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Pseudomonas aeruginosa Displays Multiple Phenotypes during Development as a Biofilm
Open accessAbstract
Complementary approaches were employed to characterize transitional episodes in Pseudomonas aeruginosa biofilm development using direct observation and whole-cell protein analysis. Microscopy and in situ reporter gene analysis were used to directly observe changes in biofilm physiology and to act as signposts to standardize protein collection for two-dimensional electrophoretic analysis and protein identification in chemostat and continuous-culture biofilm-grown populations. Using these approaches, we characterized five stages of biofilm development: (i) reversible attachment, (ii) irreversible attachment, (iii) maturation-1, (iv) maturation-2, and (v) dispersion. Biofilm cells were shown to change regulation of motility, alginate production, and quorum sensing during the process of development. The average difference in detectable protein regulation between each of the five stages of development was 35% (approximately 525 proteins). When planktonic cells were compared with maturation-2 stage biofilm cells, more than 800 proteins were shown to have a sixfold or greater change in expression level (over 50% of the proteome). This difference was higher than when planktonic P. aeruginosa were compared with planktonic cultures of Pseudomonas putida . Las quorum sensing was shown to play no role in early biofilm development but was important in later stages. Biofilm cells in the dispersion stage were more similar to planktonic bacteria than to maturation-2 stage bacteria. These results demonstrate that P. aeruginosa displays multiple phenotypes during biofilm development and that knowledge of stage-specific physiology may be important in detecting and controlling biofilm growth.
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“If this occurs, these microbes change their metabolism11 and a new ecology is set up with a modified microbiome.12,13”
From The Innate Immune System in Acute and Chronic Wounds (2016) · cites this paper as [11]
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Cites
High resolution two-dimensional electrophoresis of proteins.
O’Farrell, P. H. (1975) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)41496-8 · Cited by 19,248
Mass Spectrometric Sequencing of Proteins from Silver-Stained Polyacrylamide Gels
Shevchenko, A., Wilm, M. S., Vorm, O., & Mann, M. (1996) · Analytical Chemistry · doi:10.1021/ac950914h · Cited by 8,996
A simplification of the protein assay method of Lowry et al. which is more generally applicable
Peterson, G. L. (1977) · Analytical Biochemistry · doi:10.1016/0003-2697(77)90043-4 · Cited by 8,531
Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels
Blum, H., Beier, H., & Gross, H. J. (1987) · Electrophoresis · doi:10.1002/elps.1150080203 · Cited by 4,150
Biofilm formation as microbial development
O'Toole, G., Kaplan, H. B., & Kolter, R. (2000) · Annual Review of Microbiology · doi:10.1146/annurev.micro.54.1.49 · Cited by 3,571
The Involvement of Cell-to-Cell Signals in the Development of a Bacterial Biofilm
Davies, D. G., Parsek, M. R., Pearson, J. P., Iglewski, B. H., Costerton, J. W., & Greenberg, E. P. (1998) · Science · doi:10.1126/science.280.5361.295 · Cited by 3,396
Self-citationFlagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development
O'Toole, G. A., & Kolter, R. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.01062.x · Cited by 2,697
O'Toole, G. A., & Kolter, R. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00797.x · Cited by 2,537
Görg, A., Postel, W., & Günther, S. (1988) · Electrophoresis · doi:10.1002/elps.1150090913 · Cited by 2,401
Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry
Wilm, M., Shevchenko, A., Houthaeve, T., Breit, S., Schweigerer, L., Fotsis, T., & Mann, M. (1996) · Nature · doi:10.1038/379466a0 · Cited by 1,674
Research works printed but not linked: 1
- Harry, J. L., M. R. Wilkins, B. R. Herbert, N. H. Packer, A. A. Gooley, and K. L. Williams. 2000. Proteomics: capacity versus utility. Electrophoresis6:1071-1081.
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Sorted by citations
Bacterial biofilms: from the Natural environment to infectious diseases
Hall‐Stoodley, L., Costerton, J. W., & Stoodley, P. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro821 · Cited by 7,133
Self-citationBiofilms as Complex Differentiated Communities
Stoodley, P., Sauer, K., Davies, D. G., & Costerton, J. W. (2002) · Annual Review of Microbiology · doi:10.1146/annurev.micro.56.012302.160705 · Cited by 3,151
“(51) have recently shown that quorum sensing does not account for all biofilm-specific protein production inP.”
