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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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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 701–800 of 1,000
Wu, X., Farraj, D. A. A., Rajaselvam, J., Alkufeidy, R. M., Vijayaraghavan, P., Alkubaisi, N. A. O., Agastian, P., & Alshammari, M. K. (2020) · Saudi Journal of Biological Sciences · doi:10.1016/j.sjbs.2020.07.020 · Cited by 40
“The growth pattern of biofilm influences on maturation, dispersion and attachment (Sauer et al., 2002).”
BackgroundVilain, S., & Brözel, V. S. (2006) · Journal of Proteome Research · doi:10.1021/pr050402b · Cited by 40
Schaber, J. A., Hammond, A. A., Carty, N. L., Williams, S. C., Colmer‐Hamood, J. A., Burrowes, B. H., Dhevan, V., Griswold, J., & Hamood, A. N. (2007) · Journal of Medical Microbiology · doi:10.1099/jmm.0.47031-0 · Cited by 40
“Using microscopy, in situ reporter gene analysis and 2D electrophoretic analysis, Sauer et al. (2002) have suggested that biofilm development by P. aeruginosa occurs in five specific stages: reversible attachment, irreversible attachment, maturation-1, maturation-2 and dispersion.”
BackgroundMethodInfluentialMicrobiology of Apical Periodontitis
Siqueira, J. F., Jr., & Rôças, I. N. (2019) · Wiley eBooks · doi:10.1002/9781119272014.ch4 · Cited by 39
Klein, E. M., Knoll, M. T., & Gescher, J. (2023) · Microbial Biotechnology · doi:10.1111/1751-7915.14236 · Cited by 36
Quenching and quorum sensing in bacterial bio-films
Kameswaran, S., Gujjala, S., Zhang, S., Kondeti, S., Mahalingam, S., Manjunatha, B., & Ramesh, B. (2023) · Research in Microbiology · doi:10.1016/j.resmic.2023.104085 · Cited by 39
Biofilm-specific extracellular matrix proteins of nontypeableHaemophilus influenzae
Wu, S., Baum, M. M., Kerwin, J., Guerrero‐Given, D., Webster, S., Schaudinn, C., VanderVelde, D. G., & Webster, P. C. (2014) · Pathogens and Disease · doi:10.1111/2049-632x.12195 · Cited by 39
“…et al., 2005, Bookwalter et al., 2008, Ronander et al., 2008), biofilmspecific protein regulation, and control of transformation into the biofilm phenotype (Sauer & Camper, 2001, Oosthuizen et al., 2002, Sauer et al., 2002, Vilain et al., 2004, SoutheyPillig et al., 2005, Allegrucci et al., 2006).”
BackgroundKashef, N., Karami, S., & Djavid, G. E. (2015) · Photodiagnosis and Photodynamic Therapy · doi:10.1016/j.pdpdt.2015.04.001 · Cited by 40
“Several advantages exist for bacteria that live in a biofilm phenotype including structural stability, firm adherence to biotic or abiotic surfaces, increased virulence, and resistance to both antimicrobial therapy and the host immune response [1—3].”
BackgroundComparative transcriptomic analysis ofClostridium perfringensbiofilms and planktonic cells
Charlebois, A., Jacques, M., & Archambault, M. (2016) · Avian Pathology · doi:10.1080/03079457.2016.1189512 · Cited by 40
“Moreover, increased protein levels of superoxide dismutase and alkyl hydroperoxide reductase in Pseudomonas aeruginosa biofilm have been observed (Sauer et al., 2002).”
BackgroundHyperoside inhibits biofilm formation of Pseudomonas aeruginosa
Sun, Y., Sun, F., Feng, W., Qiu, X., Liu, Y., Yang, B., Chen, Y., & Xia, P. (2017) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2017.4641 · Cited by 39
“Twitching motility is a type IV pili‑driven movement by which bacteria can adhere and spread biofilm over a surface (40,41).”
