The DOI matches its Crossref record; 54 of the 55 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
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.
Cited by
Sorted by citations
Items 201–300 of 1,000
Armijo, L. M., Wawrzyniec, S. J., Kopciuch, M., Brandt, Y. I., Rivera, A. C., Withers, N. J., Cook, N. C., Huber, D. L., Monson, T., Smyth, H. D. C., et al. (2020) · Journal of Nanobiotechnology · doi:10.1186/s12951-020-0588-6 · Cited by 190
“Previous studies on P. aeruginosa biofilms reported using a growth period of 6 days [172, 173] .”
ResultControlling infection by tuning in and turning down the volume of bacterial small-talk
Cámara, M., Williams, P. M., & Hardman, A. (2002) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(02)00447-4 · Cited by 180
A Complex Transcription Network Controls the Early Stages of Biofilm Development byEscherichia coli
Prüß, B. M., Besemann, C. A., Denton, A. M., & Wolfe, A. J. (2006) · Journal of Bacteriology · doi:10.1128/jb.01780-05 · Cited by 178
Furanones as potential anti-bacterial coatings on biomaterials
Baveja, J. K., Willcox, M. D. P., Hume, E. B. H., Kumar, N., Odell, R. A., & Poole-Warren, L. A. (2004) · Biomaterials · doi:10.1016/j.biomaterials.2004.02.051 · Cited by 177
Microbial biofilm formation: a need to act
Römling, U., Kjelleberg, S. J., Normark, S. J., Nyman, L., Uhlin, B. E., & Åkerlund, B. (2014) · Journal of Internal Medicine · doi:10.1111/joim.12242 · Cited by 185
Quorum sensing: implications on Rhamnolipid biosurfactant production
Dusane, D. H., Zinjarde, S., Venugopalan, V. P., McLean, R. J. C., Weber, M. M., & Rahman, P. K. S. M. (2010) · Biotechnology and Genetic Engineering Reviews · doi:10.1080/02648725.2010.10648149 · Cited by 177
“During the process of biofilm development and maturation, surface-attached cells will aggregate into microcolonies that are surrounded by regions of few cells referred to as water channels (Davey and O’Toole, 2000, Sauer et al., 2002).”
BackgroundThe role of biofilms in otolaryngologic infections
Post, J. C., Stoodley, P., Hall‐Stoodley, L., & Ehrlich, G. D. (2004) · Current Opinion in Otolaryngology & Head & Neck Surgery · doi:10.1097/01.moo.0000124936.46948.6a · Cited by 176
Self-citationSiqueira, J. F., Jr., & Rôças, I. N. (2009) · Oral Surgery Oral Medicine Oral Pathology Oral Radiology and Endodontology · doi:10.1016/j.tripleo.2009.01.044 · Cited by 176
Al‐Shabib, N. A., Husain, F. M., Ahmed, F., Khan, R. A., Ahmad, I., Alsharaeh, E. H., Khan, M. S., Hussain, A., Rehman, M. T., Yusuf, M., et al. (2016) · Scientific Reports · doi:10.1038/srep36761 · Cited by 176
Rogan, M. P., Taggart, C. C., Greene, C. M., Murphy, P. G., O’Neill, S. J., & McElvaney, N. G. (2004) · The Journal of Infectious Diseases · doi:10.1086/423821 · Cited by 171
“ganisms [7].”
Localized Gene Expression in Pseudomonas aeruginosa Biofilms
Lenz, A. P., Williamson, K. S., Pitts, B., Stewart, P. S., & Franklin, M. J. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.00710-08 · Cited by 174
“aeruginosa growing in biofilms and cells growing in planktonic cultures (44, 50, 58, 59, 62).”
