, S. J., Role of Esherichia coli Operons in Directing Amyloid Fiber Formation, Science, 2002, vol. 295, pp. 851-855.
21. Fronzes, R., Remaut, H., and Waksman, G., Architectures and Biogenesis of Non-Flagellar Protein Appendages in Gram-Negative Bacteria, EMBO J., 2008, vol. 27, pp. 2271-2280.
22. White, A. P., Gibson, D. L., Collinson, S. K., Banser, P. A., and Kay, W. W., Extracellular Polysaccharide Associated with Thin Aggregative Fimbriae of Salmonella enterica serovar enteritidis, J. Bacteriol., 2003, vol. 185, pp. 5398-5407.
23. Cleary, J., Lai, L.-C., Shaw, R. K., Staatman-Iwanowska, A., Donnenberg, M. S., Frankel, G., and Knutton, S., Enteropathogenic Escherichia coli (EPEC) Adhesion to Intestinal Epithelial Cells: Role of Bundle-Forming Pili (BFP), EspA Filaments and Intimin, Microbiology (UK), 2004, vol. 150, pp. 527-538.
24. Tuohami, A., Jericho, M. H., Boyd, J. M., and Beveridge, T. J., Nanoscale Characterization and Determination of Adhesion Forces of Pseudomonas aeruginosa Pili by Using Atomic Force Microscopy, J. Bacteriol., 2006, vol. 188, pp. 370-377.
25. Sajjan, S. U., Sun, I., Goldstian, R., and Forstner, J. F., Cabl (Cbl) Type 11 Pili of Cystic Fibrosis-Associated Burkholderia (Pseudomonas) cepacia: Nucleotide Sequence of cblA Major Subunit Pilin and Novel Morphology of Assembled Appendage Fibers, J. Bacteriol., 1995, vol. 177, pp. 1030-1038.
26. Budzig, J. M. and Sheewind, O., Pili Prove Pertinent to Enterococcal Endocarditis, J. Clin. Invest., 2006, vol. 116, pp. 2582-2584.
27. McCarter, L. L., Showalter, R. E., and Silwerman, M. R., Genetic Analysis of Surface Sensing in Vibrio parahaemolyticum, Biofouling, 1992, vol. 5, pp. 163-175.
28. Prigent-Combaret, C., Vidal, O., Dorell, C., and Lejeunf, P., Abiotic Surface Sensing and Biofilm-Dependent Regulation of Gene Expression in Esherichia coli, J. Bacteriol., 1999, vol. 181, pp. 5993-6002.
29. Branda, S. S., Vik, A., Friedman, L., and Kolter, R., Biofilms: The Matrix Revisted, TRENDS in Microbiol., 2005, vol. 13, no. 1, pp. 21-25.
30. Hentzer, M., Teitzel, G. M., Balzer, G. J., Heydorn, A., Molin, S., Givscov, M., and Parsek, M. R., Alginate Overproduction Affects Pseudomonas aeruginosa Biofilm Structure and Function, J. Bacteriol., 2001, vol. 138, pp. 5395-5401.
31. Da Re, S. and Ghigo, J.-M., A CsgD-Independent Pathway for Cellulose Producton and Biofilm Formation in Esherichia coli, J. Bacteriol., 2006, vol. 188, no. 8, pp. 3073-3083.
32. Wai, S. N., Mizunoe, Y., Takade, A., Kawabata, S.-I., and Yoshida, S.-I., Vibrio cholerae 01 Strain TSI-4 Produces the Exopolysaccharide Materials That Determine Colony Morphology, Stress Resistance, and Biofilm Formation, Appl. Environ. Microbiol., 1998, vol. 64, no. 10, pp. 3648-3655.
33. Cunha, M. V., Sousa, S. A., Leitao, J. H., Moreira, L. M., Videiraa, P. A., and Sa-Correira, I., Studies on the Involvement of the Exopolysaccharide Produced by Cystic Fibrosis-Associated Isolate of the Burkholderia cepacia Complex in Biofilm Formation and in Persistence of Respiratory Infection, J. Clin. Microbiol., 2004, vol. 42, pp. 3052-3058.