She, P., Wang, Y., Luo, Z., Chen, L., Tan, R., Wang, Y., & Wu, Y. C. (2017) · MicrobiologyOpen · doi:10.1002/mbo3.545 · Cited by 41
Zhu, J., Yan, Y., Wang, Y., & Qu, D. (2018) · Journal of Applied Microbiology · doi:10.1111/jam.14187 · Cited by 39
Phenotypic variability promotes diversity and stability in competitive communities
Maynard, D. S., Serván, C. A., Capitán, J. A., & Allesina, S. (2019) · Ecology Letters · doi:10.1111/ele.13356 · Cited by 37
Thuptimdang, P., Siripattanakul‐Ratpukdi, S., Ratpukdi, T., Youngwilai, A., & Khan, E. (2020) · Water Environment Research · doi:10.1002/wer.1493 · Cited by 39
“At the cellular level, biofilm formation can be categorized into four stages of development as shown in Figure 2a (Sauer et al., 2002; Reisner et al., 2003; Garrett et al., 2008; Wood et al., 2010).”
BackgroundA role for TonB1 in biofilm formation and quorum sensing in Pseudomonas aeruginosa
Abbas, A., Adams, C., Scully, N. M., Glennon, J. D., & O’Gara, F. (2007) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2007.00845.x · Cited by 38
Ilyina, T. S., Romanova, Y. M., & Al, G. (2004) · Russian Journal of Genetics · doi:10.1023/b:ruge.0000048660.19958.c3 · Cited by 39
“At this stage, most proteins are suppressed [24].”
BackgroundMethodInfluentialO'May, C. Y., Reid, D. W., & Kirov, S. M. (2006) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2006.00157.x · Cited by 39
Vyas, K. S., & Wong, L. K. (2015) · Annals of Plastic Surgery · doi:10.1097/sap.0000000000000440 · Cited by 39
“The formation of a biofilm requires a complex set of transcription events that trigger phenotypic and morphologic changes in the microorganisms.(9) This cannot be measured by a simple cfu count alone.”
BackgroundInfluentialWang, Y., Dai, Y., Zhang, Y., Hu, Y., Yang, B., & Chen, S. (2007) · Science in China Series C Life Sciences · doi:10.1007/s11427-007-0044-y · Cited by 39
Zagrodnik, R., Thiel, M., Seifert, K., Włodarczak, M., & Łaniecki, M. (2013) · International Journal of Hydrogen Energy · doi:10.1016/j.ijhydene.2013.01.023 · Cited by 38
Biofilm Processes and Control in Water and Wastewater Treatment
Butler, C. S., & Boltz, J. P. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-382182-9.00083-9 · Cited by 45
The Influence of Fluid Flow on Modeling Quorum Sensing in Bacterial Biofilms
Vaughan, B. L., Smith, B., & Chopp, D. L. (2010) · Bulletin of Mathematical Biology · doi:10.1007/s11538-009-9485-8 · Cited by 38
“be physiologically distinct from free swimming bacteria of the same species (Prigent-Combaret et al., 2000; Sauer et al., 2002; Whiteley et al., 2001).”
BackgroundZhu, X., Oh, H., Ng, Y. C. B., Tang, P. Y. P., Barraud, N., & Rice, S. A. (2018) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01832-17 · Cited by 38
“Bacterial biofilms develop through several stages, including initial reversible attachment, irreversible attachment, maturation, and dispersal (9).”
BackgroundRicciardelli, A., Casillo, A., Vergara, A., Balasco, N., Corsaro, M. M., Tutino, M. L., & Parrilli, E. (2018) · Microbiological Research · doi:10.1016/j.micres.2018.09.010 · Cited by 38
Kamarudheen, N., & Rao, K. V. B. (2018) · Microbial Pathogenesis · doi:10.1016/j.micpath.2018.11.050 · Cited by 38
In-situ detection based on the biofilm hydrophilicity for environmental biofilm formation
Tanaka, N., Kogo, T., Hirai, N., Ogawa, A., Kanematsu, H., Takahara, J., Awazu, A., Fujita, N., Haruzono, Y., Ichida, S., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-44167-6 · Cited by 38
Yang, L., Liu, Y., Sternberg, C., & Molin, S. (2010) · Molecules · doi:10.3390/molecules15020780 · Cited by 38
“Biofilm cells display multiple phenotypes and are surrounded by resistant extracellular polymeric substance (EPS) materials [7], which are often major causes for persistent infections [6].”
