Cited by 2,327

The DOI matches its Crossref record; 6 of the 6 references it cites were found in a registry or an index.

Physiological heterogeneity in biofilms

Stewart, Philip S., Franklin, Michael J.·2008·Nature Reviews Microbiology

Abstract

Biofilms contain bacterial cells that are in a wide range of physiological states. Within a biofilm population, cells with diverse genotypes and phenotypes that express distinct metabolic pathways, stress responses and other specific biological activities are juxtaposed. The mechanisms that contribute to this genetic and physiological heterogeneity include microscale chemical gradients, adaptation to local environmental conditions, stochastic gene expression and the genotypic variation that occurs through mutation and selection. Here, we discuss the processes that generate chemical gradients in biofilms, the genetic and physiological responses of the bacteria as they adapt to these gradients and the techniques that can be used to visualize and measure the microscale physiological heterogeneities of bacteria in biofilms.

Overview

Integrity signals

Registry

Crossref · 10.1038/nrmicro1838

Cites

6 of 6 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Research works printed but not linked: 137

  1. Hall-Stoodley, L., Costerton, J. W. & Stoodley, P. Bacterial biofilms: from the natural environment to infectious diseases. Nature Rev. Microbiol. 2, 95–108 (2004). · DOI
  2. Mah, T. F. et al. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426, 306–310 (2003). · DOI
  3. Bjarnsholt, T. et al. Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151, 373–383 (2005). · DOI
  4. Jesaitis, A. J. et al. Compromised host defense on Pseudomonas aeruginosa biofilms: characterization of neutrophil and biofilm interactions. J. Immunol. 171, 4329–4339 (2003). · DOI
  5. Bryers, J. D. in Biofilms (eds Characklis, W. G. & Marshall, K. C.) 733–773 (Wiley-Intersciences, New York, 1990).
  6. Bryers, J. D. & Characklis, W. G. in Biofilms (eds Characklis, W. G. & Marshall, K. C.) 671–696 (Wiley-Intersciences, New York, 1990).
  7. Belas, R., Simon, M. & Silverman, M. Regulation of lateral flagella gene transcription in Vibrio parahaemolyticus. J. Bacteriol. 167, 210–218 (1986). · DOI
  8. McCarter, L. & Silverman, M. Surface-induced swarmer cell differentiation of Vibrio parahaemolyticus. Mol. Microbiol. 4, 1057–1062 (1990). · DOI
  9. Davies, D. G. & Geesey, G. G. Regulation of the alginate biosynthesis gene algC in Pseudomonas aeruginosa during biofilm development in continuous culture. Appl. Environ. Microbiol. 61, 860–867 (1995). · DOI
  10. Dalton, H. M. et al. Substratum-induced morphological changes in a marine bacterium and their relevance to biofilm structure. J. Bacteriol. 176, 6900–6906 (1994). · DOI
  11. An, D. & Parsek, M. R. The promise and peril of transcriptional profiling in biofilm communities. Curr. Opin. Microbiol. 10, 292–296 (2007). · DOI
  12. Southey-Pillig, C. J., Davies, D. G. & Sauer, K. Characterization of temporal protein production in Pseudomonas aeruginosa biofilms. J. Bacteriol. 187, 8114–8126 (2005). · DOI
  13. O'Toole, G. A. & Kolter, R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28, 449–461 (1998). Describes a microtitre dish screening assay that was used to identify transposon mutants that are unable to form biofilms, thereby linking distinct genetic loci to biofilm formation. · DOI · Paper page
  14. Patrauchan, M. A., Sarkisova, S. & Franklin, M. J. Strain specific proteome responses of Pseudomonas aeruginosa to biofilm-associated growth and to calcium. Microbiology 153, 3838–3851 (2007). · DOI