BackgroundResultBiofilms in wounds: management strategies
Rhoads, D. D., Wolcott, R. D., & Percival, S. L. (2008) · Journal of Wound Care · doi:10.12968/jowc.2008.17.11.31479 · Cited by 175
Characterization of Colony Morphology Variants Isolated fromStreptococcus pneumoniaeBiofilms
Allegrucci, M., & Sauer, K. (2006) · Journal of Bacteriology · doi:10.1128/jb.01369-06 · Cited by 174
Self-citationLi, X., Gu, N., Huang, T. Y., Zhong, F., & Peng, G. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.1114199 · Cited by 174
“aeruginosa progresses begins with attachment to the surfaces suitable for growth including medical instruments and food, followed by the formation of microcolonies, and finally, maturation involving the expression of matrix polymers (Sauer et al., 2002).”
BackgroundMultiple Roles of Extracellular Polymeric Substances on Resistance of Biofilm and Detached Clusters
Xue, Z., Sendamangalam, V., Gruden, C. L., & Seo, Y. (2012) · Environmental Science & Technology · doi:10.1021/es3031165 · Cited by 172
Toxin-antitoxins and bacterial virulence
Lobato‐Márquez, D., Díaz‐Orejas, R., & del Portillo, F. G. (2016) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuw022 · Cited by 172
“…physiological status of sessile bacteria within the biofilm matrix, which represents a diffusion barrier against damaging molecules (Joo and Otto 2012), and the different protein and gene expression profiles of sessile cells compared to planktonic cells (Jackson et al. 2002; Sauer et al. 2002).”
BackgroundRénier, S., Hébraud, M., & Desvaux, M. (2010) · Environmental Microbiology · doi:10.1111/j.1462-2920.2010.02378.x · Cited by 171
Mazaheri, T., Cervantes-Huamán, B. R. H., Bermúdez-Capdevila, M., Ripolles‐Avila, C., & Jerez, J. J. R. (2021) · Microorganisms · doi:10.3390/microorganisms9010181 · Cited by 170
“Lastly, the fifth stage is related to dispersion, where sessile cells can return to their planktonic forms and transfer to the environment, once again able to colonize new surfaces [53].”
BackgroundCalcium Increases Xylella fastidiosa Surface Attachment, Biofilm Formation, and Twitching Motility
Cruz, L. F., Cobine, P. A., & Fuente, L. D. L. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.06501-11 · Cited by 167
“In advanced stages, cells increase the production of EPS to create a matrix that holds together the mature biofilm (25, 47, 48).”
BackgroundEnvironmental Influences on Biofilm Development
Goller, C., & Romeo, T. (2008) · Current topics in microbiology and immunology · doi:10.1007/978-3-540-75418-3_3 · Cited by 178
The Role of Biofilms: Are We Hitting the Right Target?
Wolcott, R. D., & Dowd, S. E. (2011) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0b013e3181fca244 · Cited by 167
Li, Y., Heine, S., Entian, M., Sauer, K., & Frankenberg‐Dinkel, N. (2013) · Journal of Bacteriology · doi:10.1128/jb.01156-12 · Cited by 165
“To visualize the biofilm architecture and the dispersion response, biofilms were grown for 6 days in flow cells, and confocal images were acquired as previously described (2, 3).”
BackgroundMethodSelf-citation(2003) · Springer eBooks · doi:10.1007/978-94-017-0193-8 · Cited by 165
agr System of Listeria monocytogenes EGD-e: Role in Adherence and Differential Expression Pattern
Rieu, A., Weidmann, S., Garmyn, D., Piveteau, P., & Guzzo, J. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00608-07 · Cited by 164
“Rhl regulon plays a role in maturation of the biofilm (14, 46).”
BackgroundKostenko, V., Lyczak, J. B., Turner, K., & Martinuzzi, R. J. (2010) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00825-10 · Cited by 159
“Biofilms are generally characterized as mono- or multispecies communities of microbial cells attached to surfaces and/or each other and embedded in self-produced extracellular polymeric substances (EPS) (36).”
BackgroundMartínez‐Gil, M., Yousef‐Coronado, F., & Espinosa‐Urgel, M. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07249.x · Cited by 158
“aeruginosa at the different stages have been reported (Sauer and Camper, 2001; Sauer et al., 2002).”
