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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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“Flagella also play a critical role in the development of biofilms, where they aid in initial surface adhesion as well as biofilm dispersal (35, 39).”
Bacterial quorum sensing: circuits and applications
Garg, N., Manchanda, G., & Kumar, A. (2013) · Antonie van Leeuwenhoek · doi:10.1007/s10482-013-0082-3 · Cited by 95
“Since QS controls bacterial biofilm differentiation and maturation (Sauer et al. 2002; Xavier and Bassler 2003), interruption of QS by inhibition of QS signal generation (Rasmussen and Givskov 2006); degradation of QS signals (Dong et al.”
BackgroundFrancisella novicida Forms In Vitro Biofilms Mediated by an Orphan Response Regulator
Durham-colleran, M. W., Verhoeven, A. B., & van Hoek, M. L. (2009) · Microbial Ecology · doi:10.1007/s00248-009-9586-9 · Cited by 96
“aeruginosa, a LuxI/LuxR quorum sensing system is required to switch from free-living bacteria to sessile bacteria and biofilm formation within the lungs of cystic fibrosis patients [25, 26].”
BackgroundPseudomonas aeruginosaAlgR Represses the Rhl Quorum-Sensing System in a Biofilm-Specific Manner
Morici, L. A., Carterson, A. J., Wagner, V., Frisk, A., Schurr, J. R., zu Bentrup, K. H., Hassett, D. J., Iglewski, B. H., Sauer, K., & Schurr, M. J. (2007) · Journal of Bacteriology · doi:10.1128/jb.01797-06 · Cited by 96
Self-citationPeeters, E., Nelis, H. J., & Coenye, T. (2009) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkp253 · Cited by 96
“cepacia complex biofilms compared with the younger biofilms (grown after 24 h).(33,34) In fact, the impact of these variations in growth pattern, which are the result of differences in nutritional limitations, can greatly influence the susceptibility to antibiotics.”
BackgroundMcElroy, K., Hui, J. G. K., Woo, J. K. K., Luk, A. W. S., Webb, J. S., Kjelleberg, S. J., Rice, S. A., & Thomas, T. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1314340111 · Cited by 90
“However, nonmucoid motile cells within dispersal populations have been observed in laboratory models of lung infection (24) and also in the 18A clinical isolate used here (9).”
BackgroundBiofilm formation by Listeria monocytogenes on stainless steel surface and biotransfer potential
de Oliveira, M. M. M., Brugnera, D. F., Alves, E., & Píccoli, R. H. (2009) · Brazilian Journal of Microbiology · doi:10.1590/s1517-83822010000100016 · Cited by 96
Roque‐Borda, C. A., Primo, L. M. D. G., Medina‐Alarcón, K. P., Campos, I. C., Nascimento, C. D. F., Saraiva, M. D. M. S., Berchieri, Â., Fusco‐Almeida, A. M., Mendes‐Giannini, M. J. S., Perdigão, J., et al. (2024) · Advanced Science · doi:10.1002/advs.202410893 · Cited by 95
Developments in the study and applications of bacterial transformations of selenium species
Ojeda, J. J., Merroun, M. L., Tugarova, A. V., Lampis, S., Kamnev, A. A., & Gardiner, P. H. E. (2020) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2020.1811199 · Cited by 94
“Moreover, bacteria at any stage of biofilm development are generally believed to be physiologically distinct from those in the planktonic state [51].”
BackgroundPlanktonic-Cell Yield of a Pseudomonad Biofilm
Bester, E., Wolfaardt, G. M., Joubert, L., Garny, K., & Saftić, S. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.12.7792-7798.2005 · Cited by 94
“The authors suggested that these detached bacteria are in transition from an attached to a planktonic phenotype (28).”
BackgroundShaping the growth behaviour of biofilms initiated from bacterial aggregates
Melaugh, G., Hutchison, J., Kragh, K. N., Irie, Y., Roberts, A., Bjarnsholt, T., Diggle, S. P., Gordon, V. D., & Allen, R. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0149683 · Cited by 93
“Bacterial biofilm formation is a complex phenomenon which involves a plethora of biological mechanisms including cell motility [48], EPS production [49, 50], metabolic and other phenotypic differentiation [9, 47, 51], and cell-cell interactions such as quorum sensing [52–54].”
BackgroundCooke, A. C., Florez, C., Dunshee, E. B., Lieber, A. D., Terry, M. L., Light, C. J., & Schertzer, J. W. (2020) · mSphere · doi:10.1128/msphere.01109-20 · Cited by 98
“18ml/ min until the desired stage of biofilm growth: 8 h for reversible attachment, 24 h for irreversible attachment, 3 days for maturation I, and 5 days for maturation II (as determined previously [7] and in this study by microscopic flow cell images).”
MethodDirect Evaluation of Pseudomonas aeruginosa Biofilm Mediators in a Chronic Infection Model
Byrd, M. S., Pang, B., Hong, W., Waligora, E. A., Juneau, R. A., Armbruster, C. E., Weimer, K. E. D., Murrah, K. A., Mann, E. E., Lu, H., et al. (2011) · Infection and Immunity · doi:10.1128/iai.00057-11 · Cited by 93
“Flagella are required for swimming and swarming motility and reversible surface attachment in vitro (38, 44), as well as proinflammatory signaling via interaction with the innate immune receptor TLR5 (21).”