BackgroundNeutral super-oxidised solutions are effective in killingP. aeruginosabiofilms
Sauer, K., Thatcher, E., Northey, R. A., & Gutierrez, A. A. (2008) · Biofouling · doi:10.1080/08927010802441412 · Cited by 40
“Biofilm formation using a continuous flow tube reactor Biofilms were grown as previously described (Sauer et al. 2002; 2004; Morgan et al. 2006).”
BackgroundMethodSelf-citationPeriodicity of Cell Attachment Patterns during Escherichia coli Biofilm Development
Игоревич, А. К., Jackson, D., & Romeo, T. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.18.5632-5638.2003 · Cited by 38
“Spatial features of the biofilm no doubt reflect the particular species and its environment and in part define the biofilm phenotype (24, 29, 35).”
BackgroundHuang, Y., Dobretsov, S., Xiong, H., & Qian, P. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00578-07 · Cited by 38
“The first three stages can happen in hours (35, 43).”
BackgroundMOLECULAR BASIS OF BIOFILM DEVELOPMENT BY PSEUDOMONADS
Toutain, C. M., Caiazza, N. C., & O’Toole, G. A. (2004) · Wiley eBooks · doi:10.1128/9781555817718.ch4 · Cited by 38
Biofilm-Associated Candidiasis: Pathogenesis, Prevalence, Challenges and Therapeutic Options
Amann, V., Kissmann, A., Firacative, C., & Rosenau, F. (2025) · Pharmaceuticals · doi:10.3390/ph18040460 · Cited by 44
“[139] CLSM Using confocal laser scanning microscopy (CLSM) technology, thick biological samples, such as microbial biofilms, can be scanned by capturing images in a line-by-line fashion along the X, Y, and Z axes.”
The Influence of Biofilms in the Biology of Plasmids
Cook, L. C., & Dunny, G. M. (2014) · Microbiology Spectrum · doi:10.1128/microbiolspec.plas-0012-2013 · Cited by 37
“1 utilized rod-shaped motile bacteria such as E. coli, P. aeruginosa , and Bacillus subtilis (5, 6, 7, 8, 9).”
Analysis of the biofilm proteome of Xylella fastidiosa
Silva, M. S., de Souza, A. A., Takita, M. A., Labate, C. A., & Machado, M. A. (2011) · Proteome Science · doi:10.1186/1477-5956-9-58 · Cited by 36
“According to their protein profiles, dispersed bacteria were closer to planktonic cells than to maturestage biofilm organisms [9].”
BackgroundThe critical role of biofilms in bacterial vascular plant pathogenesis
Mina, I., Jara, N., Criollo, J. E., & Castillo, J. A. (2019) · Plant Pathology · doi:10.1111/ppa.13073 · Cited by 37
Effect of predation on the mechanical properties and detachment of MABR biofilms
Kim, B., Pérez-Calleja, P., Li, M., & Nerenberg, R. (2020) · Water Research · doi:10.1016/j.watres.2020.116289 · Cited by 37
Effect of Tissue Fluids on Hydrophobicity and Adherence of Enterococcus faecalis to Dentin
George, S., & Kishen, A. (2007) · Journal of Endodontics · doi:10.1016/j.joen.2007.07.035 · Cited by 37
Anand, S. K., & Singh, D. K. (2013) · Journal of Dairy Science · doi:10.3168/jds.2013-7012 · Cited by 37
“Resistance of biofilm-embedded bacteria to cleaning processes has also been previously reported to be different from that of their planktonic counterparts (Sternberg et al., 1999; Loo et al., 2000; Stewart and Costerton, 2001; Donlan and Costerton, 2002; Keevil, 2002; Sauer et al., 2002; Chmielewski and Frank, 2003; S…”
BackgroundMusk, D. J., & Hergenrother, P. J. (2008) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2008.03751.x · Cited by 38
“For example, P. aeruginosa biofilms have at least sixfold up- or downregulation of more than 800 genes compared with planktonic levels during the course of their differentiation into mature biofilms; this is well over 50% of this organism’s genome (Sauer et al. 2002).”
