Detergent‐induced cell aggregation in subpopulations of Pseudomonas aeruginosa as a preadaptive survival strategy
Open accessAbstract
During growth of Pseudomonas aeruginosa strain PAO1 with the toxic detergent SDS, a part of the population actively formed macroscopic cell aggregates while the other part grew as freely suspended cells. The physiological function of aggregation for growth with SDS was investigated. Three mutants growing with SDS without aggregation were isolated: the spontaneous mutant strain N and two mutants with transposon insertions in the psl operon for exopolysaccharide synthesis. SDS-induced aggregation in strain N but not in a pslJ mutant was restored by complementation with two genes encoding diguanylate cyclases responsible for synthesis of cyclic-di-guanosine monophosphate (c-di-GMP). By expressing a c-di-GMP-specific phosphodiesterase SDS-induced aggregation of strain PAO1 was reduced. Upon exposure to SDS in the presence of the uncoupler carbonyl cyanide chlorophenylhydrazone, the aggregating strains had ca. 500-fold higher survival rates than the non-aggregating strains. Co-incubation experiments revealed that strain N could integrate into aggregates of strain PAO1 and thereby increase its survival rate more than 1000-fold. These results showed that SDS-induced aggregation involved c-di-GMP signalling with the psl operon as a possible target. Cell aggregation could serve as a pre-adaptive strategy ensuring survival and growth of P. aeruginosa populations in environments with multiple toxic chemicals.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The active formation of cell aggregates is a stress response in P. aeruginosa and serves as a survival mechanism when exposed to certain detergents such as sodium dodecyl sulfate (SDS).
“The active formation of cell aggregates is also a stress response in P. aeruginosa and serves as a survival mechanism when exposed to certain detergents such as sodium dodecyl sulfate (SDS) [106],[107].”
From Bacterial autoaggregation (2018) · cites this paper as [107]
The Abstract reports that part of the P. aeruginosa population actively forms aggregates during growth with SDS. It reports a survival advantage when SDS is combined with CCCP, however; the Discussion says aggregation was dispensable under the study's SDS cultivation conditions. The claim omits that qualification when describing aggregation as a survival mechanism upon detergent exposure. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
Ryan, R. P., Fouhy, Y., Lucey, J. F., Crossman, L. C., Spiro, S., He, Y., Zhang, L., Heeb, S., Cámara, M., Williams, P. M., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600345103 · Cited by 507 · see citing works
RetractedSimon, R., Priefer, U. B., & Pühler, A. (1983) · Nature Biotechnology · doi:10.1038/nbt1183-784 · Cited by 7,342 · see citing works
Kovach, M. E., Elzer, P. H., Hill, D. S., Robertson, G. T., Farris, M. A., Roop, R. M., & Peterson, K. M. (1995) · Gene · doi:10.1016/0378-1119(95)00584-1 · Cited by 3,355 · see citing works
Solubilization of membranes by detergents.
Helenius, A., & Simons, K. (1975) · Biochimica et Biophysica Acta · doi:10.1016/0304-4157(75)90016-7 · Cited by 2,690 · see citing works
Extracellular DNA Required for Bacterial Biofilm Formation
Whitchurch, C. B., Tolker-Nielsen, T., Ragas, P. C., & Mattick, J. S. (2002) · Science · doi:10.1126/science.295.5559.1487 · Cited by 2,203 · see citing works
Miller, V. L., & Mekalanos, J. J. (1988) · Journal of Bacteriology · doi:10.1128/jb.170.6.2575-2583.1988 · Cited by 2,138 · see citing works
Lewis, K. (2001) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.45.4.999-1007.2001 · Cited by 1,988 · see citing works
Survival strategies of infectious biofilms
Fux, C. A., Costerton, J. W., Stewart, P. S., & Stoodley, P. (2004) · Trends in Microbiology · doi:10.1016/j.tim.2004.11.010 · Cited by 1,812 · see citing works
Aminoglycoside antibiotics induce bacterial biofilm formation
Hoffman, L. R., D’Argenio, D. A., MacCoss, M. J., Zhang, Z., Jones, R. A., & Miller, S. I. (2005) · Nature · doi:10.1038/nature03912 · Cited by 1,324 · see citing works