  15. Glud, R. N., Ramsing, N. B. & Revsbech, N. P. Photosynthesis and photosynthesis-coupled respiration in natural biofilms quantified with oxygen microsensors. J. Phycol. 28, 51–60 (1992). · DOI
  16. Ramsing, N. B., Kuhl, M. & Jorgensen, B. B. Distribution of sulfate-reducing bacteria, O2, and H2S in photosynthetic biofilms determined by oligonucleotide probes and microelectrodes. Appl. Environ. Microbiol. 59, 3840–3849 (1993). Reports microelectrode measurements of concentration gradients in biofilms, and integrates these with ecological analysis by the use of FISH probes. · DOI
  17. De Beer, D., Stoodley, P., Roe, F. & Lewandowski, Z. Effects of biofilm structure on oxygen distribution and mass transport. Biotechnol. Bioeng. 43, 1131–1138 (2004). · DOI
  18. Zhang, T., Fu, Y. & Bishop, P. Competition for substrate and space in biofilms. Water Environ. Res. 67, 992–1003 (1995). · DOI
  19. Schramm, A. et al. Structure and function of a nitrifying biofilm as determined by in situ hybridization and the use of microelectrodes. Appl. Environ. Microbiol. 62, 4641–4647 (1996). · DOI
  20. Xu, K. D., Stewart, P. S., Xia, F., Huang, C. T. & McFeters, G. A. Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl. Environ. Microbiol. 64, 4035–4039 (1998). · DOI
  21. Okabe, S., Satoh, H. & Watanabe, Y. In situ analysis of nitrifying biofilms as determined by in situ hybridization and the use of microelectrodes. Appl. Environ. Microbiol. 65, 3182–3191 (1999). · DOI
  22. Rani, S. A. et al. Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. J. Bacteriol. 189, 4223–4233 (2007). Experimental demonstration of spatial heterogeneity in oxygen concentration and anabolic protein and DNA synthesis. · DOI
  23. Allewalt, J. P., Bateson, M. M., Revsbech, N. P., Slack, K. & Ward, D. M. Effect of temperature and light on growth of and photosynthesis by Synechococcus isolates typical of those predominating in the octopus spring microbial mat community of Yellowstone National Park. Appl. Environ. Microbiol. 72, 544–550 (2006). · DOI
  24. Ward, D. M. Microbial diversity in natural environments: focusing on fundamental questions. Antonie Van Leeuwenhoek 90, 309–324 (2006). · DOI
  25. Stewart, P. S. Diffusion in biofilms. J. Bacteriol. 185, 1485–1491 (2003). · DOI
  26. Damgaard, L. R., Nielsen, L. P. & Revsbech, N. P. Methane microprofiles in a sewage biofilm determined with a microscale biosensor. Water Res. 35, 1379–1386 (2001). · DOI
  27. De Beer, D., Schramm, A., Santegoeds, C. M. & Kuhl, M. A nitrite microsensor for profiling environmental biofilms. Appl. Environ. Microbiol. 63, 973–977 (1997). · DOI
  28. Kuhl, M., Steuckart, C., Eickert, G. & Jeroschewski, P. A H2S microsensor for profiling biofilms and sediments: application in an acidic lake sediment. Aquat. Microb. Ecol. 15, 201–209 (1998). · DOI
  29. Okabe, S., Itoh, T., Satoh, H. & Watanabe, Y. Analyses of spatial distributions of sulfate-reducing bacteria and their activity in aerobic wastewater biofilms. Appl. Environ. Microbiol. 65, 5107–5116 (1999). · DOI
  30. De Beer, D., Glud, A., Epping, E. & Kuhl, M. A fast-responding CO2 microelectrode for profiling sediments, microbial mats, and biofilms. Limnol. Oceanogr. 42, 1590–1600 (1997). · DOI
  31. Beyenal, H., Davis, C. & Lewandowski, Z. An improved Severinghaus-type carbon dioxide microelectrode for use in biofilms. Sens Actuators B 97, 202–210 (2004). · DOI
  32. Liu, X., Roe, F., Jesaitis, A. J. & Lewandowski, Z. Resistance of biofilms to the catalase inhibitor 3-amino-1,2,4-triazole. Biotechnol. Bioeng. 59, 156–162 (1998). · DOI