BackgroundBoari, C. A., Alves, M. P., Tebaldi, V. M. R., Savian, T. V., & Píccoli, R. H. (2009) · Food Science and Technology · doi:10.1590/s0101-20612009000400029 · Cited by 37
Soybean Lectin Enhances Biofilm Formation by Bradyrhizobium japonicum in the Absence of Plants
Pérez-Giménez, J., Mongiardini, E. J., Althabegoiti, M. J., Covelli, J., Quelas, J. I., López‐García, S. L., & Lodeiro, A. R. (2009) · International Journal of Microbiology · doi:10.1155/2009/719367 · Cited by 37
IsPseudomonas aeruginosaOnly “Sensing Quorum”?
Soberón‐Chávez, G., Aguirre-Ramírez, M., & Ordóñez, L. G. (2005) · Critical Reviews in Microbiology · doi:10.1080/10408410591005138 · Cited by 37
“aeruginosa QS response is involved in biofilm formation (Davies et al. 1998; De Kievit et al. 2001; Hentzer et al. 2003; Heydorn et al. 2002; Sauer et al. 2002; Yoon et al. 2002).”
BackgroundInfluentialXia, S., Zhou, L., Zhang, Z., & Li, J. (2012) · Journal of Environmental Sciences · doi:10.1016/s1001-0742(11)61060-7 · Cited by 37
Inhibition of quorum sensing in a computational biofilm simulation
Fozard, J., Lees, M., King, J. R., & Logan, B. S. (2012) · Biosystems · doi:10.1016/j.biosystems.2012.02.002 · Cited by 37
“, 2002), with some authors reportng a difference in the structure of EPS produced by mutant strains hich are defective in quorum sensing (Sauer et al., 2002); for a ecent review see de Kievit (2009).”
BackgroundGunther, N. W., IV, Núñez, A., Fortis, L. L., & Solaiman, D. K. Y. (2006) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-006-0169-1 · Cited by 37
Junker, L. M., Peters, J. E., & Hay, A. G. (2006) · Microbiology · doi:10.1099/mic.0.28767-0 · Cited by 37
“, 1995; Stewart, 2003), giving rise to microorganisms that are, as a whole, physiologically different from their planktonic or free-swimming counterparts (Reisner et al., 2003; Sauer et al., 2002).”
BackgroundROLE FOR BIOFILMS IN INFECTIOUS DISEASE
Ehrlich, G. D., Hu, F. Z., & Post, J. C. (2004) · doi:10.1128/9781555817718.ch18 · Cited by 37
Self-citationElnegery, A. A., Mowafy, W. K., Zahra, T. A., & El-Khier, N. T. A. (2021) · Access Microbiology · doi:10.1099/acmi.0.000211 · Cited by 43
“The rhl system shares biofilm maturation through deposition of rhamnolipid [28].”
BackgroundXu, C., Yang, Y., Zhou, Y., Hao, M.-Q., Ren, Y.-Z., Wang, X., Chen, J., Ishfaq, M., Wang, S., Liu, D., et al. (2017) · Frontiers in Pharmacology · doi:10.3389/fphar.2017.00543 · Cited by 36
“GAPDH is upregulated in biofilms formed by various bacterial species (Sauer et al., 2002; Planchon et al., 2009; Wang et al., 2012).”