An overview of nosocomial infections, including the role of the microbiology laboratory
Emori, T. G., & Gaynes, R. P. (1993) · Clinical Microbiology Reviews · doi:10.1128/cmr.6.4.428 · Cited by 1,262 · see citing works
A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms
Allesen‐Holm, M., Barken, K. B., Yang, L., Klausen, M., Webb, J. S., Kjelleberg, S. J., Molin, S., Givskov, M., & Tolker‐Nielsen, T. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.05008.x · Cited by 1,098 · see citing works
Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants
Klausen, M., Heydorn, A., Ragas, P. C., Lambertsen, L. M., Aaes‐Jørgensen, A., Molin, S., & Tolker‐Nielsen, T. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03525.x · Cited by 1,023 · see citing works
Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation
Drenkard, E., & Ausubel, F. M. (2002) · Nature · doi:10.1038/416740a · Cited by 997 · see citing works
Hickman, J. W., Tifrea, D. F., & Harwood, C. S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507170102 · Cited by 838 · see citing works
C‐di‐GMP: the dawning of a novel bacterial signalling system
Römling, U., Gomelsky, M., & Galperin, M. Y. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04697.x · Cited by 687 · see citing works
Mechanisms of Cyclic-di-GMP Signaling in Bacteria
Jenal, U., & Malone, J. G. (2006) · Annual Review of Genetics · doi:10.1146/annurev.genet.40.110405.090423 · Cited by 648 · see citing works
Efflux-mediated multiresistance in Gram-negative bacteria
Poole, K. (2004) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2004.00763.x · Cited by 612 · see citing works
Ryjenkov, D. A., Tarutina, M. G., Moskvin, O. V., & Gomelsky, M. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.5.1792-1798.2005 · Cited by 577 · see citing works
Evolution of cooperation and conflict in experimental bacterial populations
Rainey, P. B., & Rainey, K. (2003) · Nature · doi:10.1038/nature01906 · Cited by 568 · see citing works
West, S. E. H., Schweizer, H. P., Dall, C., Sample, A. K., & Runyen-Janecky, L. J. (1994) · Gene · doi:10.1016/0378-1119(94)90237-2 · Cited by 567 · see citing works
Kulesekara, H., Lee, V. T., Brenčič, A., Liberati, N. T., Urbach, J. M., Miyata, S., Lee, D. G., Neely, A. N., Hyodo, M., Hayakawa, Y., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511090103 · Cited by 534 · see citing works
Friedman, L., & Kolter, R. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.14.4457-4465.2004 · Cited by 528 · see citing works
Antimicrobial resistance of Pseudomonas aeruginosa biofilms
Drenkard, E. (2003) · Microbes and Infection · doi:10.1016/j.micinf.2003.08.009 · Cited by 520 · see citing works
Christen, M., Christen, B., Folcher, M., Schauerte, A., & Jenal, U. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m504429200 · Cited by 495 · see citing works
Structural basis of activity and allosteric control of diguanylate cyclase
Chan, C., Paul, R., Samoray, D., Amiot, N., Giese, B., Jenal, U., & Schirmer, T. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406134101 · Cited by 477 · see citing works
Déziel, É., Comeau, Y., & Villemur, R. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.4.1195-1204.2001 · Cited by 463 · see citing works
Jackson, K. D., Starkey, M., Kremer, S., Parsek, M. R., & Wozniak, D. J. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.14.4466-4475.2004 · Cited by 422 · see citing works
Autolysis and Autoaggregation in Pseudomonas aeruginosa Colony Morphology Mutants
D’Argenio, D. A., Calfee, M. W., Rainey, P. B., & Pesci, E. C. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.23.6481-6489.2002 · Cited by 416 · see citing works
Luyan, Z., Jackson, K. D., Landry, R. M., Parsek, M. R., & Wozniak, D. J. (2006) · Journal of Bacteriology · doi:10.1128/jb.01202-06 · Cited by 400 · see citing works
The physiology and collective recalcitrance of microbial biofilm communities
Gilbert, P., Maira‐Litrán, T., McBain, A. J., Rickard, A. H., & Fw, W. (2002) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/s0065-2911(02)46005-5 · Cited by 371 · see citing works
Bao, Y., Lies, D. P., Fu, H., & Roberts, G. P. (1991) · Gene · doi:10.1016/0378-1119(91)90604-a · Cited by 338 · see citing works