BackgroundWu, H., Chung, P.-C., Shih, H., Wen, S., & Lai, E. (2008) · Journal of Bacteriology · doi:10.1128/jb.01775-07 · Cited by 157
“aeruginosa (37), and it has been suggested that this protein plays a role in biofilm development (12).”
BackgroundBiofilms in Infections of the Eye
Bispo, P. J. M., Haas, W., & Gilmore, M. S. (2015) · Pathogens · doi:10.3390/pathogens4010111 · Cited by 158
“, a cell in the middle of a group will experience more excreted products and fewer factors from the environment than a cell on the periphery of a population), and as a result, cells begin to differentiate [23].”
BackgroundAschtgen, M., Gavioli, M., Dessen, A., Lloubès, R., & Cascalès, E. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.07028.x · Cited by 156
“…in Vibrio parahaemolyticus and enteroaggregative Escherichia coli (EAEC, Enos-berlage et al., 2005; Aschtgen et al., 2008), and the Pseudomonas aeruginosa HSI-2 and HSI-3 T6SS gene clusters have been shown to be upregulated during biofilm formation (Sauer et al., 2002: Southey-pillig et al. 2005).”
BackgroundNouwens, A. S., Beatson, S. A., Whitchurch, C. B., Walsh, B. J., Schweizer, H. P., Mattick, J. S., & Cordwell, S. J. (2003) · Microbiology · doi:10.1099/mic.0.25967-0 · Cited by 156
“Both approaches have recently been used to monitor the molecular basis of biofilm development in P. aeruginosa (Whiteley et al., 2001; Sauer et al., 2002 ).”
MethodInsight into the microbial multicellular lifestyle via flow‐cell technology and confocal microscopy
Pamp, S. J., Sternberg, C., & Tolker‐Nielsen, T. (2008) · Cytometry Part A · doi:10.1002/cyto.a.20685 · Cited by 164
“aeruginosa attached longitudinally (72), indicating that flagella are not required for attachment per se but may enhance the process.”
BackgroundSpatiometabolic Stratification of Shewanella oneidensis Biofilms
Teal, T. K., Lies, D. P., Wold, B. J., & Newman, D. K. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.01163-06 · Cited by 155
“Although S. oneidensis forms single-layer biofilms under some conditions (41), in our flow cell system biofilms developed as mushroomshaped structures very similar to those described for other bacteria, including Pseudomonas aeruginosa, Pseudomonas fluorescens, and E. coli ( 37 ).”
BackgroundBiofilms and their relevance to veterinary medicine
Clutterbuck, A. L., Woods, E. J., Knottenbelt, D. C., Clegg, P., Cochrane, C. A., & Percival, S. L. (2007) · Veterinary Microbiology · doi:10.1016/j.vetmic.2006.12.029 · Cited by 157
A review of microbial biofilms of produce: Future challenge to food safety
Jahid, I. K., & Ha, S. (2012) · Food Science and Biotechnology · doi:10.1007/s10068-012-0041-1 · Cited by 154
“The heterogeneity of cells in biofilms are optimized to withstand treatment with disinfectants as most of these agents function at the growing stages of the cells (152-154).”
BackgroundSulfur Metabolism in the Extreme Acidophile Acidithiobacillus Caldus
eMangold, S., eValdés, J., Holmes, D. S., & Dopson, M. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2011.00017 · Cited by 154
Donlan, R. M. (2011) · Clinical Infectious Diseases · doi:10.1093/cid/cir077 · Cited by 151
Molecular mechanisms of bacterial quorum sensing as a new drug target
Suga, H., & Smith, K. (2003) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2003.08.001 · Cited by 150
Pantanella, F., Valenti, P., Natalizi, T., Passeri, D., & Berlutti, F. (2013) · PubMed · doi:10.7416/ai.2013.1904 · Cited by 147
Contribution of Stress Responses to Antibiotic Tolerance in Pseudomonas aeruginosa Biofilms
Stewart, P. S., Franklin, M. J., Williamson, K. S., Folsom, J. P., Boegli, L., & James, G. A. (2015) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00433-15 · Cited by 146
Functional organisation of Escherichia coli transcriptional regulatory network
Martínez‐Antonio, A., Janga, S. C., & Thieffry, D. (2008) · Journal of Molecular Biology · doi:10.1016/j.jmb.2008.05.054 · Cited by 146
Biofilm dispersion in Pseudomonas aeruginosa
Kim, S.-K., & Lee, J. (2016) · The Journal of Microbiology · doi:10.1007/s12275-016-5528-7 · Cited by 159
“…dispersal was originally identified in the final stage of biofilm development in Pseudomonas spp., in which bacterial cells within biofilm actively swim away from the interior of the biofilm leaving central hollows (Tolker-Nielsen et al., 2000; Sauer et al., 2002; Purevdorj-Gage et al., 2005).”