  33. De Beer, D., Srinivasan, R. & Stewart, P. S. Direct measurement of chlorine penetration into biofilms during disinfection. Appl. Environ. Microbiol. 60, 4339–4344 (1994). · DOI · Paper page
  34. Jang, A., Szabo, J., Hosni, A. A., Coughlin, M. & Bishop, P. L. Measurement of chlorine dioxide penetration in dairy process pipe biofilms during disinfection. Appl. Microbiol. Biotechnol. 72, 368–376 (2006). · DOI
  35. De Beer, D., Huisman, J., Van den Heuvel, J. & Ottengraf, S. The effect of pH profiles in methanogenic aggregates on the kinetics of acetate conversion. Water Res. 26, 1329–1336 (1992). · DOI
  36. Huang, C. T., Yu, F. P., McFeters, G. & Stewart, P. S. Nonuniform spatial patterns of respiratory activity within biofilms during disinfection. Appl. Environ. Microbiol. 61, 2252–2256 (1995). · DOI
  37. Wentland, E., Stewart, P. S., Huang, C. T. & McFeters, G. A. Spatial variations in growth rate within Klebsiella pneumoniae colonies and biofilm. Biotechnol. Prog. 12, 316–321 (1996). · DOI
  38. Huang, C. T., Xu, K. D., McFeters, G. A. & Stewart, P. S. Spatial patterns of alkaline phosphatase expression within bacterial colonies and biofilms in response to phosphate starvation. Appl. Environ. Microbiol. 64, 1526–1531 (1998). · DOI
  39. Kuhl, M. & Jorgensen, B. B. Microsensor measurements of sulfate reduction and sulfide oxidation in compact microbial communities of aerobic biofilms. Appl. Environ. Microbiol. 58, 1164–1174 (1992). · DOI
  40. Otto, K. & Silhavy, T. J. Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc. Natl Acad. Sci. USA 99, 2287–2292 (2002). · DOI
  41. Kolenbrander, P. E. et al. Communication among oral bacteria. Microbiol. Mol. Biol. Rev. 66, 486–505 (2002). · DOI · Paper page
  42. Stover, C. K. et al. Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406, 959–964 (2000). · DOI
  43. Allegrucci, M. & Sauer, K. Characterization of colony morphology variants isolated from Streptococcus pneumoniae biofilms. J. Bacteriol. 189, 2030–2038 (2007). · DOI
  44. Hansen, S. K., Rainey, P. B., Haagensen, J. A. & Molin, S. Evolution of species interactions in a biofilm community. Nature 445, 533–536 (2007). · DOI
  45. Valle, J., Vergara-Irigaray, M., Merino, N., Penades, J. R. & Lasa, I. σB regulates IS256-mediated Staphylococcus aureus biofilm phenotypic variation. J. Bacteriol. 189, 2886–2896 (2007). · DOI
  46. Yildiz, F. H. & Schoolnik, G. K. 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 (1999). · DOI
  47. McEllistrem, M. C., Ransford, J. V. & Khan, S. A. Characterization of in vitro biofilm-associated pneumococcal phase variants of a clinically relevant serotype 3 clone. J. Clin. Microbiol. 45, 97–101 (2007). · DOI
  48. Koh, K. S. et al. Phenotypic diversification and adaptation of Serratia marcescens MG1 biofilm-derived morphotypes. J. Bacteriol. 189, 119–130 (2007). · DOI
  49. Kirisits, M. J., Prost, L., Starkey, M. & Parsek, M. R. Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 71, 4809–4821 (2005). · DOI
  50. Haussler, S. Biofilm formation by the small colony variant phenotype of Pseudomonas aeruginosa. Environ. Microbiol. 6, 546–551 (2004). · DOI · Paper page
  51. Nguyen, D. & Singh, P. K. Evolving stealth: genetic adaptation of Pseudomonas aeruginosa during cystic fibrosis infections. Proc. Natl Acad. Sci. USA 103, 8305–8306 (2006). · DOI
  52. Hansen, S. K. et al. Characterization of a Pseudomonas putida rough variant evolved in a mixed-species biofilm with Acinetobacter sp. strain C6. J. Bacteriol. 189, 4932–4943 (2007). · DOI