BackgroundLeid, J. G., Costerton, J. W., Shirtliff, M. E., Gilmore, M. S., & Engelbert, M. (2002) · DNA and Cell Biology · doi:10.1089/10445490260099692 · Cited by 36
“Third, a number of studies have shown that the gene expression within biofilms is altered due to the physical action of attachment (Davies et al. , 1993; Dalton and March, 1998; Mah and O’Toole, 2001; Pratten et al. , 2001; Sauer and Camper, 2001; Sauer et al. , 2002).”
Self-citationResident Parking Only: Rhamnolipids Maintain Fluid Channels in Biofilms
Espinosa‐Urgel, M. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.3.699-700.2003 · Cited by 36
“However, it has been only in the past few years that research on the biology of microbial biofilms has geared from a descriptive discipline toward the study of the molecular mechanisms underlying this form of bacterial life (18, 19, 20, 22).”
BackgroundQUORUM SENSING IN BIOFILMS: GOSSIP IN SLIME CITY
Hentzer, M., Givskov, M., & Eberl, L. (2004) · doi:10.1128/9781555817718.ch7 · Cited by 36
Out-Smarting the Host: Bacteria Maneuvering the Immune Response to Favor Their Survival
Mues, N., & Chu, H. W. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00819 · Cited by 35
vpsA-andluxO-independent biofilms ofVibrio cholerae
ller, J. M. ⁄., Miller, M. C., Nielsen, A. T., Schoolnik, G. K., & Spormann, A. M. (2007) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2007.00884.x · Cited by 35
“For a variety of microorganisms it was reported that biofilms disintegrate as part of their life cycle (TolkerNielsen et al., 2000; Sauer et al., 2002; Rice et al., 2005).”
BackgroundPolymer Designs to Control Biofilm Growth on Medical Devices
Francolini, I., Donelli, G., & Stoodley, P. (2003) · Reviews in Environmental Science and Bio/Technology · doi:10.1023/b:resb.0000040469.26208.83 · Cited by 35
“Sauer et al. (2002) showed, by comparing two-dimensional-gel protein patterns, that dispersed cells of P. aeruginosa are more similar to planktonic than to mature biofilm cells.”
BackgroundEffect of acid stress on the physiology of biofilm cells of Streptococcus mutans
McNeill, K. D., & Hamilton, I. R. (2004) · Microbiology · doi:10.1099/mic.0.26482-0 · Cited by 35
“…cell-to-cell signalling, including a variety of pathways invoked not only during the initiation of biofilm formation, but also during the succession of the biofilm community (O’Toole & Kolter, 1998; Christensen et al., 1998; Prigent-Combaret et al., 1999; Davey &O’Toole, 2000; Sauer et al., 2002).”
BackgroundAnalysis of the growth phase-associated transcriptome of Streptococcus pyogenes
Beyer-Sehlmeyer, G., Kreikemeyer, B., Hörster, A., & Podbielski, A. (2005) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2005.02.010 · Cited by 35
Biofilm Formation in the Rhizosphere: Multispecies Interactions and Implications for Plant Growth
Angus, A. A., & Hirsch, A. M. (2013) · doi:10.1002/9781118297674.ch66 · Cited by 35
“and characteristics described by Sauer et al. (2002).”
BackgroundOmpR and RcsB abolish temporal and spatial changes in expression of flhD in Escherichia coli Biofilm
Samanta, P., Clark, E. R., Knutson, K., Horne, S. M., & Prüß, B. M. (2013) · BMC Microbiology · doi:10.1186/1471-2180-13-182 · Cited by 34
“Originally described in Pseudomonas aeruginosa, it is now widely accepted that biofilm development in many bacteria involves reversible attachment, irreversible attachment, maturation, and dispersion [31].”