BackgroundMethodInfluentialSelf-citationUnderstanding biofilm resistance to antibacterial agents
Davies, D. G. (2003) · Nature Reviews Drug Discovery · doi:10.1038/nrd1008 · Cited by 2,786
Self-citationPhysiological heterogeneity in biofilms
Stewart, P. S., & Franklin, M. J. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1838 · Cited by 2,483
Survival strategies of infectious biofilms
Fux, C. A., Costerton, J. W., Stewart, P. S., & Stoodley, P. (2004) · Trends in Microbiology · doi:10.1016/j.tim.2004.11.010 · Cited by 1,797
Self-citationMolecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria
Hall, C. W., & Mah, T. (2017) · FEMS Microbiology Reviews · doi:10.1093/femsre/fux010 · Cited by 1,831
Bacterial Biofilms: An Emerging Link to Disease Pathogenesis
Parsek, M. R., & Singh, P. K. (2003) · Annual Review of Microbiology · doi:10.1146/annurev.micro.57.030502.090720 · Cited by 1,557
Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors
Hentzer, M., Wu, H., Andersen, J. B., Riedel, K., Rasmussen, T. B., Bagge, N., Kumar, N., Schembri, M. A., Song, Z., Kristoffersen, P., et al. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg366 · Cited by 1,440
Self-citationThe biofilm life cycle: expanding the conceptual model of biofilm formation
Sauer, K., Stoodley, P., Goeres, D. M., Hall‐Stoodley, L., Burmølle, M., Stewart, P. S., & Bjarnsholt, T. (2022) · Nature Reviews Microbiology · doi:10.1038/s41579-022-00767-0 · Cited by 1,581
Self-citationThe role of bacterial biofilms in chronic infections
Bjarnsholt, T. (2013) · Apmis · doi:10.1111/apm.12099 · Cited by 1,259
Bacterial biofilm formation on implantable devices and approaches to its treatment and prevention
Khatoon, Z., McTiernan, C. D., Suuronen, E. J., Mah, T., & Alarcon, E. I. (2018) · Heliyon · doi:10.1016/j.heliyon.2018.e01067 · Cited by 1,227
“The formation is typically classified into three stages; (i) initial attachment (reversible and irreversible), (ii) maturation of microcolonies, and (iii) dispersion/detachment [1, 8, 21, 23, 27, 64, 65, 66, 67, 68].”
BackgroundStewart, P. S. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.5.1485-1491.2003 · Cited by 1,188
Signals, Regulatory Networks, and Materials That Build and Break Bacterial Biofilms
Karatan, E., & Watnick, P. I. (2009) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00041-08 · Cited by 1,099
“As the authors of the first study (281) point out, the ability of motile cells to swim away from the voids FIG.”
BackgroundStaphylococcus aureus biofilms
Archer, N. K., Mazaitis, M. J., Costerton, J. W., Leid, J. G., Powers, M. E., & Shirtliff, M. E. (2011) · Virulence · doi:10.4161/viru.2.5.17724 · Cited by 1,072
Self-citationBiofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants
Klausen, M., Heydorn, A., Ragas, P. C., Lambertsen, L. M., Aaes‐Jørgensen, A., Molin, S., & Tolker‐Nielsen, T. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03525.x · Cited by 1,055
“Another study showed that a non-flagellated mutant of the P. aeruginosa PA14 strain attached poorly in comparison with the wild type in a flowthrough system with glutamic acid medium (Sauer et al., 2002).”
BackgroundSharma, S. J., Mohler, J. L., Mahajan, S. D., Schwartz, S. A., Bruggemann, L., & Aalinkeel, R. (2023) · Microorganisms · doi:10.3390/microorganisms11061614 · Cited by 1,150
Biofilm formation in food industries: A food safety concern
Srey, S., Jahid, I. K., & Ha, S. (2012) · Food Control · doi:10.1016/j.foodcont.2012.12.001 · Cited by 1,005
Resistance of bacterial biofilms to disinfectants: a review
Bridier, A., Briandet, R., Thomas, V., & Dubois‐Brissonnet, F. (2011) · Biofouling · doi:10.1080/08927014.2011.626899 · Cited by 997
“…in the oxidative stress response have also been shown to be induced in biofilms of L. monocytogenes, P. aeruginosa, E. coli or Tannerella forsythia (Sauer et al. 2002; Tremoulet et al. 2002; Ren et al. 2004; Pham et al. 2010) and may afford protection for bacteria against the activity of oxidizing…”
BackgroundBiofilm Dispersal: Mechanisms, Clinical Implications, and Potential Therapeutic Uses
Kaplan, J. B. (2010) · Journal of Dental Research · doi:10.1177/0022034509359403 · Cited by 949
“…bacteria to surfaces (O’Toole and Kolter, 1998; Chiang and Burrows, 2003); (ii) repressed in mature biofilms (Sauer and Camper, 2001; Whiteley et al., 2001; Sauer et al., 2002, 2004); and (iii) induced upon biofilm dispersal (Jackson et al., 2002; Sauer et al., 2002; Purevdorj-Gage et al., 2005).”