  53. Boles, B. R., Thoendel, M. & Singh, P. K. Self-generated diversity produces “insurance effects” in biofilm communities. Proc. Natl Acad. Sci. USA 101, 16630–16635 (2004). Demonstrated that P. aeruginosa undergoes genetic diversification during short-term biofilm growth, which might allow increased resistance of the population to environmental stresses. · DOI
  54. Cooper, T. F., Beaumont, H. J. & Rainey, P. B. Biofilm diversity as a test of the insurance hypothesis. Microbiology 151, 2815–2816; discussion 2816–2818 (2005). · DOI
  55. Deziel, E., Comeau, Y. & Villemur, R. Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J. Bacteriol. 183, 1195–1204 (2001). · DOI
  56. Baty, A. M. et al. Differentiation of chitinase-active and non-chitinase-active subpopulations of a marine bacterium during chitin degradation. Appl. Environ. Microbiol. 66, 3566–3573 (2000). Used a gfp reporter to the chitinase promoter to demonstrate that biofilms of the marine bacterium Pseudoalteromonas sp. resulted in two distinct subpopulations with respect to chitinase activity; this seems to have been due to stochastic gene expression. · DOI
  57. Baty, A. M., Eastburn, C. C., Techkarnjanaruk, S., Goodman, A. E. & Geesey, G. G. Spatial and temporal variations in chitinolytic gene expression and bacterial biomass production during chitin degradation. Appl. Environ. Microbiol. 66, 3574–3585 (2000). · DOI
  58. Hasty, J., Pradines, J., Dolnik, M. & Collins, J. J. Noise-based switches and amplifiers for gene expression. Proc. Natl Acad. Sci. USA 97, 2075–2080 (2000). · DOI
  59. McAdams, H. H. & Arkin, A. Stochastic mechanisms in gene expression. Proc. Natl Acad. Sci. USA 94, 814–819 (1997). · DOI
  60. Chai, Y., Chu, F., Kolter, R. & Losick, R. Bistability and biofilm formation in Bacillus subtilis. Mol. Microbiol. 67, 254–263 (2007). Demonstrated that matrix polymer production in B. subtilis is under the control of a bistable mechanism that involves the repressor SinR and its anti-repressor SinI. · DOI
  61. Branda, S. S., Chu, F., Kearns, D. B., Losick, R. & Kolter, R. A major protein component of the Bacillus subtilis biofilm matrix. Mol. Microbiol. 59, 1229–1238 (2006). · DOI
  62. Branda, S. S., Gonzalez-Pastor, J. E., Ben-Yehuda, S., Losick, R. & Kolter, R. Fruiting body formation by Bacillus subtilis. Proc. Natl Acad. Sci. USA 98, 11621–11626 (2001). Showed that, when cultured in biofilms, B. subtilis spore formation is spatially organized and occurs in structures that resemble fruiting bodies. · DOI · Paper page
  63. Keren, I., Kaldalu, N., Spoering, A., Wang, Y. & Lewis, K. Persister cells and tolerance to antimicrobials. FEMS Microbiol. Lett. 230, 13–18 (2004). · DOI
  64. Levin, B. R. & Rozen, D. E. Non-inherited antibiotic resistance. Nature Rev. Microbiol. 4, 556–562 (2006). · DOI
  65. Kussell, E., Kishony, R., Balaban, N. Q. & Leibler, S. Bacterial persistence: a model of survival in changing environments. Genetics 169, 1807–1814 (2005). · DOI
  66. Correia, F. F. et al. Kinase activity of overexpressed HipA is required for growth arrest and multidrug tolerance in Escherichia coli. J. Bacteriol. 188, 8360–8367 (2006). · DOI
  67. Korch, S. B. & Hill, T. M. Ectopic overexpression of wild-type and mutant hipA genes in Escherichia coli: effects on macromolecular synthesis and persister formation. J. Bacteriol. 188, 3826–3836 (2006). · DOI
  68. Li, Y. & Zhang, Y. PhoU is a persistence switch involved in persister formation and tolerance to multiple antibiotics and stresses in Escherichia coli. Antimicrob. Agents Chemother. 51, 2092–2099 (2007). · DOI
  69. Spoering, A. L., Vulic, M. & Lewis, K. GlpD and PlsB participate in persister cell formation in Escherichia coli. J. Bacteriol. 188, 5136–5144 (2006). · DOI
