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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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“The cell lysis released nutrients into the biofilm matrix [65,66],”
BackgroundBooster biocides and microfouling
Faÿ, F., Linossier, I., Carteau, D., Dheilly, A., Silkina, A., & Vallée‐Rehel, K. (2010) · Biofouling · doi:10.1080/08927014.2010.518234 · Cited by 25
“Several studies have shown that there are metabolic differences leading to changes in the biochemical components, including carbohydrates and proteins in biofilm and planktonic cells of bacteria and diatoms (Sauer and Camper 2001; Sauer et al. 2002; Gjersing et al. 2007; Khodse and Bhosle 2010).”
BackgroundObservations of cell cluster hollowing in Staphylococcus epidermidis biofilms
Stewart, P. S., Rani, S. A., Gjersing, E. L., Codd, S. L., Zheng, Z., & Pitts, B. (2007) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2007.02112.x · Cited by 25
“Because S. epidermidis is nonmotile, the hollowing observed in biofilms of this bacterium cannot be aided by motility as it seems to be in many of the cases described previously (Tolker-Nielsen et al. 2000; Sauer et al. 2002; Hunt et al. 2004; Parsek and Fuqua 2004; Stapper et al. 2004).”
BackgroundResultInfluentialThe adherence of Pseudomonas fluorescens to marble, granite, synthetic polymers, and stainless steel
Careli, R. T., de Andrade, N. J., Soares, N. D. F. F., Júnior, J. I. R., ROSADO, M. S., & Bernardes, P. C. (2009) · Food Science and Technology · doi:10.1590/s0101-20612009000100026 · Cited by 25
Impact of Bacterial Biofilm in Veterinary Medicine: An Overview
Chakraborty, S., Dutta, T. K., De, A., Das, M., & Ghosh, S. (2018) · International Journal of Current Microbiology and Applied Sciences · doi:10.20546/ijcmas.2018.704.366 · Cited by 25
Changes in biofilm formation in the nonflagellated flhB1 mutant of Azospirillum brasilense Sp245
Shelud’ko, A. V., Filip’echeva, Y. A., Shumilova, E. M., Khlebtsov, B. N., Буров, А. М., Petrova, L. P., & Katsy, E. I. (2015) · Microbiology · doi:10.1134/s0026261715010129 · Cited by 25
Impaired oral health: a required companion of bacterial aspiration pneumonia
Ashford, J. R. (2024) · Frontiers in Rehabilitation Sciences · doi:10.3389/fresc.2024.1337920 · Cited by 27
Physiological consequences of mutations in the htpG heat shock gene of Escherichia coli
Grudniak, A., Pawlak, K., Bartosik, K., & Wolska, K. I. (2013) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2013.04.003 · Cited by 24
Extracellular polymeric substances mediate the coaggregation of aquatic biofilm-forming bacteria
Hede, N., & Khandeparker, L. (2020) · Hydrobiologia · doi:10.1007/s10750-020-04411-x · Cited by 25
Seyer, D., Cosette, P., Siroy, A., Dé, E., Lenz, C., Vaudry, H., Coquet, L., & Jouenne, T. (2005) · Biofilms · doi:10.1017/s1479050505001638 · Cited by 24
“The range of the membrane proteome alterations (about 50%) is similar to that observed by Sauer et al. (2002) for the whole proteome of mature biofilm cells (i.”
BackgroundPatell, S., Gu, M., Davenport, P. W., Givskov, M., Waite, R. D., & Welch, M. (2010) · Environmental Microbiology Reports · doi:10.1111/j.1758-2229.2010.00158.x · Cited by 24
Species-dependent hydrodynamics of flagellum-tethered bacteria in early biofilm development
Bennett, R. R., Lee, C. K., de Anda, J., Nealson, K. H., Yildiz, F. H., O’Toole, G. A., Wong, G. C. L., & Golestanian, R. (2016) · Journal of The Royal Society Interface · doi:10.1098/rsif.2015.0966 · Cited by 24
“Stages of biofilm formation include initially approaching the surface and reversible attachment, irreversible attachment, microcolony formation, production of exopolysaccharide matrix and structured growth [7], and dispersion [1,8].”