BackgroundInfluentialRumbaugh, K. P., & Sauer, K. (2020) · Nature Reviews Microbiology · doi:10.1038/s41579-020-0385-0 · Cited by 989
Self-citationWagner, V., Bushnell, D. S., Passador, L., Brooks, A. I., & Iglewski, B. H. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.7.2080-2095.2003 · Cited by 923
mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa
Choi, K., & Schweizer, H. P. (2006) · Nature Protocols · doi:10.1038/nprot.2006.24 · Cited by 882
Abiotic Stress Responses and Microbe-Mediated Mitigation in Plants: The Omics Strategies
Meena, K. K., Sorty, A. M., Bitla, U. M., Choudhary, K., Gupta, P., Pareek, A., Singh, D. P., Prabha, R., Sahu, P. K., Gupta, V. K., et al. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.00172 · Cited by 849
“Characteristic versatile metabolic scope and unique biofilm forming ability of the members of this genus (Kertesz et al., 1993; Sauer et al., 2002, 2004; Arevalo-Ferro et al., 2005; VerBerkmoes et al., 2006) permits these species to thrive well under diverse environmental conditions, thus making…”
BackgroundHickman, J. W., Tifrea, D. F., & Harwood, C. S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507170102 · Cited by 848
Biofilm Formation by Plant-Associated Bacteria
Danhorn, T., & Fuqua, C. (2007) · Annual Review of Microbiology · doi:10.1146/annurev.micro.61.080706.093316 · Cited by 825
Rhamnolipid Surfactant Production Affects Biofilm Architecture in Pseudomonas aeruginosa PAO1
Davey, M. E., Caiazza, N. C., & O’Toole, G. A. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.3.1027-1036.2003 · Cited by 790
“aeruginosa biofilms, including the macrocolonies surrounded by fluidfilled channels, is a regulated developmental process requiring distinct genetic surface structures and regulatory elements (23, 29, 30, 35).”
BackgroundBiofilm in Implant Infections: Its Production and Regulation
Costerton, J. W., Montanaro, L., & Arciola, C. R. (2005) · The International Journal of Artificial Organs · doi:10.1177/039139880502801103 · Cited by 804
“This process is partially controlled by quorum sensing, an interbacterial communication mechanism that is dependent on population density and associated with radical (more than 50%) changes in protein expression patterns (36).”
BackgroundSelf-citationBiofilmsPreprint
López, D., Vlamakis, H. C., & Kolter, R. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a000398 · Cited by 796
Involvement of Nitric Oxide in Biofilm Dispersal of Pseudomonas aeruginosa
Barraud, N., Hassett, D. J., Hwang, S.-H., Rice, S. A., Kjelleberg, S. J., & Webb, J. S. (2006) · Journal of Bacteriology · doi:10.1128/jb.00779-06 · Cited by 785
“Previous studies have suggested that dispersal of single organisms from biofilms is linked to the motility of a subpopulation of cells (32, 48, 53).”
BackgroundBjarnsholt, T., Alhede, M., Alhede, M., Eickhardt-Sørensen, S. R., Moser, C., Kühl, M., Jensen, P. Ø., & Høiby, N. (2013) · Trends in Microbiology · doi:10.1016/j.tim.2013.06.002 · Cited by 764
Making 'sense' of metabolism: autoinducer-2, LUXS and pathogenic bacteria
Vendeville, A., Winzer, K., Heurlier, K., Tang, C. M., & Hardie, K. R. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1146 · Cited by 674
“harveyi, LuxP (which clearly has a role in cell–cell communication), revealed that the protein was complexed to a FURANOSYLBORATEDIESTER33 (3A-methyl5,6-dihydro-furo(2,3-d)(1,3,2)dioxaborole-2,2,6, 6A-tetraol; S-THMF-borate) (FIGS 1,2).”
BackgroundValentini, M., & Filloux, A. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.r115.711507 · Cited by 665
“How do we reconcile the global effect of the intracellular c-di-GMP concentration on stimulating the biofilm lifestyle with the discrete actions of c-di-GMP on biofilm formation? Biofilm formation is considered as a developmental process that includes attachment to and movement on the surface, formation of microcoloni…”
BackgroundNadell, C. D., Xavier, J. B., & Foster, K. R. (2008) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2008.00150.x · Cited by 686
The application of biofilm science to the study and control of chronic bacterial infections
Costerton, W. J., Veeh, R., Shirtliff, M. E., Pasmore, M. E., Post, C., & Ehrlich, G. D. (2003) · Journal of Clinical Investigation · doi:10.1172/jci20365 · Cited by 650
“The genes expressed in a biofilm differ from those expressed in the corresponding planktonic cell more than they do from the genes expressed in a spore or in the biofilm cells of another species (28).”
BackgroundSelf-citationNeurotransmitters: The Critical Modulators Regulating Gut–Brain Axis
Mittal, R., Debs, L. H., Patel, A. P., Nguyen, D., Patel, K. V., O’Connor, G., Grati, M., Mittal, J., Yan, D. L. S., Eshraghi, A. A., et al. (2016) · Journal of Cellular Physiology · doi:10.1002/jcp.25518 · Cited by 661
“This bacterial communication is necessary for biofilm formation, swarming motility, induction of gene expression, exopolysaccharide production, and the exchange of virulence factors (Sauer et al., 2002; Liu et al., 2015; Abraham, 2016).”
