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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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BackgroundResultComparative evaluation of biofilm disinfectant efficacy tests
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Matin, A., Laoui, T., Falath, W. S., & Farooque, M. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.142721 · Cited by 199
Silver against Pseudomonas aeruginosa biofilms
Bjarnsholt, T., Kirketerp‐Møller, K., Kristiansen, S., Phipps, R. K., Nielsen, A. K., Jensen, P. Ø., Høiby, N., & Givskov, M. (2007) · Apmis · doi:10.1111/j.1600-0463.2007.apm_646.x · Cited by 198
“Accepted 19 April 2007. available surface followed by growth and proliferation of bacterial microcolonies embedded in a self-made protective matrix of exopolymers (EPS) (1, 2).”
BackgroundInterspecific Bacterial Interactions are Reflected in Multispecies Biofilm Spatial Organization
Liu, W., Røder, H. L., Madsen, J. S., Bjarnsholt, T., Sørensen, S. J., & Burmølle, M. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01366 · Cited by 206
“…cells attaching to a surface, followed by growth into a mature structurally complex biofilm and culminating in the dispersal of detached cells from the biofilm, allowing colonization of new niches (Tolker-Nielsen et al., 2000; Sauer et al., 2002; Hall-Stoodley et al., 2004; Monds and O’Toole, 2009).”
BackgroundTargeting Biofilms Therapy: Current Research Strategies and Development Hurdles
Jiang, Y., Geng, M., & Bai, L. (2020) · Microorganisms · doi:10.3390/microorganisms8081222 · Cited by 209
What is type VI secretion doing in all those bugs?
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Comparison of the Antimicrobial Effects of Chlorine, Silver Ion, and Tobramycin on Biofilm
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“According to previous studies, the effects of the limited penetration of antimicrobial agents (38), changes in the bacterial phenotype of biofilm cells (25, 32 , 40), and biofilm cells in persister states (21, 22, 36, 45), as well as the different reactivities of antimicrobial agents, were widely considered to be fact…”
BackgroundSelf-citationPalanisamy, N. K., Ferina, N., Amirulhusni, A. N., Mohd-Zain, Z., Hussaini, J., Ping, L. J., & Durairaj, R. (2014) · Journal of Nanobiotechnology · doi:10.1186/1477-3155-12-2 · Cited by 196
“The matrix allows the interconnection of immobilized cells which serves as a digestive system and shuts them off from external extracellular enzymes [18,19].”
BackgroundDivision of Labor in Biofilms: the Ecology of Cell Differentiation
van Gestel, J., Vlamakis, H. C., & Kolter, R. (2015) · Microbiology Spectrum · doi:10.1128/microbiolspec.mb-0002-2014 · Cited by 206
“The phenotype of dispersing cells is more similar to those of motile cells that initiate bio fi lm formation than it is to the cells inhabiting a mature microcolony (194).”
BackgroundInfluentialCharge-Switchable Nanozymes for Bioorthogonal Imaging of Biofilm-Associated Infections
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Quorum Quenching Mediated Approaches for Control of Membrane Biofouling
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BackgroundVirulence Factors of Erwinia amylovora: A Review
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“Although the mechanistic details behind biofilm formation remain largely unknown and genetic and structural analyses should be done for full characterization of these structures, it is suggested that they are formed in response to environmental triggers [24,44] and quorum sensing signals [24,45].”
BackgroundAdhesion as a weapon in microbial competition
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“Microbes secrete a range of products that aid in adhesion to surfaces and to other cells (Hall-Stoodley et al. 2004, Petrova & Sauer 2012, Sauer et al. 2002), but even within a single species, microbes vary widely in their tendency to adhere (Carter et al. 2011, Crociani et al. 1995, Dranginis et…”
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“Factors affecting on electro-active biofilm formation Biofilm formation is a continuous and sequential process including transport, attachment, formation of micro-colonies and biofilm maturation in MFCs on the electrode surface (in anode or cathode) (Sauer et al., 2002; Venkata Mohan et al., 2014).”
BackgroundInfluentialControlling Bacterial Biofilms
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“The biofilm developmental life cycle comes full circle when the biofilm cells disperse (51).”
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“Similarly, other studies have shown that motility is not a prerequisite for successful biofilm development (Heydorn et al., 2002; Sauer et al., 2002).”
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“It has therefore been suggested that cells growing as a biofilm express genes that are distinct from those in cells growing planktonically (4, 38).”
BackgroundInterplay of physical mechanisms and biofilm processes: review of microfluidic methods
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“aeruginosa macrocolonies developed on abiotic surfaces (7, 40).”
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Microbial interactions in building of communities
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“Mono-species biofilm formation often proceeds through distinct developmental stages, as exemplified by Pseudomonas aeruginosa (Sauer et al., 2002) and by Candida albicans (Chandra et al., 2001).”
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“We found the assay to be a reproducible measure of cellular attachment and biofilm production when used within the parameters of the original application of the assay, namely, indirect comparative assessment of irreversible bacterial attachment (biofilm production; Sauer et al., 2002) and, subsequently, in vitro biofi…”
MethodDifferences in Metabolism between the Biofilm and Planktonic Response to Metal Stress
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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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