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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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BackgroundMiao, W., Sheng, L., Yang, T., Wu, G., Zhang, M., Sun, J., & Aikemu, A. (2020) · BMC Complementary Medicine and Therapies · doi:10.1186/s12906-020-2833-9 · Cited by 18
Biodegradation of guar gum and its enhancing effect on biogas production from coal
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Evolution of Pseudomonas aeruginosa Pathogenicity: From Acute to Chronic Infections
Oliver, A., Mena, A., & Macia, M. D. (2014) · ASM Press eBooks · doi:10.1128/9781555815639.ch36 · Cited by 18
Zhao, J., Jiang, H., Cheng, W., Wu, J., Zhao, J., Wang, J., & Dong, L. (2014) · Journal of Basic Microbiology · doi:10.1002/jobm.201300987 · Cited by 18
“In the experiment, we observed no significant biofilm formation at reversible attachment stage and irreversible attachment stage, which is different with previous study [27].”
BackgroundResultGeneral Theory for Integrated Analysis of Growth, Gene, and Protein Expression in Biofilms
Zhang, T., Pabst, B., Klapper, I., & Stewart, P. S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083626 · Cited by 18
Cleary, J. M., Lipsky, Z. W., Kim, M., Marques, C. N. H., & German, G. K. (2018) · Journal of The Royal Society Interface · doi:10.1098/rsif.2017.0848 · Cited by 16
Causes and Consequences of a Variant Strain of Phaeobacter inhibens With Reduced Competition
Majzoub, M. E., McElroy, K., Maczka, M., Thomas, T., & Egan, S. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02601 · Cited by 18
Kalia, M., Resch, M. D., Cherny, K. E., & Sauer, K. (2022) · mSphere · doi:10.1128/msphere.00505-22 · Cited by 17
“2 mL/min), using 5-fold diluted VBMM medium (4, 17).”
MethodSelf-citationMorphogenesis of bacterial cables in polymeric environments
Corte, S. G. L., Stevens, C. A., Cárcamo‐Oyarce, G., Ribbeck, K., Wingreen, N. S., & Datta, S. S. (2025) · Science Advances · doi:10.1126/sciadv.adq7797 · Cited by 17
Surface Cell Density Effects on Escherichia coli Gene Expression during Cell Attachment
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Elkhashab, T. H. T., Erfan, D. M., & Kamal, A. A. M. (2016) · The Egyptian Journal of Medical Microbiology · doi:10.12816/0037098 · Cited by 17
Dynamic Sessile‐Droplet Habitats for Controllable Cultivation of Bacterial Biofilm
Jin, Z., Nie, M., Hu, R., Zhao, T., Xu, J., Chen, D., Yun, J., Luyan, Z., & Du, W. (2018) · Small · doi:10.1002/smll.201800658 · Cited by 17
Is it Time to Say Goodbye to Culture and Sensitivity? The Case for Culture-independent Urology
Dixon, M. R., Sha, S. T., Stefil, M., & McDonald, M. W. (2019) · Urology · doi:10.1016/j.urology.2019.11.030 · Cited by 17
Online Quality Measurements of Total Suspended Solids for Offshore Reinjection: A Review Study
Hansen, D. S., Bram, M. V., Lauridsen, S. M. Ø., & Yang, Z. (2021) · Energies · doi:10.3390/en14040967 · Cited by 17
“The biofilm often consist of different microorganism types; even microorganisms that are unable to attach to the surface on their own can still attach themselves to the EPS or directly to the earlier development of the colony [128,129].”
BackgroundSagS and its unorthodox contributions to Pseudomonas aeruginosa biofilm development
Park, S., & Sauer, K. (2021) · Biofilm · doi:10.1016/j.bioflm.2021.100059 · Cited by 17
“3D-biofilm structure, cell-cell communication, and metabolic changes) that can be correlated to distinct episodes or stages of biofilm development [31].”
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Commentary: A Host-Produced Quorum-Sensing Autoinducer Controls a Phage Lysis-Lysogeny Decision
Igler, C., & Abedon, S. T. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01171 · Cited by 17
“, as is associated with DPO detection, biofilm bacteria can be especially metabolically active and additionally, by breaking free of microcolonies, potentially more vulnerable to lytic phages (Sauer et al., 2002; Abedon, 2017b; Vidakovic et al., 2018).”
BackgroundOn the growth and form of bacterial colonies
Porter, R. L., Trenado-Yuste, C., Martínez-Calvo, A., Su, M., Wingreen, N. S., Datta, S. S., & Huang, K. C. (2025) · Nature Reviews Physics · doi:10.1038/s42254-025-00849-x · Cited by 20
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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