BackgroundHorizontal Gene Transfer of Antibiotic Resistance Genes in Biofilms
Michaelis, C., & Grohmann, E. (2023) · Antibiotics · doi:10.3390/antibiotics12020328 · Cited by 700
“The original concept of a biofilm life cycle is based on in vitro Pseudomonas aeruginosa biofilms and has been widely generalized to describe all biofilms [22].”
BackgroundThe application of biofilm science to the study and control of chronic bacterial infections
Costerton, W. J., Veeh, R., Shirtliff, M. E., Pasmore, M. E., Post, C., & Ehrlich, G. D. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200320365 · Cited by 632
Self-citationThe developmental model of microbial biofilms: ten years of a paradigm up for review
Monds, R. D., & O’Toole, G. A. (2009) · Trends in Microbiology · doi:10.1016/j.tim.2008.11.001 · Cited by 642
Quorum sensing and swarming migration in bacteria
Daniels, R., Vanderleyden, J., & Michiels, J. J. (2003) · FEMS Microbiology Reviews · doi:10.1016/j.femsre.2003.09.004 · Cited by 622
Regulation of flagellar motility during biofilm formation
Guttenplan, S. B., & Kearns, D. B. (2013) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12018 · Cited by 645
“Once biofilm formation has been initiated, flagellar gene expression decreases as a biofilm matures (O’Toole & Kolter, 1998; Vallet et al., 2001; Whitely et al., 2001; Sauer et al., 2002; Klausen et al., 2003; Wolfgang et al., 2004).”
BackgroundInfluentialA Fatty Acid Messenger Is Responsible for Inducing Dispersion in Microbial Biofilms
Davies, D. G., & Marques, C. N. H. (2008) · Journal of Bacteriology · doi:10.1128/jb.01214-08 · Cited by 604
“aeruginosa PAO1 were grown in modified EPRI medium in continuous culture at room temperature in a biofilm tube reactor (27).”
BackgroundMethodInfluentialSelf-citationCell Death in Pseudomonas aeruginosa Biofilm Development
Webb, J. S., Thompson, L. S., James, S., Charlton, T., Tolker‐Nielsen, T., Koch, B. M., Givskov, M., & Kjelleberg, S. J. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.15.4585-4592.2003 · Cited by 600
“aeruginosa are more similar to planktonic cells than to mature biofilm cells (51).”
BackgroundDental plaque: biological significance of a biofilm and community life‐style
Marsh, P. (2005) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2005.00790.x · Cited by 599
Biofilm-Specific Antibiotic Resistance
Mah, T. (2012) · Future Microbiology · doi:10.2217/fmb.12.76 · Cited by 589
Friedman, L., & Kolter, R. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.14.4457-4465.2004 · Cited by 528
Antimicrobial resistance of Pseudomonas aeruginosa biofilms
Drenkard, E. (2003) · Microbes and Infection · doi:10.1016/j.micinf.2003.08.009 · Cited by 521
Characterization of Nutrient-Induced Dispersion in Pseudomonas aeruginosa PAO1 Biofilm
Sauer, K., Cullen, M., Rickard, A. H., Zeef, L. A. H., Davies, D. G., & Gilbert, P. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.21.7312-7326.2004 · Cited by 518
“The developmental life cycle of biofilms comes full circle when biofilm cells disperse (50).”
BackgroundMethodInfluentialSelf-citationBiofilm-associated persistence of food-borne pathogens
Bridier, A., Sanchez-Vizuete, P., Guilbaud, M., Piard, J.-C., Naïtali, M., & Briandet, R. (2014) · Food Microbiology · doi:10.1016/j.fm.2014.04.015 · Cited by 519
Hinsa-Leasure, S. M., Espinosa‐Urgel, M., Ramos, J. L., & O’Toole, G. A. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03615.x · Cited by 498
“Following up on these previous studies, Sauer et al. (2002) made detailed observations of early biofilm development, and also observed reversible and subsequent irreversible attachment steps by P. aeruginosa.”
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Gupta, P., Sarkar, S., Das, B., Bhattacharjee, S., & Tribedi, P. (2016) · Archives of Microbiology · doi:10.1007/s00203-015-1148-6 · Cited by 493
“Microbial biofilm develops through five consecutive stages such as initial reversible attachment, irreversible attachment, maturation stage I, maturation stage II and dispersion (Sauer et al. 2002; Stoodley et al. 2002b).”
BackgroundFlagella and bacterial pathogenicity
Duan, Q., Zhou, M., Zhu, L., & Zhu, G. (2012) · Journal of Basic Microbiology · doi:10.1002/jobm.201100335 · Cited by 489
“(iii) formation of microcolonies, and (iv) biofilm maturation [19, 20].”