BackgroundVahedi‐Shahandashti, R., Kermanshahi, R. K., & Ghadam, P. (2016) · TURKISH JOURNAL OF MEDICAL SCIENCES · doi:10.3906/sag-1505-51 · Cited by 34
Molecular and Proteomic Analysis of Levofloxacin and Metronidazole Resistant Helicobacter pylori
Hanafi, A., Lee, W. C., Loke, M. F., Teh, X., Shaari, A., Dinarvand, M., Lehours, P., Mégraud, F., Leow, A. H., Vadivelu, J., et al. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.02015 · Cited by 34
“Annexin V-positive and propidium iodide-negative cells were considered as apoptotic cells (Sawai and Domae, 2011).”
BackgroundBrockman, K. L., Azzari, P. N., Branstool, M. T., Atack, J. M., Schulz, B. L., Jen, F. E. ‐., Jennings, M. P., & Bakaletz, L. O. (2018) · mBio · doi:10.1128/mbio.01682-18 · Cited by 33
“Biofilm formation and maturation are a dynamic process with ongoing changes in gene and protein expression over time (26, 37).”
BackgroundDeep-Subsurface Pressure Stimulates Metabolic Plasticity in Shale-Colonizing Halanaerobium spp
Booker, A. E., Hoyt, D. W., Meulia, T., Eder, E., Nicora, C., Purvine, S. O., Daly, R. A., Moore, J. D., Wunch, K. G., Pfiffner, S. M., et al. (2019) · Applied and Environmental Microbiology · doi:10.1128/aem.00018-19 · Cited by 34
“(epimerases [32] [WG8-10872] and isomerases [33] [WG8-10873]), sugar transport (TamB [34] [WG8-10736] and TolC [35] [WG8-10534]), and glycogen formation (pullu-”
BackgroundRubini, D., Varthan, P. V., Senthilganesh, J., Hari, B. N. V., & Nithyanand, P. (2020) · Microbial Pathogenesis · doi:10.1016/j.micpath.2020.103973 · Cited by 34
Ripa, R., Shen, A. Q., & Funari, R. (2020) · ACS Omega · doi:10.1021/acsomega.9b03540 · Cited by 34
Tolker‐Nielsen, T. (2015) · ASM Press eBooks · doi:10.1128/9781555817466.ch3 · Cited by 35
Biofilms: possible strategies for suppression in chronic wounds
Percival, S. L., & CUTTING, K. F. (2009) · Nursing Standard · doi:10.7748/ns.23.32.64.s50 · Cited by 35
Favre‐Bonté, S., Chamot, E., Köhler, T., Romand, J.-A., & van Delden, C. (2007) · BMC Microbiology · doi:10.1186/1471-2180-7-33 · Cited by 34
“aeruginosa biofilms [7,26], C4-HSL seems to be important during the maturation stage of biofilm development [27], for the total amount of biofilm formed [8], and for the maintenance of biofilm architecture [28].”
Phenazines: Natural products for microbial growth control
Sousa, C. A., Ribeiro, M., Vale, F., & Simões, M. V. (2023) · hLife · doi:10.1016/j.hlife.2023.11.005 · Cited by 35
“Also, QS regulates changes between phenotypes of typical single cells and cells in complex communities [11].”
Vohra, M., Kour, A., Kalia, N. P., Kumar, M., Sharma, S., Jaglan, S., Kamath, N., & Sharma, S. (2023) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2023.128563 · Cited by 33
How to study biofilms: technological advancements in clinical biofilm research
Cleaver, L. M., & Garnett, J. A. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1335389 · Cited by 35
Yang, Y., Kong, X., Niu, B., Yang, J., & Chen, Q. (2024) · Foods · doi:10.3390/foods13071076 · Cited by 33
“The formation process of biofilms is the transition from plankton to the state of envelope [11], and there are multi-component changes in the formation process.”
