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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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BackgroundWeak Rolling Adhesion Enhances Bacterial Surface Colonization
Anderson, B. N., Ding, A. M., Nilsson, L. M., Kusuma, K., Tchesnokova, V. L., Viola Vogel, B., Sokurenko, E. V., & Thomas, W. E. (2006) · Journal of Bacteriology · doi:10.1128/jb.00899-06 · Cited by 75
“Active forms of surface mobility, including type IV pili-mediated twitching motility (27) and flagellar motility (12, 39, 42, 44, 56), have been shown to be important for biofilm formation for E.”
BackgroundTargeted Release of Tobramycin from a pH-Responsive Grafted Bilayer Challenged with S. aureus
Lee, H., Dastgheyb, S., Hickok, N. J., Eckmann, D. M., & Composto, R. J. (2015) · Biomacromolecules · doi:10.1021/bm501751v · Cited by 75
Cherny, K. E., & Sauer, K. (2019) · Journal of Bacteriology · doi:10.1128/jb.00059-19 · Cited by 75
“products or oxygen depletion in the interior of biofilms, making dispersion a process by which bacteria avoid stress associated with biofilm growth and seek nutrient rich environments better suited for survival at new locales (3, 5, 8, 12).”
BackgroundSelf-citationA Global Metabolic Shift Is Linked to Salmonella Multicellular Development
White, A. P., Weljie, A. M., Apel, D., Zhang, P., Shaykhutdinov, R. A., Vogel, H. J., & Surette, M. G. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011814 · Cited by 74
“Microarrays [23,24,25], mutagenesis [26,27] and proteomics [28,29], along with many other approaches, have been successfully used to identify differences between planktonic and biofilm cells.”
MethodPseudomonas aeruginosa Promotes Escherichia coli Biofilm Formation in Nutrient-Limited Medium
Culotti, A., & Packman, A. I. (2014) · PLoS ONE · doi:10.1371/journal.pone.0107186 · Cited by 74
Eckert, R., Brady, K. M., Greenberg, E. P., Qi, F., Yarbrough, D. K., He, J. G., McHardy, I. H., Anderson, M. H., & Shi, W. (2006) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00509-06 · Cited by 74
“aeruginosa readily forms a biofilm, characterized by the secretion of an extracellular matrix of various polysaccharides and the up-regulation of a number of genes involved in surface adherence (19, 20, 32, 36, 41).”
BackgroundBehnke, S., Parker, A. E., Woodall, D., & Camper, A. K. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.05514-11 · Cited by 74
“Cells in a biofilm display different phenotypes, therefore allowing for the differentiation of the biofilm into complex multicellular structures and optimizing survival during treatment with antibiotics or disinfectants (8, 27).”
BackgroundSelf-citationApproaches to Targeting Bacterial Biofilms in Cystic Fibrosis Airways
Martin, I., Waters, V. J., & Grasemann, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22042155 · Cited by 76
Chung, J. H., Eisha, S., Park, S., Morris, A. J., & Martin, I. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24108709 · Cited by 80
“Maturing biofilms are characterized by profound changes in the expression of genes that control twitching motility, EPS secretion, and quorum sensing systems, resulting in an intricately structured, highly responsive, heterogeneous bacterial community [23].”
BackgroundJain, K., Parida, S., Mangwani, N., Dash, H. R., & Das, S. (2013) · Annals of Microbiology · doi:10.1007/s13213-013-0618-9 · Cited by 73
“The biofilm growth pattern specifies the previous finding of biofilm growth phases that include attachment, maturation and dispersion (Sauer et al. 2002).”
BackgroundBalsanelli, E., Baura, V. A., Pedrosa, F. D. O., de Souza, E. M., & Monteiro, R. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110392 · Cited by 73
“counterparts [16].”
Critical roles of arginine in growth and biofilm development by S treptococcus gordonii
Jakubovics, N. S., Robinson, J. C., Samarian, D. S., Kolderman, E., Yassin, S. A., Bettampadi, D., Bashton, M., & Rickard, A. H. (2015) · Molecular Microbiology · doi:10.1111/mmi.13023 · Cited by 73
Biofilms in endodontic infection
Siqueira, J. F., Jr., Rôças, I. N., & Ricucci, D. (2010) · Endodontic Topics · doi:10.1111/j.1601-1546.2012.00279.x · Cited by 78
Petrova, O. E., Cherny, K. E., & Sauer, K. (2014) · Journal of Bacteriology · doi:10.1128/jb.01628-14 · Cited by 80
“sonication as previously described (34) followed by centrifugation for 5”
MethodSelf-citationLevels of selection in biofilms: multispecies biofilms are not evolutionary individuals
Clarke, E. (2016) · Biology & Philosophy · doi:10.1007/s10539-016-9517-3 · Cited by 75
Amari, D. T., Marques, C. N. H., & Davies, D. G. (2013) · Journal of Bacteriology · doi:10.1128/jb.00707-13 · Cited by 72
“Induction of biofilm dispersion in Pseudomonas aeruginosa occurs naturally when biofilm microcolonies attain a critical size, releasing bacteria as free cells into the surrounding environment (2, 3).”
BackgroundMethodInfluentialSelf-citationThe Pseudomonas aeruginosa AlgZR two-component system coordinates multiple phenotypes
Okkotsu, Y., Little, A. S., & Schurr, M. J. (2014) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2014.00082 · Cited by 72
“There are multiple steps in biofilm maturation: (1) initial attachment, (2) microcolony formation, (3) maturation, and (4) dispersion (Sauer et al., 2002; Stoodley et al., 2002).”