BackgroundA review of the scientific evidence for biofilms in wounds
Percival, S. L., Hill, K. E., Williams, D. W., Hooper, S. J., Thomas, D. W., & Costerton, J. W. (2012) · Wound Repair and Regeneration · doi:10.1111/j.1524-475x.2012.00836.x · Cited by 482
“In fact, Pseudomonas aeruginosa is known to display multiple phenotypes during development as a biofilm.(7) Biofilm-grown bacteria also produce quorum sensing signaling molecules, which enable them to act as a complex multicellular entity.”
BackgroundSelf-citationGlobal impact of mature biofilm lifestyle on Escherichia coli K‐12 gene expression
Beloin, C., Valle, J., Latour‐Lambert, P., Fauré, P., Kzreminski, M., Balestrino, D., Haagensen, J. A. J., Molin, S., Prensier, G., Arbeille, B., et al. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03865.x · Cited by 478
“Accordingly, Pseudomonas putida and P. aeruginosa biofilm proteome analyses showed that a large number of genes are differentially regulated during biofilm development (Sauer and Camper, 2001; Sauer et al., 2002).”
BackgroundChelator-Induced Dispersal and Killing of Pseudomonas aeruginosa Cells in a Biofilm
Banin, E., Brady, K. M., & Greenberg, E. P. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.72.3.2064-2069.2006 · Cited by 473
“aeruginosa biofilms exposed to various conditions (6, 34, 41).”
Backgroundde la Fuente‐Núñez, C., Korolik, V., Bains, M., Nguyen, U., Breidenstein, E. B. M., Horsman, S. R., Lewenza, S., Burrows, L. L., & Hancock, R. E. W. (2012) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00064-12 · Cited by 465
“As expected, flagellar genes were downregulated, as were genes ( nirS , norC , and nosZ ) known to play a role in anaerobic biofilm developmental process by encoding proteins involved in anaerobic respiration (53, 64).”
InfluentialRhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms
Boles, B. R., Thoendel, M., & Singh, P. K. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04743.x · Cited by 446
“These findings are consistent with recent work showing that the protein expression profiles of detached P. aeruginosa more closely resembled planktonic bacteria than biofilm cells (Sauer et al., 2002).”
BackgroundResultInfluentialQuorum sensing in Pseudomonas aeruginosa biofilms
de Kievit, T. R. (2008) · Environmental Microbiology · doi:10.1111/j.1462-2920.2008.01792.x · Cited by 461
“Indeed, comparative transcriptome and proteome analyses of P. aeruginosa biofilm and planktonic cells (Whiteley et al., 2001; Sauer et al., 2002; Hentzer et al., 2004) failed to reveal a specific programme of biofilm development.”
BackgroundDispersion as an Important Step in the Candida albicans Biofilm Developmental Cycle
Uppuluri, P., Chaturvedi, A. K., Srinivasan, A., Banerjee, M., Ramasubramaniam, A. K., Köhler, J. R., Kadosh, D., & Lopez-Ribot, J. L. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000828 · Cited by 432
“Several reports have elucidated some of the molecular mechanisms orchestrating dispersion in bacterial biofilms [28–31].”
BackgroundPathogenesis of the Pseudomonas aeruginosa Biofilm: A Review
Tuon, F. F., Dantas, L. R., Suss, P. H., & Ribeiro, V. S. T. (2022) · Pathogens · doi:10.3390/pathogens11030300 · Cited by 430
Dental plaque biofilms: communities, conflict and control
Marsh, P. D., Moter, A., & DeVine, D. (2010) · Periodontology 2000 · doi:10.1111/j.1600-0757.2009.00339.x · Cited by 432
Biofilm maturity studies indicate sharp debridement opens a time-dependent therapeutic window
Wolcott, R. D., Rumbaugh, K. P., James, G. A., Schultz, G. S., Phillips, P. L., Yang, Q., Watters, C., Stewart, P. S., & Dowd, S. E. (2010) · Journal of Wound Care · doi:10.12968/jowc.2010.19.8.77709 · Cited by 424
Biofilm formation in plant–microbe associations
Ramey-Hartung, B., Koutsoudis, M. D., von Bodman, S. B., & Fuqua, C. (2004) · Current Opinion in Microbiology · doi:10.1016/j.mib.2004.10.014 · Cited by 422
“Cells within biofilms are physiologically distinct from the same cells grown in dispersed culture [4,5].”