  70. Rodriguez, G. G., Phipps, D., Ishiguro, K. & Ridgway, H. F. Use of a fluorescent redox probe for direct visualization of actively respiring bacteria. Appl. Environ. Microbiol. 58, 1801–1808 (1992). · DOI
  71. Schaule, G., Flemming, H. C. & Ridgway, H. F. Use of 5-cyano-2,3-ditolyl tetrazolium chloride for quantifying planktonic and sessile respiring bacteria in drinking water. Appl. Environ. Microbiol. 59, 3850–3857 (1993). · DOI
  72. Zheng, Z. & Stewart, P. S. Growth limitation of Staphylococcus epidermidis in biofilms contributes to rifampin tolerance. Biofilms 1, 31–45 (2004). · DOI
  73. Nielsen, J. L., Aquino de Muro, M. & Nielsen, P. H. Evaluation of the redox dye 5-cyano-2,3-tolyl-tetrazolium chloride for activity studies by simultaneous use of microautoradiography and fluorescence in situ hybridization. Appl. Environ. Microbiol. 69, 641–643 (2003). · DOI
  74. Ullrich, S., Karrasch, B., Hoppe, H., Jeskulke, K. & Mehrens, M. Toxic effects on bacterial metabolism of the redox dye 5-cyano-2,3-ditolyl tetrazolium chloride. Appl. Environ. Microbiol. 62, 4587–4593 (1996). · DOI
  75. Smith, J. J. & McFeters, G. A. Effects of substrates and phosphate on INT (2-(4-iodophenyl)-3-(4-nitrophenyl)-5-phenyl tetrazolium chloride) and CTC (5-cyano-2,3-ditolyl tetrazolium chloride) reduction in Escherichia coli. J. Appl. Bacteriol. 80, 209–215 (1996). · DOI
  76. Korber, D. R., Choi, A., Wolfaardt, G. M., Ingham, S. C. & Caldwell, D. E. Substratum topography influences susceptibility of Salmonella enteritidis biofilms to trisodium phosphate. Appl. Environ. Microbiol. 63, 3352–3358 (1997). · DOI
  77. Lindsay, D., Brozel, V. S., Mostert, J. F. & von Holy, A. Differential efficacy of a chlorine dioxide-containing sanitizer against single species and binary biofilms of a dairy-associated Bacillus cereus and a Pseudomonas fluorescens isolate. J. Appl. Microbiol. 92, 352–361 (2002). · DOI
  78. Hentzer, M. et al. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22, 3803–3815 (2003). · DOI
  79. Teitzel, G. M. & Parsek, M. R. Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl. Environ. Microbiol. 69, 2313–2320 (2003). · DOI
  80. Hope, C. K. & Wilson, M. Analysis of the effects of chlorhexidine on oral biofilm vitality and structure based on viability profiling and an indicator of membrane integrity. Antimicrob. Agents Chemother. 48, 1461–1468 (2004). · DOI
  81. Barraud, N. et al. Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J. Bacteriol. 188, 7344–7353 (2006). · DOI
  82. Berney, M., Hammes, F., Bosshard, F., Weilenmann, H. U. & Egli, T. Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight Kit in combination with flow cytometry. Appl. Environ. Microbiol. 73, 3283–3290 (2007). · DOI
  83. Biggerstaff, J. P. et al. New methodology for viability testing in environmental samples. Mol. Cell. Probes 20, 141–146 (2006). · DOI
  84. Stocks, S. M. Mechanism and use of the commercially available viability stain, BacLight. Cytometry A 61, 189–195 (2004). · DOI
  85. Suci, P. A. & Tyler, B. J. Action of chlorhexidine digluconate against yeast and filamentous forms in an early-stage Candida albicans biofilm. Antimicrob. Agents Chemother. 46, 3522–3531 (2002). · DOI
  86. Banin, E., Brady, K. M. & Greenberg, E. P. Chelator-induced dispersal and killing of Pseudomonas aeruginosa cells in a biofilm. Appl. Environ. Microbiol. 72, 2064–2069 (2006). · DOI
  87. Haagensen, J. A. et al. Differentiation and distribution of colistin- and sodium dodecyl sulfate-tolerant cells in Pseudomonas aeruginosa biofilms. J. Bacteriol. 189, 28–37 (2007). · DOI