BackgroundCortisol directly impacts Flavobacterium columnare in vitro growth characteristics
Declercq, A. M., Aerts, J., Ampe, B., Haesebrouck, F., Saeger, S. D., & Decostere, A. (2016) · Veterinary Research · doi:10.1186/s13567-016-0370-9 · Cited by 24
“[37] characterized five stages of biofilm development in Pseudomonas aeruginosa: (i) reversible attachment, (ii) irreversible attachment, (iii) a first maturation stage, (iv) a second maturation stage, and (v) dispersion.”
BackgroundGenetic determinants of Pseudomonas aeruginosa fitness during biofilm growth
Schinner, S., Engelhardt, F., Preuße, M., Thöming, J. G., Tomasch, J., & Häußler, S. (2020) · Biofilm · doi:10.1016/j.bioflm.2020.100023 · Cited by 24
New Technologies for Studying Biofilms
Franklin, M. J., Chang, C. B., Akiyama, T., & Bothner, B. B. (2015) · ASM Press eBooks · doi:10.1128/9781555817466.ch1 · Cited by 24
Tremaroli, V., Fedi, S., Tamburini, S., Viti, C., Tatti, E., Ceri, H., Turner, R. J., & Zannoni, D. (2010) · Biofouling · doi:10.1080/08927014.2010.537099 · Cited by 24
Fast exopolysaccharide secretion of Pseudomonas aeruginosa on polar polymer surfaces
Carnazza, S., Satriano, C., Guglielmino, S. P. P., & Marletta, G. (2005) · Journal of Colloid and Interface Science · doi:10.1016/j.jcis.2005.03.089 · Cited by 24
Waterborne pathogens and dental waterlines
Se, M. (2003) · Dental Clinics of North America · doi:10.1016/s0011-8532(03)00019-3 · Cited by 24
“These bacterial pheromones regulate a wide range of physiologic processes including elaboration of virulence factors and increased production of exopolymer [22–24].”
BackgroundLeggett, A., Li, D., Sindeldecker, D. A., Staats, A. M., Rigel, N., Bruschweiler‐Li, L., Brüschweiler, R., & Stoodley, P. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.833269 · Cited by 23
Zhou, J., Hao, D., Wang, X., Liu, T., He, C., Xie, F., Sun, Y., & Zhang, J. (2006) · PROTEOMICS · doi:10.1002/pmic.200501354 · Cited by 23
Biofilms in the food and beverage industries: an introduction
Cloete, T. E., Molobela, I. P., Merwe, A. V. D., & Richards, M. (2009) · Elsevier eBooks · doi:10.1533/9781845697167.1.3 · Cited by 23
Shetye, G. S., Singh, N., Jia, C., Nguyen, C. D. K., Wang, G., & Luk, Y. (2014) · ChemBioChem · doi:10.1002/cbic.201402093 · Cited by 23
Narisawa, N., Kawarai, T., Suzuki, N., Sato, Y., Ochiai, K., Ohnishi, M., Watanabe, H., & Senpuku, H. (2011) · Journal of Bacteriology · doi:10.1128/jb.05240-11 · Cited by 23
“Biofilm formation consists of several phases: (i) initial adherence of planktonic cells to a surface, (ii) irreversible attachment to the surface, (iii) unstructured biofilm growth through cell division and exopolysaccharide synthesis, and (iv) maturation into a complex three-dimensional architecture of microcolonies…”
BackgroundTrivedi, U., Madsen, J. S., Rumbaugh, K. P., Wolcott, R. D., Burmølle, M., & Sørensen, S. J. (2016) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2016.1252312 · Cited by 26
“versus biofilm cells differ dramatically (Sauer et al., 2002).”
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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