BackgroundJackson, K. D., Starkey, M., Kremer, S., Parsek, M. R., & Wozniak, D. J. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.14.4466-4475.2004 · Cited by 422
Biofilm Theory Can Guide the Treatment of Device-Related Orthopaedic Infections
Costerton, J. W. (2005) · Clinical Orthopaedics and Related Research · doi:10.1097/00003086-200508000-00003 · Cited by 420
“The humoral system reacts to the presence of immunogenic epitopes on the surfaces of bacteria by producing specific antibodies, and biofilm bacteria produce surface proteins that are very distinct from those on the surfaces of planktonic cells of the same species.(18) Selan et al(19) have identified a surface epitope…”
BackgroundSelf-citationBiofilms and chronic wound inflammation
Wolcott, R. D., Rhoads, D. D., & Dowd, S. E. (2008) · Journal of Wound Care · doi:10.12968/jowc.2008.17.8.30796 · Cited by 418
The Role of Bacterial Biofilm in Antibiotic Resistance and Food Contamination
Abebe, G. M. (2020) · International Journal of Microbiology · doi:10.1155/2020/1705814 · Cited by 444
“During this step, a number of physiological and structural changes have occurred, such as nonmotility of the attached cells [58].”
BackgroundStructure and Regulation of the Type VI Secretion System
Silverman, J. M., Brunet, Y. R., Cascalès, E., & Mougous, J. D. (2010) · Annual Review of Microbiology · doi:10.1146/annurev-micro-121809-151619 · Cited by 403
Osteomyelitis and the role of biofilms in chronic infection
Brady, R. A., Leid, J. G., Calhoun, J. H., Costerton, J. W., & Shirtliff, M. E. (2008) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2007.00357.x · Cited by 403
“In addition, detachment and seeding of virgin surfaces may be accomplished by the migration of single, motile cells from the cores of attached microcolonies (Sauer et al., 2002).”
BackgroundSelf-citationLuyan, Z., Jackson, K. D., Landry, R. M., Parsek, M. R., & Wozniak, D. J. (2006) · Journal of Bacteriology · doi:10.1128/jb.01202-06 · Cited by 400
“aeruginosa undergoes distinct stages of biofilm development, including attachment, maturation, and dispersion (30, 34, 39).”
BackgroundMicroscopic and physiologic evidence for biofilm-associated wound colonization in vivo
Davis, S. C., Ricotti, C., Cazzaniga, A., Welsh, E., Eaglstein, W. H., & Mertz, P. M. (2008) · Wound Repair and Regeneration · doi:10.1111/j.1524-475x.2007.00303.x · Cited by 393
Ramsey, D. M., & Wozniak, D. J. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04552.x · Cited by 392
“After attachment, P. aeruginosa develops microcolonies on both biotic and abiotic surfaces (O’Toole et al., 2000; Sauer et al., 2002; Jackson et al., 2003) (Fig.”
BackgroundMethodInfluentialMini-review: quorum sensing in the marine environment and its relationship to biofouling
Dobretsov, S., Teplitski, M., & Paul, V. J. (2009) · Biofouling · doi:10.1080/08927010902853516 · Cited by 390
“QS helps to control the switch from the behaviors typical of single-cell organisms to those appropriate to cells within a colony or a biofilm (Sauer et al. 2002).”
Biofilm formation by clinical isolates and the implications in chronic infections
Sánchez, C. J., Mende, K., Beckius, M. L., Akers, K. S., Romano, D. R., Wenke, J. C., & Murray, C. K. (2013) · BMC Infectious Diseases · doi:10.1186/1471-2334-13-47 · Cited by 390
“Adaptation to surface attached growth within a biofilm is accompanied by significant changes in gene and protein expression, as well as metabolic activity [7,8] which confers resistance to antimicrobial therapy [9,10] and host mechanisms of clearance [11,12].”
BackgroundInhibition of biofouling by marine microorganisms and their metabolites
Dobretsov, S., Dahms, H.-U., & Qian, P. (2006) · Biofouling · doi:10.1080/08927010500504784 · Cited by 390
“It had been proven that Gram-negative bacteria in biofilms produce cell-to-cell communication signals (quorum sensing signals) that accumulate to threshold concentrations and activate target genes, as well as having effects on bacterial biofilm formation (Davies et al. 1998; Parsek & Greenberg, 2000; Sauer et al. 2002…”
BackgroundInvolvement of a Novel Efflux System in Biofilm-Specific Resistance to Antibiotics
Zhang, L., & Mah, T. (2008) · Journal of Bacteriology · doi:10.1128/jb.01655-07 · Cited by 387
“None of these genes have been identified as biofilm-specific genes in genomic and proteomic studies (37, 38, 41), likely due to differences between P.”
BackgroundQuorum sensing: the power of cooperation in the world of Pseudomonas
Juhas, M., Eberl, L., & Tümmler, B. (2005) · Environmental Microbiology · doi:10.1111/j.1462-2920.2005.00769.x · Cited by 385
Sticky Situations: Key Components That Control Bacterial Surface Attachment
Petrova, O. E., & Sauer, K. (2012) · Journal of Bacteriology · doi:10.1128/jb.00003-12 · Cited by 373
“Spinning is an indication of flagellar attachment to the substrate (140, 155), with the bacterium rotating around its axis.”