34. Zogaj, X., Nimtz, M., Ronde, M., Borkranz, W., and Romling, U., The Multicellular Morphotipes of Salmonella typhimurium and E. coli Produce Cellulose as the Second Component of the Extracellular Matrix, Mol. Microbiol., 2001, vol. 39, pp. 1452-1463.
35. Ledeboer, N. A. and Bradley, J., Exopolysaccharide Sugar Contribute to Biofilm Formation by Salmonella enterica serovar typhimurium on Hep-2 Cells and Chicken Intestinal Epithelium, J. Bacteriol., 2005, vol. 187, pp. 3214-3226.
36. Branda, S. S., Chu, F., Kears, D. B., Losick, R., and Kolter, K., A Major Component of the Bacillus subtilis Biofilm Matrix, Mol. Microbiol., 2006, vol. 59, pp. 1229-1238.
37. O'Tool, G. and Kolter, R., Initiation of Biofilm Formation in Pseudomonas fluorescens WCS356 Proceeds via Multiple, Convergent Signaling Pathways: a Genetic Analysis, Mol. Microbiol., 1998, vol. 28, pp. 449-461.
38. Romling, U., Sierralta, D. W., Eriksson, K., and Normark, S., Multicellular and Aggregative Behavior of Salmonella typhimurium Strains Is Controlled by Mutations in the agfD Promoter, Mol. Microbiol., 1998, vol. 28, pp. 249-264.
39. Yi, K., Rasmussen, A. W., Gudlavalleti, S. K., Stephens, D. S., and Stojiljkovie, I., Biofilm Formation by Neisseria meningitides, Infect. Immun., 2004, vol. 72, pp. 6132-6138.
40. Azizbekyan, R. R., Smirnova, T. A., Grigor'eva, T. M., Kuznetsova, N. I., and Nikolaenko, M. A., Application of Congo Red for Selection of Gram-Positive Bacterial Strains Producing Regular S Layers, Biotekhnologiya, 2007, no. 6, pp. 5-11.
41. Solano, C., Garsia, B., Valle, J., Berasian, C., Ghigo, J.-M., Gamazo, K., and Lasa, I., Genetic Analysis of Salmonella enteritidis Biofilm Formation: Crucial Role of Cellulose, Mol. Microbiol., 2002, vol. 43, pp. 793-808.
42. Shelud'ko, A. V., Kulibyakina, O. V., Shirokov, A. A., Petrova, L. P., Matora, L. Yu., and Katsy, G. I., The Effect of Mutations Affecting Synthesis of Lipopolysaccharides and Calcofluor-Binding Polysaccharides on Biofilm Formation by Azospirillum brasilense, Mikrobiologiya, 2008, vol. 77, no. 3, pp. 358-363 [Microbiology (Engl. Transl.), vol. 77, no. 3, pp. 313-317].
43. Trchoo, N., Biofilm and Food Industry, J. Sci. Technol, 2003, vol. 25, pp. 807-815.
44. Filoche, S. K., Zhu, M., and Wu, C. D., In situ Biofilm Formation by Multi-Species Oral Bacteria Under Flowing and Anaerobic Condition, J. Dental Res., 2004, vol. 83, pp. 802-806.
45. Luft, J. H., Ruthenium Red and Violet. 1. Chemistry, Purification, Methods of Use for Electron Microscopy and Mechanism of Action, Anat. Record, 1971, vol. 171, pp. 347-368.
46. Marrie, T. J. and Costerton, J. W., Morphology of Bacterial Attachment to Cardiac Pacemaker Leads and Power Packs, J. Clin. Microbiol., 1984, vol. 19, pp. 911-914.