BackgroundInfluentialLiao, J., Schurr, M. J., & Sauer, K. (2013) · Journal of Bacteriology · doi:10.1128/jb.00318-13 · Cited by 145
Self-citationMarques, C. N. H., Morozov, A., Planzos, P., & Zelaya, H. M. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.01576-14 · Cited by 143
“ogies), as described previously (22, 31), in 5% LB for a period of 6 days and Awakening of Persister Cells”
MethodLee, W., Ahn, C. H., Hong, S., Kim, S., Lee, S., Baek, Y., & Yoon, J. (2010) · Journal of Membrane Science · doi:10.1016/j.memsci.2010.01.035 · Cited by 143
Influence of growth history on sloughing and erosion from biofilms
Telgmann, U., Horn, H., & Morgenroth, E. (2004) · Water Research · doi:10.1016/j.watres.2004.05.020 · Cited by 144
Listeria monocytogenes EGD-e Biofilms: No Mushrooms but a Network of Knitted Chains
Rieu, A., Briandet, R., Habimana, O., Garmyn, D., Guzzo, J., & Piveteau, P. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.00255-08 · Cited by 144
“In P. aeruginosa, las and rhl, two systems of cell-to-cell signaling, control biofilm formation; the las system is involved in early biofilm development, whereas the rhl system is implicated in the maturation of the biofilm (15, 50 ).”
BackgroundExploring early steps in biofilm formation: set-up of an experimental system for molecular studies
Crouzet, M., Sénéchal, C. L., Brözel, V. S., Costaglioli, P., Barthe, C., Bonneu, M., Garbay, B., & Vilain, S. (2014) · BMC Microbiology · doi:10.1186/s12866-014-0253-z · Cited by 142
“Biofilm physiology is dynamic [24] so analysis may be complicated by the action of several variables: nature of the substratum [25,26], the strain used and its degree of domestication [27], the”
BackgroundPhenotypic Characterization ofStreptococcus pneumoniaeBiofilm Development
Allegrucci, M., Hu, F. Z., Shen, K., Hayes, J., Ehrlich, G. D., Post, J. C., & Sauer, K. (2006) · Journal of Bacteriology · doi:10.1128/jb.188.7.2325-2335.2006 · Cited by 146
Self-citationCell-to-Cell Communication in Bacteria
Tucker, K. D., & Passador, L. (2005) · CRC Press eBooks · doi:10.1201/9781420028232.ch11 · Cited by 140
Heras, K. L., García-Orue, I., Rancan, F., Igartúa, M., Santos‐Vizcaíno, E., & Hernández, R. M. (2024) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2024.115342 · Cited by 143
Klausen, M., Gjermansen, M., Kreft, J., & Tolker‐Nielsen, T. (2006) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2006.00280.x · Cited by 147
Schreiber, K., Boes, N., Eschbach, M., Jaensch, L., Wehland, J., Bjarnsholt, T., Givskov, M., Hentzer, M., & Schobert, M. (2005) · Journal of Bacteriology · doi:10.1128/jb.188.2.659-668.2006 · Cited by 139
“aeruginosa biofilms indicate that a large portion of a mature biofilm population is under oxygen limitation (38).”