  88. Kaneko, Y., Thoendel, M., Olakanmi, O., Britigan, B. E. & Singh, P. K. The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J. Clin. Invest. 117, 877–888 (2007). Together with reference 93, demonstrated the differing antimicrobial susceptibility of spatially segregated populations within a biofilm. · DOI
  89. Auschill, T. M. et al. Spatial distribution of vital and dead microorganisms in dental biofilms. Arch. Oral Biol. 46, 471–476 (2001). · DOI
  90. Honraet, K., Goetghebeur, E. & Nelis, H. J. Comparison of three assays for the quantification of Candida biomass in suspension and CDC reactor grown biofilms. J. Microbiol. Methods 63, 287–295 (2005). · DOI
  91. Hamasaki, K., Taniguchi, A., Tada, Y., Long, R. A. & Azam, F. Actively growing bacteria in the inland sea of Japan, identified by combined bromodeoxyuridine immunocapture and denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 73, 2787–2798 (2007). · DOI
  92. Hjort, K., Lembke, A., Speksnijder, A., Smalla, K. & Jansson, J. K. Community structure of actively growing bacterial populations in plant pathogen suppressive soil. Microb. Ecol. 53, 399–413 (2007). · DOI
  93. Jackson, K. D., Starkey, M., Kremer, S., Parsek, M. R. & Wozniak, D. J. Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J. Bacteriol. 186, 4466–4475 (2004). · DOI
  94. Friedman, L. & Kolter, R. Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J. Bacteriol. 186, 4457–4465 (2004). · DOI
  95. Nivens, D. E., Ohman, D. E., Williams, J. & Franklin, M. J. Role of alginate and its O acetylation in formation of Pseudomonas aeruginosa microcolonies and biofilms. J. Bacteriol. 183, 1047–1057 (2001). · DOI
  96. Whitchurch, C. B., Tolker-Nielsen, T., Ragas, P. C. & Mattick, J. S. Extracellular DNA required for bacterial biofilm formation. Science 295, 1487 (2002). · DOI · Paper page
  97. Allesen-Holm, M. et al. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol. Microbiol. 59, 1114–1128 (2006). · DOI
  98. Sarkisova, S., Patrauchan, M. A., Berglund, D., Nivens, D. E. & Franklin, M. J. Calcium-induced virulence factors associated with the extracellular matrix of mucoid Pseudomonas aeruginosa biofilms. J. Bacteriol. 187, 4327–4337 (2005). · DOI
  99. Neu, T., Swerhone, G. D. & Lawrence, J. R. Assessment of lectin-binding analysis for in situ detection of glycoconjugates in biofilm systems. Microbiology 147, 299–313 (2001). · DOI
  100. Lawrence, J. R., Swerhone, G. D., Kuhlicke, U. & Neu, T. R. In situ evidence for microdomains in the polymer matrix of bacterial microcolonies. Can. J. Microbiol. 53, 450–458 (2007). · DOI
  101. Laue, H. et al. Contribution of alginate and levan production to biofilm formation by Pseudomonas syringae. Microbiology 152, 2909–2918 (2006). · DOI
  102. Strathmann, M., Wingender, J. & Flemming, H. C. Application of fluorescently labelled lectins for the visualization and biochemical characterization of polysaccharides in biofilms of Pseudomonas aeruginosa. J. Microbiol. Methods 50, 237–248 (2002). · DOI
  103. Sternberg, C. et al. Distribution of bacterial growth activity in flow-chamber biofilms. Appl. Environ. Microbiol. 65, 4108–4117 (1999). · DOI
  104. Werner, E. et al. Stratified growth in Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 70, 6188–6196 (2004). · DOI
  105. Teal, T. K., Lies, D. P., Wold, B. J. & Newman, D. K. Spatiometabolic stratification of Shewanella oneidensis biofilms. Appl. Environ. Microbiol. 72, 7324–7330 (2006). Used the unstable gfp reporter gene in S. oneidensis to demonstrate the reproducible stratification of metabolic programming to local environmental conditions and biofilm developmental processes. · DOI