BackgroundGhosh, S., Qureshi, A., & Purohit, H. J. (2017) · International Biodeterioration & Biodegradation · doi:10.1016/j.ibiod.2017.01.019 · Cited by 33
Nazir, R., Zaffar, R., & Amin, I. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-817495-1.00008-6 · Cited by 37
Development, standardization, and validation of a biofilm efficacy test: The single tube method
Goeres, D. M., Walker, D. K., Buckingham‐Meyer, K., Lorenz, L., Summers, J., Fritz, B. G., Goveia, D., Dickerman, G. E., Schultz, J. M., & Parker, A. E. (2019) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2019.105694 · Cited by 33
From Microbial Communities to Distributed Computing Systems
Karkaria, B. D., Treloar, N. J., Barnes, C. P., & Fedorec, A. J. H. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00834 · Cited by 33
“…itself is a form of computation through communication, invoking a pattern of gene expression to drive a developmental process (Davies et al., 1998; Sauer et al., 2002; Liu et al., 2017; Abisado et al., 2018), similar to how morphogen gradients that define cell fate are a well-characterized form…”
BackgroundPihl, M., Davies, J. R., de Paz, L. E. C., & Svensäter, G. (2010) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2010.00697.x · Cited by 33
Physiological properties ofStreptococcus mutansUA159 biofilm-detached cells
Liu, J., Ling, J.-Q., Zhang, K., & Wu, C. D. (2012) · FEMS Microbiology Letters · doi:10.1111/1574-6968.12066 · Cited by 33
“The biofilm life cycle has been identified as having several phases, including attachment, microcolony formation, development and maturation, and detachment (Sauer et al., 2002).”
BackgroundAhmed, D., Islam, M. S., Begum, Y. A., Janzon, A., Qadri, F., & Sjöling, Å. (2012) · Journal of Applied Microbiology · doi:10.1111/jam.12109 · Cited by 33
“The first step in biofilm formation is a reversible monolayer of bacteria attached to the surface; this step is initially dependent on flagellar motility and on expression of surface adhesion molecules (Sauer et al. 2002; Moorthy and Watnick 2004).”
BackgroundAnaerobic Biofilm Infections in Cystic Fibrosis
Costerton, J. W. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00698-6 · Cited by 33
Self-citationThe Ever-Changing Role of Biofilms in Plastic Surgery
Constantine, R. S., Constantine, F. C., & Rohrich, R. J. (2014) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0000000000000213 · Cited by 33
Biofilm feeding: Microbial colonization of food promotes the growth of a detritivorous arthropod
Horvathova, T., Babik, W., & Bauchinger, U. (2016) · ZooKeys · doi:10.3897/zookeys.577.6149 · Cited by 33
“…growth Copyright Terézia Horváthová et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.”
BackgroundInfluentialContact Lens Storage Case Hygiene Practice and Storage Case Contamination
Vijay, A. K., Willcox, M. D. P., Zhu, H., & Stapleton, F. J. (2014) · Eye & Contact Lens Science & Clinical Practice · doi:10.1097/icl.0000000000000070 · Cited by 33
The biofilm-metal interface: A hotspot for microbiologically influenced corrosion
Qi, P., Zeng, Y., Zhang, D., Sun, Y., & Wang, P. (2025) · Cell Reports Physical Science · doi:10.1016/j.xcrp.2025.102500 · Cited by 32
Spatiotemporal pharmacodynamics of meropenem- and tobramycin-treated Pseudomonas aeruginosa biofilms
Haagensen, J. A. J., Verotta, D., Huang, L., Engel, J. N., Spormann, A. M., & Yang, K. Y. (2017) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkx288 · Cited by 32
“33,35 Cellswithinthe interior of the biofilm, potentially protected from the effects of tobramycin byperipheral cells, mayhave adapted toa more antibiotic-tolerant stateprior todispersal.”