BackgroundPhysiology of Pseudomonas aeruginosa in biofilms as revealed by transcriptome analysis
Folsom, J. P., Richards, L., Pitts, B., Roe, F., Ehrlich, G. D., Parker, A. E., Mazurie, A., & Stewart, P. S. (2010) · BMC Microbiology · doi:10.1186/1471-2180-10-294 · Cited by 139
“aeruginosa by many investigators [47-50], so our finding that this communication system is silent in three-day old drip-flow biofilms seems at odds with the literature.”
ResultSelf-citationQuorum Sensing: A Primer for Food Microbiologists
Smith, J. L., Fratamico, P. M., & Novak, J. S. (2004) · Journal of Food Protection · doi:10.4315/0362-028x-67.5.1053 · Cited by 139
Biofilm Development and Cell Death in the Marine Bacterium Pseudoalteromonas tunicata
Mai‐Prochnow, A., Evans, F. F., Dalisay, D. S., Stelzer‐Braid, S., Egan, S., James, S., Webb, J. S., & Kjelleberg, S. J. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.6.3232-3238.2004 · Cited by 139
“Dispersal of bacteria from the interior regions of microcolonies has been observed, apparently resulting in the formation of transparent voids inside the microcolonies (29, 45, 51).”
BackgroundBiofilm enhanced geologic sequestration of supercritical CO2
Mitchell, A. C., Phillips, A. J., Hiebert, R., Gerlach, R., Spangler, L. H., & Cunningham, A. B. (2008) · International journal of greenhouse gas control · doi:10.1016/j.ijggc.2008.05.002 · Cited by 137
“Previous studies have shown significant attachment of microorganisms such as P. aeruginosa to glass in a matter of 10’s of minutes to hours (Sauer et al., 2002).”
BackgroundSkariyachan, S., Sridhar, V. S., Packirisamy, S., Kumargowda, S. T., & Challapilli, S. B. (2018) · Folia Microbiologica · doi:10.1007/s12223-018-0585-4 · Cited by 137
Bacterial biofilms predominate in both acute and chronic human lung infections
Kolpen, M., Kragh, K. N., Barraza, J. P., Faurholt‐Jepsen, D., Lindegaard, B., Egelund, G. B., Jensen, A. V., Ravn, P., Mathiesen, I. H. M., Gheorge, A. G., et al. (2022) · Thorax · doi:10.1136/thoraxjnl-2021-217576 · Cited by 137
Kuboniwa, M., Tribble, G. D., James, C. E., Kılıç, A. O., Tao, L., Herzberg, M. C., Shizukuishi, S., & Lamont, R. J. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05099.x · Cited by 137
Analytical Challenges of Microbial Biofilms on Medical Devices
Vértes, Á., Hitchins, V. M., & Phillips, K. S. (2012) · Analytical Chemistry · doi:10.1021/ac2029997 · Cited by 137
Crenarchaeal Biofilm Formation under Extreme Conditions
Koerdt, A., Gödeke, J., Berger, J., Thormann, K. M., & Albers, S. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014104 · Cited by 137
“The maturation of bacterial biofilms proceeds via defined steps including initial attachment and further development into microcolonies secreting extrapolymeric substances [32].”
BackgroundNitric oxide-releasing chitosan oligosaccharides as antibacterial agents
Lu, Y., Slomberg, D. L., & Schoenfisch, M. H. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2013.11.015 · Cited by 149
“Biofilms are communities of microorganisms adhered to a surface and surrounded by a self-produced extracellular polysaccharide (EPS) matrix that impedes immune response [6,7].”