  106. Walters, M. C., Roe, F., Bugnicourt, A., Franklin, M. J. & Stewart, P. S. 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 (2003). · DOI
  107. Borriello, G., Richards, L., Ehrlich, G. D. & Stewart, P. S. Arginine or nitrate enhances antibiotic susceptibility of Pseudomonas aeruginosa in biofilms. Antimicrob. Agents Chemother. 50, 382–384 (2006). · DOI
  108. Bagge, N. et al. Dynamics and spatial distribution of β-lactamase expression in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 48, 1168–1174 (2004). · DOI
  109. De Kievit, T. R. & Iglewski, B. H. Quorum sensing, gene expression, and Pseudomonas biofilms. Methods Enzymol. 310, 117–128 (1999). · DOI
  110. Lequette, Y. & Greenberg, E. P. Timing and localization of rhamnolipid synthesis gene expression in Pseudomonas aeruginosa biofilms. J. Bacteriol. 187, 37–44 (2005). · DOI
  111. Yang, L. et al. Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology 153, 1318–1328 (2007). · DOI
  112. Yarwood, J. M., Bartels, D. J., Volper, E. M. & Greenberg, E. P. Quorum sensing in Staphylococcus aureus biofilms. J. Bacteriol. 186, 1838–1850 (2004). Used a reporter gene in Staphylococcus aureus to follow complex spatial and temporal patterns of expression of a quorum-sensing gene. · DOI
  113. De Kievit, T. R. et al. Multidrug efflux pumps: expression patterns and contribution to antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 45, 1761–1770 (2001). Used reporter genes in P. aeruginosa to quantify and map spatial and temporal patterns of multidrug efflux-pump expression in biofilms. · DOI
  114. Uppuluri, P., Sarmah, B. & Chaffin, W. L. Candida albicans SNO1 and SNZ1 expressed in stationary-phase planktonic yeast cells and base of biofilm. Microbiology 152, 2031–2038 (2006). · DOI
  115. Moller, S. et al. In situ gene expression in mixed-culture biofilms: evidence of metabolic interactions between community members. Appl. Environ. Microbiol. 64, 721–732 (1998). · DOI
  116. Klausen, M., Aaes-Jorgensen, A., Molin, S. & Tolker-Nielsen, T. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol. Microbiol. 50, 61–68 (2003). Used fluorescent-protein-labelled wild-type and motility-mutant strains of P. aeruginosa to show the role of cell migration and type IV pili in biofilm developmental processes. · DOI
  117. Amann, R. I. Fluorescently labelled, rRNA-targeted oligonucleotide probes in the study of microbial ecology. Mol. Ecol. 4, 543–554 (1995). · DOI
  118. DeLong, E. F., Wickham, G. S. & Pace, N. R. Phylogenetic stains: ribosomal RNA-based probes for the identification of single cells. Science 243, 1360–1363 (1989). · DOI
  119. Moller, S., Pedersen, A. R., Poulsen, L. K., Arvin, E. & Molin, S. Activity and three-dimensional distribution of toluene-degrading Pseudomonas putida in a multispecies biofilm assessed by quantitative in situ hybridization and scanning confocal laser microscopy. Appl. Environ. Microbiol. 62, 4632–4640 (1996). · DOI
  120. Xu, K. D., McFeters, G. A. & Stewart, P. S. Biofilm resistance to antimicrobial agents. Microbiology 146, 547–549 (2000). · DOI
  121. Jang, A., Okabe, S., Watanabe, Y., Kim, I. & Bishop, P. Measurement of growth rate of ammonia oxidizing bacteria in partially submerged rotating biological contactor by fluorescent in situ hybridization (FISH). J. Environ. Sci. Eng. 4, 413–420 (2005). · DOI
  122. Lehtola, M. J., Torvinen, E., Miettinen, I. T. & Keevil, C. W. Fluorescence in situ hybridization using peptide nucleic acid probes for rapid detection of Mycobacterium avium subsp. avium and Mycobacterium avium subsp. paratuberculosis in potable-water biofilms. Appl. Environ. Microbiol. 72, 848–853 (2006). · DOI