BackgroundListeria monocytogenes Colonizes Pseudomonas fluorescens Biofilms and Induces Matrix Over-Production
Puga, C. H., Dahdouh, E., SanJosé, C., & Orgaz, B. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01706 · Cited by 92
Trampari, E., Holden, E. R., Wickham, G. J., Ravi, A., Martins, L. D. O., Savva, G. M., & Webber, M. A. (2021) · npj Biofilms and Microbiomes · doi:10.1038/s41522-020-00178-0 · Cited by 92
Gene expression profile of the plant pathogen Xylella fastidiosa during biofilm formation in vitro
de Souza, A. A., Takita, M. A., Coletta-Filho, H. D., Caldana, C., Yanai, G. M., Muto, N. H., de Oliveira, R. C., Nunes, L. R., & Machado, M. A. (2004) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2004.tb09716.x · Cited by 92
“The number of biofilm specific genes is similar to other organisms [15,24] but higher than Pseudomonas aeruginosa where a small amount of biofilm induced genes (0.”
BackgroundHarvey, R. J., & Lund, V. J. (2007) · PubMed · Cited by 92
Gupta, K. H., Liao, J., Petrova, O. E., Cherny, K. E., & Sauer, K. (2014) · Molecular Microbiology · doi:10.1111/mmi.12587 · Cited by 92
“Briefly, total cell extracts from biofilms were obtained by sonication as previously described (Sauer et al., 2002) followed by centrifugation for 2 min at 21 200 g to pellet unbroken cells.”
MethodSelf-citationDobretsov, S., Dahms, H.-U., Huang, Y., Wahl, M., & Qian, P. (2007) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2007.00285.x · Cited by 91
“Biofilm formation, in turn, can control many processes at surfaces, for example the uptake or release of compounds by host organisms, bacterial virulence for the host, and biocorrosion (Parsek & Greenberg, 2000; Sauer et al., 2002).”
BackgroundLi, X. Z., Webb, J. S., Kjelleberg, S. J., & Rosche, B. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.72.2.1639-1644.2006 · Cited by 91
“In general, increased resistance in biofilms may be a result of altered gene expression which leads to physiological and/or structural changes during biofilm formation (17, 31, 33, 38).”
BackgroundBöl, M., Ehret, A. E., Albero, A. B., Hellriegel, J., & Krull, R. (2012) · Critical Reviews in Biotechnology · doi:10.3109/07388551.2012.679250 · Cited by 88
“With the attachment of these abraded cells and flakes to a substratum, the cycle starts again (Sauer et al., 2002; Stoodley et al., 2002b).”
Pearson, M. M., Laurence, C. A., Guinn, S. E., & Hansen, E. J. (2006) · Infection and Immunity · doi:10.1128/iai.74.3.1588-1596.2006 · Cited by 91
Chronic tonsillitis and biofilms: a brief overview of treatment modalities
Bakar, M. A., McKimm, J., Haque, S. Z., Majumder, M. A. A., & Haque, M. (2018) · Journal of Inflammation Research · doi:10.2147/jir.s162486 · Cited by 100
Proteomics of the bacterial cross-talk by quorum sensing
Cagno, R. D., Angelis, M. D., Calasso, M. P., & Gobbetti, M. (2010) · Journal of Proteomics · doi:10.1016/j.jprot.2010.09.003 · Cited by 90
Characterization of the OxyR regulon of Neisseria gonorrhoeae
Seib, K. L., Wu, H., Srikhanta, Y. N., Edwards, J. L., Falsetta, M. L., Hamilton, A. J., Maguire, T. L., Grimmond, S. M., Apicella, M. A., McEwan, A. G., et al. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05478.x · Cited by 90
“aeruginosa (Sauer et al., 2002), Campy-”
Pysz, M. A., Conners, S. B., Montero, C. I., Shockley, K. R., Johnson, M. R., Ward, D. E., & Kelly, R. M. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.10.6098-6112.2004 · Cited by 90
“Increased protein levels of superoxide dismutase and alkyl hydroperoxide reductase in aerobic mesophile biofilms have also been reported (90).”
BackgroundPseudomonas aeruginosa biofilms react with and precipitate toxic soluble gold
Karthikeyan, S., & Beveridge, T. J. (2002) · Environmental Microbiology · doi:10.1046/j.1462-2920.2002.00353.x · Cited by 89
Patrauchan, M. A., Sarkisova, S. A., & Franklin, M. J. (2007) · Microbiology · doi:10.1099/mic.0.2007/010371-0 · Cited by 88
“…from cells in planktonic culture, several previous studies have used transcriptomic and proteomic approaches to identify changes in gene expression during P. aeruginosa biofilm development (Sauer et al. , 2002; Southey-Pillig et al. , 2005; Waite et al. , 2005, 2006; Whiteley et al. , 2001).”
BackgroundMethodResultInfluentialT he B iofilm C oncept: C onsequences for F uture P rophylaxis of O ral D iseases?
Scheie, A. A., & Petersen, F. C. (2004) · Critical Reviews in Oral Biology & Medicine · doi:10.1177/154411130401500102 · Cited by 89
“Evidence is emerging that expression of genes required during the various stages is well-regulated (Davies et al., 1998; Pratt and Kolter, 1999; Sauer et al., 2002; Stoodley 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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