BackgroundThe Social Life of Aeromonas through Biofilm and Quorum Sensing Systems
Talagrand-Reboul, É., Jumas‐Bilak, E., & Lamy, B. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00037 · Cited by 136
Høiby, N. (2002) · Journal of Cystic Fibrosis · doi:10.1016/s1569-1993(02)00104-2 · Cited by 136
Bacteria/Material Interfaces: Role of the Material and Cell Wall Properties
Ploux, L., Ponche, A., & Anselme, K. (2010) · Journal of Adhesion Science and Technology · doi:10.1163/016942410x511079 · Cited by 136
Deng, J., Orner, E. P., Chau, J. F., Anderson, E. M., Kadilak, A. L., Rubinstein, R. L., Bouchillon, G. M., Goodwin, R. A., Gage, D. J., & Shor, L. (2014) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2014.12.006 · Cited by 135
“The micro-scale structure of biofilms includes several layers of bacteria, each with different phenotypes (Ramos et al., 2001; Sauer et al., 2002), and pores and networks facilitating the flow of nutrients and oxygen (Li and Yuan, 2002).”
BackgroundInterrelationships between Colonies, Biofilms, and Planktonic Cells of Pseudomonas aeruginosa
Mikkelsen, H., Duck, Z., Lilley, K. S., & Welch, M. (2007) · Journal of Bacteriology · doi:10.1128/jb.01687-06 · Cited by 135
“Some of the reasons for discrepancies between the studies appear to be related to the method of analysis (transcriptomic [12, 35, 36] versus proteomic [25, 34] studies).”
Interdependence between iron acquisition and biofilm formation in Pseudomonas aeruginosa
Kang, D., & Kirienko, N. V. (2018) · The Journal of Microbiology · doi:10.1007/s12275-018-8114-3 · Cited by 137
“In Pseudomonas aeruginosa, biofilm development follows a stereotypical course (Sauer et al., 2002; Stoodley et al., 2002).”
Bacteria and Antibiotics in Wound Healing
Caldwell, M. D. (2020) · Surgical Clinics of North America · doi:10.1016/j.suc.2020.05.007 · Cited by 136
Koczan, J., Lenneman, B. R., Mcgrath, M., & Sundin, G. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.05138-11 · Cited by 124
“These developmental phases include planktonic (free swimming), attachment (reversible and irreversible), mature biofilm, and detachment (30).”
BackgroundGuttenplan, S. B., Blair, K. M., & Kearns, D. B. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001243 · Cited by 134
Anti-Biofilm Compounds Derived from Marine Sponges
Stowe, S. D., Richards, J. J., Tucker, A. T., Thompson, R. J., Melander, C., & Cavanagh, J. (2011) · Marine Drugs · doi:10.3390/md9102010 · Cited by 135
“The EPS is a complex, highly polar mixture of biomolecular materials that provides the resident bacteria with protection against bactericidal compounds and host immune responses [29].”
BackgroundVibrio cholerae CytR is a repressor of biofilm development
Haugo, A. J., & Watnick, P. I. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.03023.x · Cited by 132
“More comprehensive genomics- and proteomics-based profiling of biofilmassociated cells is under way or completed in many bacterial backgrounds, and these studies are likely to yield a deeper understanding of the physiological state of the biofilm-associated cell (Sauer and Camper, 2001; Schoolnik et al., 2001; Whitele…”
BackgroundQuilès, F., Humbert, F., & Delille, A. (2009) · Spectrochimica Acta Part A Molecular and Biomolecular Spectroscopy · doi:10.1016/j.saa.2009.11.026 · Cited by 131
Al-Wrafy, F. A., Brzozowska, E., Górska, S., & Gamian, A. (2017) · Postępy Higieny i Medycyny Doświadczalnej · doi:10.5604/01.3001.0010.3792 · Cited by 139
New insights on molecular regulation of biofilm formation in plant‐associated bacteria
Castiblanco, L. F., & Sundin, G. W. (2015) · Journal of Integrative Plant Biology · doi:10.1111/jipb.12428 · Cited by 130
“aeruginosa proteome showed a sixfold or more difference in regulation level between planktonic cells and the maturation stage-2, for example, with most of them being upregulated (Sauer et al. 2002).”