BackgroundHeacock-Kang, Y., Sun, Z., Zarzycki‐Siek, J., Poonsuk, K., McMillan, I., Chuanchuen, R., & Hoang, T. T. (2018) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01459-18 · Cited by 32
Novel Therapies for Biofilm-Based Candida spp. Infections
Černáková, L., Light, C. J., Salehi, B., Rogel-Castillo, C., Victoriano, M., Martorell, M., Sharifi‐Rad, J., Martins, N. A., & Rodrigues, C. F. (2019) · Advances in experimental medicine and biology · doi:10.1007/5584_2019_400 · Cited by 32
Hook, A. L., Flewellen, J. L., Zaid, I. M., Berry, R. M., Dubern, J., Carabelli, A. M., Wildman, R. D., Russell, N. A., Williams, P. M., & Alexander, M. R. (2019) · mSystems · doi:10.1128/msystems.00390-19 · Cited by 32
Contribution of Microbial Acclimation to Lignite Biomethanization
Zhao, W., Su, X., Xia, D., Li, D., & Guo, H. (2020) · Energy & Fuels · doi:10.1021/acs.energyfuels.9b03137 · Cited by 32
Dong, X., & Yang, L. (2014) · Biofouling · doi:10.1080/08927014.2014.975797 · Cited by 32
“…with observations in other cases where it was shown that in the final stage of biofilm formation, cells may detach and swim away from the mature biofilm and revert to a planktonic lifestyle (Sauer et al. 2002; An et al. 2010), due to the lack of available nutrients (Sauer et al. 2004).”
BackgroundAlexander, S.-A., Kyi, C., & Schiesser, C. H. (2015) · Organic & Biomolecular Chemistry · doi:10.1039/c5ob00284b · Cited by 32
New advances on the Brettanomyces bruxellensis biofilm mode of life
Lebleux, M., Abdo, H., Coelho, C., Basmaciyan, L., Albertin, W., Maupeu, J., Laurent, J., Roullier‐Gall, C., Alexandre, H., Guilloux-Bénatier, M., et al. (2019) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2019.108464 · Cited by 32
Bacterial Adhesion to Natural and Synthetic Fibre-Forming Polymers: Influence of Material Properties
Čuk, N., Simončić, B., Fink, R., & Tomšič, B. (2024) · Polymers · doi:10.3390/polym16172409 · Cited by 31
A Design Principle of Group-level Decision Making in Cell Populations
Fujimoto, K., & Sawai, S. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003110 · Cited by 30
“[59,60].”
Applications of Streptomyces spp. Enhanced Compost in Sustainable Agriculture
Buzón-Durán, L., Pérez‐Lebeña, E., Martín‐Gil, J., Sánchez‐Báscones, M., & Martín‐Ramos, P. (2020) · Soil biology · doi:10.1007/978-3-030-39173-7_13 · Cited by 31
Giraud, C., Bernard, C. S., Ruer, S., & de Bentzmann, S. (2009) · Environmental Microbiology Reports · doi:10.1111/j.1758-2229.2009.00070.x · Cited by 31
Effect of novel antibacterial gallium-carboxymethyl cellulose on Pseudomonas aeruginosa
Valappil, S. P., Yiu, H. H. P., Bouffier, L., Hope, C. K., Evans, G., Claridge, J. B., Higham, S. M., & Rosseinsky, M. J. (2012) · Dalton Transactions · doi:10.1039/c2dt32235h · Cited by 31
Leid, J. G., Kerr, M., Selgado, C., Johnson, C., Moreno, G. O., Smith, A. P., Shirtliff, M. E., O’Toole, G. A., & Cope, E. K. (2009) · Infection and Immunity · doi:10.1128/iai.00075-09 · Cited by 31
“clusters proceed to individual dispersed cells, flagella are again upregulated (48, 49).”
BackgroundRhipicephalus (Boophilus) microplus
Pereira, M. D. C., & Labruna, M. B. (2008) · Cited by 31
Shao, J., Cheng, H., Wang, C., & Wang, Y. (2012) · Molecules · doi:10.3390/molecules170911242 · Cited by 31
“put forward five stages of biofilm formation, namely: (i) reversible attachment (>0 min); (ii) irreversible attachment (2 h); (iii) maturation-1 (3 days); (iv) maturation-2 (6 days); and (v) dispersion (9–12 days) [21].”
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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