BackgroundPetrova, O. E., Cherny, K. E., & Sauer, K. (2014) · Journal of Bacteriology · doi:10.1128/jb.02244-14 · Cited by 77
“Evidence for this is also provided by previous microscopic observations of nutrient-induced dispersion occurring within and outside microcolonies, as well as by findings of nutrient-induced dispersion not being affected in certain biofilms (such as those formed by flgB or pilA mutant strains or the dipA-overexpressing…”
BackgroundInfluentialSelf-citationClinical and Microbiological Aspects of Biofilm-Associated Surgical Site Infections
Edmiston, C. E., McBain, A. J., Roberts, C. D., & Leaper, D. J. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-11038-7_3 · Cited by 75
Tribelli, P. M., & López, N. I. (2011) · Extremophiles · doi:10.1007/s00792-011-0384-1 · Cited by 71
“dispersion stage in biofilms ( Sauer et al. 2002 ) and also it was shown that hypermotile mutants of P. aeruginosa have decreased biofilm formation capability in comparison to the wild type (Caiazza et al. 2007).”
BackgroundComparative transcriptomic analysis of Porphyromonas gingivalisbiofilm and planktonic cells
Lo, A. W. H., Seers, C. A., Boyce, J. D., Dashper, S. G., Slakeski, N., Lissel, J. P., & Reynolds, E. C. (2009) · BMC Microbiology · doi:10.1186/1471-2180-9-18 · Cited by 71
Benamara, H., Rihouey, C., Jouenne, T., & Alexandre, S. (2010) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2010.09.004 · Cited by 69
“Thus, a great number of genetic [12–16] andproteomic investigations [17–20]havebeendevoted todetermine the degree towhich gene regulation during biofilmdevelopment controls the switch from planktonic to biofilm growth.”
BackgroundSwimming Behavior of Pseudomonas aeruginosa Studied by Holographic 3D Tracking
Vater, S. M., Weiße, S., Maleschlijski, S., Lotz, C., Koschitzki, F., Schwartz, T., Obst, U., & Rosenhahn, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087765 · Cited by 70
“Not only initial attachment of bacteria but also biofilm development, maturation and dispersal rely on motility [3].”
BackgroundGhanbari, A., Dehghany, J., Schwebs, T., Müsken, M., Häußler, S., & Meyer‐Hermann, M. (2016) · Scientific Reports · doi:10.1038/srep32097 · Cited by 71
Rana, K. L., Kour, D., Yadav, A. N., Yadav, N., & Saxena, A. K. (2020) · Elsevier eBooks · doi:10.1016/b978-0-444-64279-0.00016-5 · Cited by 75
Islam, M. A., Karim, A., Mishra, P., Dubowski, J. J., Yousuf, A., Sarmin, S., & Khan, M. M. R. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.140138 · Cited by 70
Serum Inhibits P. aeruginosa Biofilm Formation on Plastic Surfaces and Intravenous Catheters
Hammond, A. A., Dertien, J. S., Colmer‐Hamood, J. A., Griswold, J., & Hamood, A. N. (2008) · Journal of Surgical Research · doi:10.1016/j.jss.2008.09.003 · Cited by 72
“aeruginosa biofilm depends on the flagellar-based swimming motility and the type IV pilus-based twitching motility [10].”
BackgroundInfluentialSOS involvement in stress-inducible biofilm formation
Gotoh, H., Kasaraneni, N., Devineni, N., Dallo, S. F., & Weitao, T. (2010) · Biofouling · doi:10.1080/08927014.2010.501895 · Cited by 68
“Biofilms are multicellular communities of unicellular organisms enveloped in an extracellular polymeric matrix that can coat abiotic and biotic surfaces in natural environments and hospital settings (Sauer et al. 2002; Stoodley et al. 2002).”
BackgroundMitzel, M. R., & Tufenkji, N. (2014) · Environmental Science & Technology · doi:10.1021/es404598v · Cited by 70
Infection in ventricular assist devices: the role of biofilm
Padera, R. F. (2006) · Cardiovascular Pathology · doi:10.1016/j.carpath.2006.04.008 · Cited by 69
“The organisms from the biofilm community that do disperse have reverted back to the planktonic gene expression profile [22], and this active detachment is a physiologically mediated event [17].”
BackgroundKozlova, E. V., Popov, V. L., Sha, J., Foltz, S. M., Erova, T. E., Agar, S. L., Horneman, A. J., & Chopra, A. K. (2008) · Microbial Pathogenesis · doi:10.1016/j.micpath.2008.08.007 · Cited by 70
Simonetti, O., Cirioni, O., Ghiselli, R., Goteri, G., Scalise, A., Orlando, F., Silvestri, C., Riva, A., Saba, V., Kiran, M. D., et al. (2008) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01340-07 · Cited by 70
“Another option is the expression of certain genes in a biofilm, conferring enhanced resistance to antibiotics (30, 34).”
BackgroundFactors Affecting Microbial Adhesion to Stainless Steel and Other Materials Used in Medical Devices
Verran, J., & Whitehead, K. A. (2005) · The International Journal of Artificial Organs · doi:10.1177/039139880502801111 · Cited by 70
“However, the cells do not attach to the naked substratum, but to a surface which has been “conditioned” by organic material in the surrounding environment (12, 13).”
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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