BackgroundImmobilized viable microbial cells: from the process to the proteome… or the cart before the horse
Junter, G., & Jouenne, T. (2004) · Biotechnology Advances · doi:10.1016/j.biotechadv.2004.06.003 · Cited by 130
“physiological changes has been highlighted by Sauer et al. (2002), who analysed by twodimensional gel electrophoresis, four development stages of a Pseudomonas aeruginosa biofilm on silicone tubing in a continuous flow reactor: reversible attachment, irreversible attachment, maturation and…”
Lanter, B. B., Sauer, K., & Davies, D. G. (2014) · mBio · doi:10.1128/mbio.01206-14 · Cited by 129
Self-citationTherapeutic Strategies against Biofilm Infections
Mishra, S., Gupta, A., Upadhye, V. J., Singh, S. C., Sinha, R. P., & Häder, D. (2023) · Life · doi:10.3390/life13010172 · Cited by 143
“This opens up many therapeutic intervention opportunities [16,61].”
BackgroundHamilton, S., Bongaerts, R. J., Mulholland, F., Cochrane, B. C., Porter, J., Lucchini, S., Lappin-Scott, H. M., & Hinton, J. C. D. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-599 · Cited by 128
“This system is identical to the glass flow cell system described above apart from replacing the glass flow cell with silicone rubber tubing that permits the harvesting of large amounts of biofilm biomass [32,76,96].”
MethodExtracellular enzymes affect biofilm formation of mucoid Pseudomonas aeruginosa
Tielen, P., Rosenau, F., Wilhelm, S., Jaeger, K., Flemming, H., & Wingender, J. (2010) · Microbiology · doi:10.1099/mic.0.037036-0 · Cited by 129
Growing and Analyzing Biofilms in Flow Cells
Sternberg, C., & Tolker‐Nielsen, T. (2006) · Current Protocols in Microbiology · doi:10.1002/9780471729259.mc01b02s00 · Cited by 128
“To estimate the extent of biofilm development in the silicone tubing, a glass capillary with a square cross-section can be inserted into the tubing during the setup of the system to provide a window for microscopic investigation (Sauer et al., 2002).”
BackgroundHigh-resolution three-dimensional imaging of biofilm development using optical coherence tomography
Xi, C., Marks, D. L., Schlachter, S. C., Luo, W., & Boppart, S. A. (2006) · Journal of Biomedical Optics · doi:10.1117/1.2209962 · Cited by 128
Conrad, J. C. (2012) · Research in Microbiology · doi:10.1016/j.resmic.2012.10.016 · Cited by 125
Secor, P. R., James, G. A., Fleckman, P. H., Olerud, J. E., McInnerney, K., & Stewart, P. S. (2011) · BMC Microbiology · doi:10.1186/1471-2180-11-143 · Cited by 129
“Bacteria within these communities secrete an extracellular polymer matrix, form complex structures, and are phenotypically distinct from their planktonic counterparts [1,2], and are orders of magnitude more resistant to antibiotics and biocides than planktonic bacteria [3].”
BackgroundHassett, D. J., Korfhagen, T. R., Irvin, R. T., Schurr, M. J., Sauer, K., Lau, G. W., Sutton, M. D., Yu, H. D., & Høiby, N. (2010) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728220903454988 · Cited by 126
Self-citationTolker‐Nielsen, T. (2014) · Apmis · doi:10.1111/apm.12335 · Cited by 133
“[156, 157], type IV pili [75, 156, 158], Cup fimbria [159], extracellular DNA [160], and Psl”
BackgroundBacterial resistance to biocides in the healthcare environment: should it be of genuine concern?