  123. Ferrari, B. C., Tujula, N., Stoner, K. & Kjelleberg, S. Catalyzed reporter deposition-fluorescence in situ hybridization allows for enrichment-independent detection of microcolony-forming soil bacteria. Appl. Environ. Microbiol. 72, 918–922 (2006). · DOI
  124. Pernthaler, A., Pernthaler, J. & Amann, R. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl. Environ. Microbiol. 68, 3094–3101 (2002). · DOI
  125. Fazi, S., Amalfitano, S., Pernthaler, J. & Puddu, A. Bacterial communities associated with benthic organic matter in headwater stream microhabitats. Environ. Microbiol. 7, 1633–1640 (2005). · DOI
  126. Magnuson, T. S., Neal, A. L. & Geesey, G. G. Combining in situ reverse transcriptase polymerase chain reaction, optical microscopy, and X-ray photoelectron spectroscopy to investigate mineral surface-associated microbial activities. Microb. Ecol. 48, 578–588 (2004). · DOI
  127. Wagner, M., Nielsen, P. H., Loy, A., Nielsen, J. L. & Daims, H. Linking microbial community structure with function: fluorescence in situ hybridization-microautoradiography and isotope arrays. Curr. Opin. Biotechnol. 17, 83–91 (2006). · DOI
  128. Huang, W. E. et al. Raman-FISH: combining stable-isotope Raman spectroscopy and fluorescence in situ hybridization for the single cell analysis of identity and function. Environ. Microbiol. 9, 1878–1889 (2007). · DOI
  129. Lee, N. et al. Combination of fluorescent in situ hybridization and microautoradiography — a new tool for structure-function analyses in microbial ecology. Appl. Environ. Microbiol. 65, 1289–1297 (1999). · DOI
  130. Ouverney, C. C. & Fuhrman, J. A. Combined microautoradiography-16S rRNA probe technique for determination of radioisotope uptake by specific microbial cell types in situ. Appl. Environ. Microbiol. 65, 1746–1752 (1999). · DOI
  131. Kindaichi, T., Ito, T. & Okabe, S. Ecophysiological interaction between nitrifying bacteria and heterotrophic bacteria in autotrophic nitrifying biofilms as determined by microautoradiography-fluorescence in situ hybridization. Appl. Environ. Microbiol. 70, 1641–1650 (2004). · DOI
  132. Ito, T., Nielsen, J. L., Okabe, S., Watanabe, Y. & Nielsen, P. H. Phylogenetic identification and substrate uptake patterns of sulfate-reducing bacteria inhabiting an oxic–anoxic sewer biofilm determined by combining microautoradiography and fluorescent in situ hybridization. Appl. Environ. Microbiol. 68, 356–364 (2002). · DOI
  133. Bonner, R. F. et al. Laser capture microdissection: molecular analysis of tissue. Science 278, 1481–1483 (1997). · DOI
  134. Emmert-Buck, M. R. et al. Laser capture microdissection. Science 274, 998–1001 (1996). · DOI
  135. Rani, S. A., Pitts, B. & Stewart, P. S. Rapid diffusion of fluorescent tracers into Staphylococcus epidermidis biofilms visualized by time lapse microscopy. Antimicrob. Agents Chemother. 49, 728–732 (2005). · DOI
  136. Stewart, P. S. et al. Observations of cell cluster hollowing in Staphylococcus epidermidis biofilms. Lett. Appl. Microbiol. 44, 454–457 (2007). · DOI
  137. Seymour, J. D., Codd, S. L., Gjersing, E. L. & Stewart, P. S. Magnetic resonance microscopy of biofilm structure and impact on transport in a capillary bioreactor. J. Magn. Reson. 167, 322–327 (2004). · DOI

Cited by

Sorted by citations

See all 2,327

Metadata

Authors
Stewart, P. S., & Franklin, M. J.
Venue
Nature Reviews Microbiology
Published
2008-03
Volume
6
Issue
3
Pages
199-210
ISSN
  • 1740-1526
  • 1740-1534
Cited by
2,327
References
6
Language
en

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review