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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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BackgroundEndemic Malagasy Dalbergia species inhibit quorum sensing in Pseudomonas aeruginosa PAO1
Rasamiravaka, T., Jedrzejowski, A., Kiendrébeogo, M., Rajaonson, S., Randriamampionona, D., Rabemanantsoa, C., Andriantsimahavandy, A., Rasamindrakotroka, A., Duez, P., Jaziri, M. E., et al. (2013) · Microbiology · doi:10.1099/mic.0.064378-0 · Cited by 43
“If biofilm differentiation and maturation are indeed mainly regulated by the las system (Davies et al., 1998; Sauer et al., 2002), Favre-Bonté et al.”
BackgroundInactivation of Streptococcus gordonii SspAB Alters Expression of Multiple Adhesin Genes
Zhang, Y., Yu, L., Nobbs, A. H., Khammanivong, A., & Herzberg, M. C. (2005) · Infection and Immunity · doi:10.1128/iai.73.6.3351-3357.2005 · Cited by 43
“Sessile, planktonic, and free-growing cells express different phenotypes (27, 32, 41).”
BackgroundBruchmann, J., Sachsenheimer, K., Rapp, B. E., & Schwartz, T. (2015) · PLoS ONE · doi:10.1371/journal.pone.0117300 · Cited by 47
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“Briefly, total cell extracts from planktonic and biofilm cells were obtained by sonication as previously described (Sauer et al., 2002) followed by centrifugation for 5 min at 21 200g to pellet unbroken cells.”
MethodInfluentialSelf-citationKarampatzakis, A., Song, C., Allsopp, L. P., Filloux, A., Rice, S. A., Cohen, Y., Wohland, T., & Török, P. (2017) · npj Biofilms and Microbiomes · doi:10.1038/s41522-017-0028-z · Cited by 43
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Self-citationMovement, Replication, and Emigration Rates of Individual Bacteria in a Biofilm
Rice, A., Hamilton, M. A., & Camper, A. K. (2003) · Microbial Ecology · doi:10.1007/s00248-002-1028-x · Cited by 43
“[19] showed that there was activation of the las regulon, loss of motility, and a change in regulation of over 50 proteins in P.”
BackgroundSelf-citationEffect of arsenite on swimming motility delays surface colonization in Herminiimonas arsenicoxydans
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“, 2003a, b; Todhanakasem & Young, 2008) and/or dispersal processes (Sauer et al., 2002; Tolker-Nielsen et al., 2000).”
BackgroundPereira, F. D. E. S., Bonatto, C. C., Lopes, C. A. P., Pereira, A. L., & Silva, L. P. (2015) · Microbial Pathogenesis · doi:10.1016/j.micpath.2015.07.005 · Cited by 42
“1d), a type of organization observed in mature biofilms, which has great importance in its dispersion phase [2,16,17].”
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“problem? One reason to answer “yes” to this question is that microorganisms in biofilms present many novel drug targets because the activities and pathways of microorganisms in a biofilm are distinct from those that are important in free-floating microbial cells [3].”
BackgroundDifferential Proteomic Analysis of a Polymicrobial Biofilm
Abidin, Z. Z., Veith, P. D., Dashper, S. G., Zhu, Y., Catmull, D. V., Chen, Y., Heryanto, D. C., Chen, D., Pyke, J. S., Tan, K. H., et al. (2012) · Journal of Proteome Research · doi:10.1021/pr300201c · Cited by 42
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Sensitivity of bacterial biofilms and planktonic cells to a new antimicrobial agent, Oxsil® 320N
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Phenotypic switching: an opportunity to bacteria thrive
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LuxS-Dependent AI-2 Regulates Versatile Functions in Enterococcus faecalis V583
Shao, C., Shang, W., Yang, Z., Sun, Z., Li, Y., Guo, J., Wang, X., Zou, D., Wang, S., Lei, H., et al. (2012) · Journal of Proteome Research · doi:10.1021/pr3002244 · Cited by 40
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The Danger Signal Extracellular ATP Is an Inducer of Fusobacterium nucleatum Biofilm Dispersal
Ding, Q., & Tan, K. S. (2016) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2016.00155 · Cited by 43
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Against friend and foe: Type 6 effectors in plant-associated bacteria
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“…the T6SS has been linked to biofilm formation in a number of diverse human pathogens such as Vibrio parahaemolyticus, E. coli, and P. aeruginosa (Sauer et al., 2002; Enos-Berlage et al., 2005; Southey-Pillig et al., 2005; Aschtgen et al., 2008) When R. solanacearum lacking a functional TssBRS…”
BackgroundBiofilms’ Role in Planktonic Cell Proliferation
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“While this conceptual view of biofilm development as a linear process, consisting of five consecutive phases [2], can be beneficial in elucidating the various biotic and abiotic factors that influence biofilm formation, it can also obscure the fact that detachment does occur during earlier stages of the biofilm life-c…”
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“aeruginosa (Sauer et al., 2002; Webb et al., 2003, 2004; Kirov et al., 2005), have been shown to generate phenotypic variants, which are the consequence of genetic mutation(s) (Cano et al.”
BackgroundComplex Signaling Networks Controlling Dynamic Molecular Changes in Pseudomonas aeruginosa Biofilm
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Division of Labor, Bet Hedging, and the Evolution of Mixed Biofilm Investment Strategies
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Enhancing curcumin's solubility and antibiofilm activity via silica surface modification
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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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