Maillard, J. (2007) · Journal of Hospital Infection · doi:10.1016/s0195-6701(07)60018-8 · Cited by 126
Schaudinn, C., Gorur, A., Keller, D. C., Sedghizadeh, P. P., & Costerton, J. W. (2009) · The Journal of the American Dental Association · doi:10.14219/jada.archive.2009.0307 · Cited by 125
Self-citationdPABBs: A Novel in silico Approach for Predicting and Designing Anti-biofilm Peptides
Sharma, A. B., Gupta, P., Kumar, R., & Bhardwaj, A. (2016) · Scientific Reports · doi:10.1038/srep21839 · Cited by 125
Staudinger, B. J., Muller, J. F., Halldórsson, S., Boles, B. R., Angermeyer, A., Nguyen, D. M., Rosen, H., Baldursson, Ó., Gottfreðsson, M., Gudmundsson, G. H., et al. (2014) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201312-2142oc · Cited by 121
“Biofilm-Defective Mutants Form Antibiotic Tolerant Aggregates Whereas motility is required for biofilm formation in several systems (33, 61, 62), our experiments indicate that motility loss enhances aggregate formation.”
BackgroundPetrova, O. E., & Sauer, K. (2010) · Journal of Bacteriology · doi:10.1128/jb.00387-10 · Cited by 124
“amination under long-wave UV excitation (10, 54).”
BackgroundSelf-citationMicrobial Biofilms in Ophthalmology and Infectious Disease
Behlau, I. (2008) · Archives of Ophthalmology · doi:10.1001/archopht.126.11.1572 · Cited by 125
“These proteins were involved in metabolism, phospholipid and lipopolysaccharide biosynthesis, membrane transport and secretion, and adaptation and protective mechanisms.(150)”
BackgroundImprovements on colony morphology identification towards bacterial profiling
Sousa, A. M., Machado, I., Nicolau, A., & Pereira, M. O. (2013) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2013.09.020 · Cited by 143
Biofilm Lithography enables high-resolution cell patterning via optogenetic adhesin expression
Jin, X., & Riedel-Kruse, I. H. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1720676115 · Cited by 124
“Left unstimulated in the dark, these cells readily desorb from the surface (43), but in illuminated regions, membrane-expressed Ag43 reduces the desorption rate of adsorbed cells, effectively anchoring them to the surface (38).”
BackgroundPatrauchan, M. A., Sarkisova, S. A., Sauer, K., & Franklin, M. J. (2005) · Microbiology · doi:10.1099/mic.0.28041-0 · Cited by 124
“During biofilm development, bacteria demonstrate physiological and sometimes morphological changes, which ultimately lead to the formation of a mature biofilm (Dalton et al., 1994; Davies et al., 1993; Sauer et al., 2002; Whiteley et al., 2001).”
BackgroundMethodInfluentialSelf-citationGenetic evidence that the Vibrio cholerae monolayer is a distinct stage in biofilm development
Moorthy, S., & Watnick, P. I. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04000.x · Cited by 124
“…not in the monolayer Induction of exopolysaccharide synthesis gene transcription upon association with a surface is a well-documented phenomenon in bacterial biofilm development (Davies et al., 1993; Prigent-Combaret et al., 1999; Whiteley et al., 2001; Haugo and Watnick, 2002; Sauer et al., 2002).”
BackgroundMolecular determinants of staphylococcal biofilm dispersal and structuring
LE, K. Y., Dastgheyb, S., Ho, T. V., & Otto, M. J. (2014) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2014.00167 · Cited by 125
“…to include a total of five stages, but such further differentiation has not yet been made for staphylococcal biofilm development Frontiers in Cellular and Infection Microbiology www.frontiersin.org November 2014 | Volume 4 | Article 167 | 1 CELLULAR AND INFECTION MICROBIOLOGY (Sauer et al., 2002).”
BackgroundControlled delivery of antimicrobial gallium ions from phosphate-based glasses
Valappil, S. P., Ready, D. R., Neel, E. A. A., Pickup, D. M., O'Dell, L. A., Chrzanowski, W., Pratten, J. R., Newport, R. J., Smith, M. E., Wilson, M., et al. (2008) · Acta Biomaterialia · doi:10.1016/j.actbio.2008.09.019 · Cited by 121
“Biofilm formation occurs as a result of a sequence of events: microbial surface attachment, cell proliferation, matrix production and detachment [5].”
BackgroundRollet, C., Gal, L., & Guzzo, J. (2008) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2008.01415.x · Cited by 123
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
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