47. Karlyshev, A. V., McCrossan, M. V., and Wren, B. W., Demonstration of Polysaccharide Capsule in Campylobacter jejuni Using Electron Microscopy, Infect. Immun., 2001, vol. 69, pp. 1-13.
48. Hunter, R. C. and Beveridge, T. G., High-Resolution Visualization of Pseudomonas aeruginosa PAOI Biofilms by Freeze-Substitution Transmission Electron Microscopy, J. Bacteriol., 2005, vol. 187, pp. 7619-7630.
49. Zahler, J. and Stewart, S. P., Transmission Electron Microscopic Study of Antibiotic Action on Klebsiella pneumoniae Biofilm, Antimicrob. Agents Chemother., 2002, vol. 46, pp. 2679-2683.
50. Gosteva, V. V., Klitsunova, N. V., and Bondarenko, V. M., Interaction of Clostridium difficile with Bacterial Communities of Parietal Biofilm in Mouse Colon, Zh. Mikrobiol. Epidemiol. Immunol., 2009, no. 1, pp. 3-6.
51. Beveridge, T. J., Visualizing Bacterial Cell Walls and Biofilms, Microbe, 2006, vol. 1, no. 6, pp. 1-6.
52. Costerton, J. W., Irvin, R. T., and Cheng, K. J., The Role of Bacterial Surface Structures in Pathogenesis, in Crit. Rev. Microbiol., Isenberg, H. D., Ed., Boca Raton: CRC Press, 1981, vol. 8, pp. 303-338.
53. Zogaj, X., Bokranz, W., Nimtz, M., and Romling, U., Production of Cellulose and Curli Fimbriae by Members of the Family Enterobacteriaceae Isolated from the Human Gastrointestinal Tract, Infect. Immun., 2003, vol. 71, pp. 4151-4158.
54. Erlandsen, S. L., Kristich, C. H., Dunny, C., and Wells, C. H., High-Resolution Visualization of Microbial Glycocalix with Low-Voltage Scanning Electron Microscopy: Depends of Cationic Dyes, J. Histochim. Cytochem, 2004, vol. 52, pp. 1427-1435.
55. Kania, R. E., Lamers, G. E. M., Vonk, M., Huy, P. T. B., Hemistra, P. S., Blomering, G. V., and Grote, J. J., Demonstration of Bacterial Cells and Glycocalyx in Human Tonsils, Arch. Otolaryngol., 2007, vol. 133, pp. 115-121.
56. Kolari, M., Attachment Mechanisms and Properties of Bacterial Biofilms on Non-Living Surfaces, Academic Dissertation in Microbiology, Univ. Helsinki, 2003.
57. Skillman, L. C., Sutherland, I. W., and Jones, M. V., Co-Operative Biofilm Formation Between Two Species of Enterobacteriacae, Biofilms, 1997, pp. 119-127.
58. Jonas, K., Tomenius, H., Kader, A., Staffan, N., Romling, U., Belova, L. M., and Melefore, O., Roles of Curli, Cellulose and Bap A in Salmonella Biofilm Morphology Studied by Atomic Force Microscopy, BMC Microbol., 2007, vol. 7, pp. 1-13.
59. Smirnova, T. A., Didenko, L. V., Andreev, A. L., Alekseeva, N. V., Stepanova, T. A., and Romanova, Yu. M., Electron Microscopic Study of Burkholderia cepacia Biofilms, Mikrobiologiya, 2008, vol. 77, no. 1, pp. 63-70 [Microbiology (Engl. Transl.), vol. 77, no. 1, pp. 55-61].
60. Didenko, L. V., Konstantinova, N. D., Romanova, Yu. M., Alekseeva, N. V., Andreevskaya, S. G., and Gintsburg, A. L., Ultrastructural Organization of Salmonella typhimurium Cells at Prolonged Starvatin and transition to a Nonculturable State, Mol. Genet. Mikrobiol. Virusol., 2000, no. 3, pp. 21-26.