BackgroundInfluentialSelf-citationDrescher, K., Shen, Y., Bassler, B. L., & Stone, H. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300321110 · Cited by 378
“In standard assays with glucose-based medium, flagellar-mediated swimming motility leads to increased residence times of cells near surfaces (36), and flagella also enhance attachment to surfaces (21, 22, 37).”
BackgroundAn update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal
Harmsen, M., Yang, L., Pamp, S. J., & Tolker‐Nielsen, T. (2010) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2010.00690.x · Cited by 393
Schwarz, S., West, T. E., Boyer, F., Chiang, W., Carl, M. A., Hood, R. D., Rohmer, L., Tolker‐Nielsen, T., Skerrett, S. J., & Mougous, J. D. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001068 · Cited by 375
“such as exopolysaccharides [14,37,38,39,40].”
Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm
Lee, K. W. K., Periasamy, S., Mukherjee, M., Xie, C., Kjelleberg, S. J., & Rice, S. A. (2013) · The ISME Journal · doi:10.1038/ismej.2013.194 · Cited by 374
“About 1–2% of the entire genome (79 genes in Escherichia coli and 73 genes in Pseudomonas aeruginosa) and more than 800 proteins were differentially expressed when biofilms and planktonic bacteria were compared (Whiteley et al., 2001; Sauer et al., 2002; Schembri et al., 2003).”
BackgroundBiofilm Matrix and Its Regulation in Pseudomonas aeruginosa
Wei, Q., & Luyan, Z. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms141020983 · Cited by 397
“aeruginosa biofilm development [111], and might be important for the survival of bacterial cells growing in anaerobic conditions in biofilms [112,113].”
BackgroundHuman polymicrobial infections
BROGDEN, K., Guthmiller, J. M., & TAYLOR, C. (2005) · The Lancet · doi:10.1016/s0140-6736(05)70155-0 · Cited by 369
Biofilms: A role in recurrent mastitis infections?
Melchior, M. B., Vaarkamp, H., & Fink‐Gremmels, J. (2005) · The Veterinary Journal · doi:10.1016/j.tvjl.2005.01.006 · Cited by 369
Jesaitis, A. J., Franklin, M. J., Berglund, D. L., Sasaki, M., Lord, C. I., Bleazard, J. B., Duffy, J. E., Beyenal, H., & Lewandowski, Z. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.8.4329 · Cited by 373
A global view of antibiotic resistance
Martínez, J. L., Fajardo-Lubian, A., Garmendia, L., Hernandez, A., Linares, J. F., Martínez‐Solano, L., & Sánchez, M. B. (2008) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2008.00142.x · Cited by 362
Biofilm Forming Lactobacillus: New Challenges for the Development of Probiotics
Salas-Jara, M., Ilabaca, A., Vega, M. A., & García, A. (2016) · Microorganisms · doi:10.3390/microorganisms4030035 · Cited by 353
“Detachment seems to be an active process allowing the colonization of new niches [44].”
BackgroundDevelopment and maturation of Escherichia coli K‐12 biofilms
Reisner, A., Haagensen, J. A. J., Schembri, M. A., Zechner, E. L., & Molin, S. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03490.x · Cited by 352
“AI-2 mediated cell-to-cell signalling is not involved in formation of mature biofilms The observed differentiation process during biofilm development of E. coli strains carrying a derepressed IncF plasmid is very similar to that previously described for Pseudomonas aeruginosa PAO1 (Sauer et al., 2002).”
BackgroundResultInfluentialEffects of iron on DNA release and biofilm development by Pseudomonas aeruginosa
Yang, L., Barken, K. B., Skindersoe, M. E., Christensen, A. B., Givskov, M., & Tolker‐Nielsen, T. (2007) · Microbiology · doi:10.1099/mic.0.2006/004911-0 · Cited by 359
“Biofilm formation is described as a developmental sequence that varies to some extent between bacterial species but often results in the formation of mature microbial communities with tower- or mushroom-shaped microcolonies (Davey & O’Toole, 2000; Sauer et al., 2002; Klausen et al., 2003a).”
Microbial landscapes: new paths to biofilm research
Battin, T. J., Sloan, W. T., Kjelleberg, S. J., Daims, H., Head, I. M., Curtis, T. P., & Eberl, L. (2006) · Nature Reviews Microbiology · doi:10.1038/nrmicro1556 · Cited by 336
Mucosal Biofilm Formation on Middle-Ear Mucosa in the Chinchilla Model of Otitis Media
Ehrlich, G. D. (2002) · JAMA · doi:10.1001/jama.287.13.1710 · Cited by 333
Self-citationCaneschi, A., Bardhi, A., Barbarossa, A., & Zaghini, A. (2023) · Antibiotics · doi:10.3390/antibiotics12030487 · Cited by 331
“(1) The exposures needed to suppress the emergence of resistance for Gram-negative bacteria varied depending on: the antibiotic assayed; the extent of the experiment; the bacterial species and the specific bacterial isolate tested (genomic differences between laboratory reference strains and the corresponding clinical…”
BackgroundExploitation of marine algae: biogenic compounds for potential antifouling applications
Bhadury, P., & Wright, P. (2004) · Planta · doi:10.1007/s00425-004-1307-5 · Cited by 327
“Sauer et al. (2002), using twodimensional gel electrophoresis and reporter-gene analysis, have shown that P. aeruginosa displays five distinct physiologies during biofilm development.”