61. Romanova, Yu. M., Smirnova, T. A., Andreev, A. L., Il'ina, T. S., Didenko, L. V., and Gintsburg, A. L., Formation of Biofilms as an Example of the Social Behavior of Bacteria, Mikrobiologiya, 2006, vol. 75, no. 4, pp. 481-485 [Microbiology (Engl. Transl.), vol. 75, no. 4, pp. 481-485].
62. Greiner, L. L., Edwards, J. L., Shao, J., Rabinak, C., Entz, D., and Apicella, M. A., Biofilm Formation by Neisseria gonorrhoeae, Infect. Immun., 2005, vol. 73, pp. 1964-1970.
63. Rybal'chenko, O. V., The Electron Microscopic Study of Cell-to-Cell Interactions between Antagonistic Microorganisms, Mikrobiologiya, 2006, vol. 75, no. 4, pp. 550-555 [Microbiology (Engl. Transl.), vol. 75, no. 4, pp. 476-480].
64. Beveridge, T. J., Structures of Gram-Negative Cell Walls and Their Derived Membrane Vesicles, J. Bacteriol., 1999, vol. 181, pp. 4725-4733.
65. Allan, N. D., Kool, C., Sokol, A., and Beveridge, T. J., Putative Virulence Factors Are Released in Associated with Membrane Vesicles from Burkholderia cepacia, Can. J. Microbiol., 2003, vol. 49, pp. 613-624.
66. Kreft, J.-U., Biofilm Promote Altruism, Arch. Microbiol., 2004, vol. 150, pp. 2751-2760.
67. Stoodely, P., Wilson, S., Hall-Stoodley, S., Boyle, J. D., Lappin-Scott, H. M., and Costerton, J. W., Growth and Detachment of Cell Cluster from Mature Mixed-Species Biofilm, Appl. Environ. Microbiol., 2001, vol. 67, no. 12, pp. 5608-5613.
68. El'-Registan, G. I., Mulyukin, A. L., Nikolaev, Yu. A., Suzina, N. E., Gal'chenko, V. F., and Duda, V. I., Adaptogenic Functions of Extracellular Autoregulators of Microorganisms, Mikrobiologiya, 2006, vol. 75, no. 4, pp. 446-456 [Microbiology (Engl. Transl.), vol. 75, no. 4, pp. 380-389].
69. Wijman, J. G. E., de Leeuw, P. P. L., Moezelar, R., Zwietering, M. H., and Abee, T., Air-Liquid Interface Biofilm of Bacillus cereus: Formation, Sporulation and Dispersion, J. Appl. Environ. Microbiol., 2007, vol. 73, pp. 1481-1488.
70. Koshikawa, T., Yamazaki, M., Yoshimi, M., Ogawa, S., Yamada, A., Watabe, K., and Torii, M., Surface Hydrophobicity of Spores of Bacillus Spp., J. Gen. Microbiol., 1989, vol. 135, pp. 2717-2722.
71. Duda, V. I., Cytological Traits of Spore-Forming Bacteria, Usp. Mikrobiol., 1982, vol. 17, pp. 87-117.
72. Driks, A., Surface Appendages of Bacterial Spores, Mol. Microbiol., 2007, vol. 63, pp. 623-625.
73. Smirnova, T. A., Kulinich, L. I., Galperin, M. Yu., and Azizbekyan, R. R., Subspecies-Specific Haemagglutination Patterns of Fimbriated Bacillus thuringiensis Spores, FEMS Microbiol. Letts., 1991, vol. 90, pp. 1-4.
74. Smirnova, T. A., Poglazova, M. N., Mashkovtseva, A. V., Kulinich, L. I., Gal'perin, M. Yu., and Azizbekyan, R. R., Investigation of Adhesive Characteristics of the Spores of Bacillus thuringiensis subsp. galleriae and dendrolimus, Mikrobiologiya, 1991, vol. 60, no. 4, pp. 697-703.