MethodAbdallah, M., Benoliel, C., Drider, D., Dhulster, P., & Chihib, N. (2014) · Archives of Microbiology · doi:10.1007/s00203-014-0983-1 · Cited by 329
“Sauer et al. (2002) found that the transition of P. aeruginosa cells from planktonic to sessile state varied the expression of more than 800 proteins.”
BackgroundEmerging rules for effective antimicrobial coatings
Salwiczek, M., Qu, Y., Gardiner, J., Strugnell, R. A., Lithgow, T. J., McLean, K. M., & Thissen, H. W. (2013) · Trends in biotechnology · doi:10.1016/j.tibtech.2013.09.008 · Cited by 312
Hypothesis for the Role of Nutrient Starvation in Biofilm Detachment
Hunt, S. M., Werner, E., Huang, B., Hamilton, M. A., & Stewart, P. S. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.12.7418-7425.2004 · Cited by 312
“We focused on these triggers in particular because they have the potential to explain the observation of biofilm cell cluster hollowing (13, 15, 17, 21 , 24, 28).”
Backgroundde Aldecoa, A. L. I., Zafra, O., & González‐Pastor, J. E. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01390 · Cited by 330
“In this sense, although several mechanisms were described for the eDNA release in planktonic cultures, some of them were not found or were different in biofilms (Sauer et al., 2002; Greiner et al., 2005; Allesen-Holm et al., 2006; Kim and Lee, 2016).”
BackgroundBacterial biofilms: prokaryotic adventures in multicellularity
Webb, J. S., Givskov, M., & Kjelleberg, S. J. (2003) · Current Opinion in Microbiology · doi:10.1016/j.mib.2003.10.014 · Cited by 309
Mimicking biofilm formation and development: Recent progress in in vitro and in vivo biofilm models
Guzmán‐Soto, I., McTiernan, C. D., Gonzalez-Gomez, M., Ross, A., Gupta, K., Suuronen, E. J., Mah, T., Griffith, M., & Alarcon, E. I. (2021) · iScience · doi:10.1016/j.isci.2021.102443 · Cited by 332
“Furthermore, biofilm-forming bacteria experience changes in phenotype during biofilm development (Sauer et al., 2002; Southey-Pillig et al., 2005).”
BackgroundImplantable Device-Related Infection
VanEpps, J. S., & Younger, J. G. (2016) · Shock · doi:10.1097/shk.0000000000000692 · Cited by 306
“’’ The transition represents a phenotypic switch that involves significant changes in both gene and protein expression (75, 76).”
Background
Metadata
- Authors
- Sauer, K., Camper, A. K., Ehrlich, G. D., Costerton, J. W., & Davies, D. G.
- Affiliations
- Montana State University (US)
- Allegheny-Singer Research Institute (US)
- Binghamton University (US)
- Venue
- Journal of Bacteriology
- Publisher
- American Society for Microbiology
- Published
- 2002-02-15
- Volume
- 184
- Issue
- 4
- Pages
- 1140-1154
- ISSN
- 0021-9193 (ISSN-L)
- 1098-5530
- PMC
- PMC134825
- OpenAlex
- W2122608498
- Cited by
- 1,691
- References
- 55
- Citations by year
- 2026: 32 · 2025: 52 · 2024: 47 · 2023: 71 · 2022: 56 · 2021: 60 · 2020: 74 · 2019: 77 · 2018: 66 · 2017: 79 · 2016: 85 · 2015: 91 · 2014: 112 · 2013: 93 · 2012: 70
- FWCI
- 20.74
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Bacteriology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Montana State University ScholarWorks (Montana State University) (submittedVersion)
- Funders
- National Science Foundation
- Montana State University
- Deutsche Forschungsgemeinschaft
- National Institutes of Health
- Binghamton University
- National Institute on Deafness and Other Communication Disorders (R01DC002148, R01DC004173, DC04173-01, DC-02148)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
- Keywords
- Pseudomonas aeruginosa, biofilm growth, biofilm maturation, biofilm dispersal, motility regulation, alginate production, quorum sensing, proteome, stage-specific gene expression, planktonic versus biofilm cells, biofilm physiology
- MeSH terms
- Amino Acids, Bacterial Proteins, Phenotype, Pseudomonas aeruginosa, Electrophoresis, Gel, Two-Dimensional, Oxidative Stress, Biofilms, Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization, Proteome
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