Putative Exopolysaccharide Synthesis Genes Influence Pseudomonas aeruginosa Biofilm Development
Matsukawa, M., & Greenberg, E. P. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.14.4449-4456.2004 · Cited by 337 · see citing works
Kessler, B., de Lorenzo, V., & Timmis, K. N. (1992) · Molecular and General Genetics MGG · doi:10.1007/bf00587591 · Cited by 324 · see citing works
Extracellular DNA in Single- and Multiple-Species Unsaturated Biofilms
Steinberger, R. E., & Holden, P. A. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.9.5404-5410.2005 · Cited by 309 · see citing works
Characterization of Colony Morphology Variants Isolated from Pseudomonas aeruginosa Biofilms
Kirisits, M. J., Prost, L. R., Starkey, M., et al. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.8.4809-4821.2005 · Cited by 290 · see citing works
Bacteriophage and Phenotypic Variation in Pseudomonas aeruginosa Biofilm Development
Webb, J. S., Lau, M., & Kjelleberg, S. J. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.23.8066-8073.2004 · Cited by 288 · see citing works
Spiers, A. J., Kahn, S. G., Bohannon, J., Travisano, M., & Rainey, P. B. (2002) · Genetics · doi:10.1093/genetics/161.1.33 · Cited by 281 · see citing works
Hyperactive transposase mutants of the Himar 1 mariner transposon
Lampe, D. J., Akerley, B. J., Rubin, E. J., Mekalanos, J. J., & Robertson, H. M. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.20.11428 · Cited by 281 · see citing works
Cyclic‐di‐GMP‐mediated signalling within the σS network of Escherichia coli
Weber, H., Pesavento, C., Possling, A., et al. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05440.x · Cited by 280 · see citing works
Cell signalling by oligosaccharides. Two-component systems in Pseudomonas aeruginosa: why so many?
Rodrigue, A., Quentin, Y., Lazdunski, A. M., et al. (2000) · Trends in Microbiology · doi:10.1016/s0966-842x(00)01833-3 · Cited by 271 · see citing works
Biofilm formation and cellulose expression among diverse environmental Pseudomonas isolates
Ude, S., Arnold, D. L., Moon, C. D., Timms‐Wilson, T. M., & Spiers, A. J. (2006) · Environmental Microbiology · doi:10.1111/j.1462-2920.2006.01080.x · Cited by 267 · see citing works
A Polysaccharide resembling Alginic Acid from a Pseudomonas Micro-organism
Linker, A., & Jones, R. S. (1964) · Nature · doi:10.1038/204187a0 · Cited by 160 · see citing works
Biofilm formation by the small colony variant phenotype of <i>Pseudomonas aeruginosa</i>
Häußler, S. (2004) · Environmental Microbiology · doi:10.1111/j.1462-2920.2004.00618.x · Cited by 143 · see citing works
Rapid gene inactivation inPseudomonas aeruginosa
Windgassen, M., Urban, A., & Jaeger, K. (2000) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2000.tb09424.x · Cited by 125 · see citing works
Hagelueken, G., Adams, T., Wiehlmann, L., Widow, U., Kolmar, H., Tümmler, B., Heinz, D. W., & Schubert, W. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510501103 · Cited by 122 · see citing works
Chemotaxis proteins and transducers for aerotaxis inPseudomonas aeruginosa
Hong, C. S., Shitashiro, M., Kuroda, A., Ikeda, T., Takiguchi, N., Ohtake, H., & Kato, J. (2004) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(04)00009-6 · Cited by 119 · see citing works
Alginate acetylation influences initial surface colonization by mucoid Pseudomonas aeruginosa
Tielen, P., Strathmann, M., Jaeger, K., Flemming, H., & Wingender, J. (2005) · Microbiological Research · doi:10.1016/j.micres.2004.11.003 · Cited by 118 · see citing works
Self-citationOverhage, J., Schemionek, M., Webb, J. S., & Rehm, B. H. A. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.8.4407-4413.2005 · Cited by 114 · see citing works
Goymer, P., Kahn, S. G., Malone, J. G., Gehrig, S. M., Spiers, A. J., & Rainey, P. B. (2006) · Genetics · doi:10.1534/genetics.106.055863 · Cited by 107 · see citing works
Ross, P., Aloni, Y., Weinhouse, H., Michaeli, D., Weinberger-Ohana, P., Mayer, R., & Benziman, M. (1986) · Carbohydrate Research · doi:10.1016/s0008-6215(00)90372-0 · Cited by 102 · see citing works
The metabolic versatility of pseudomonads
Clarke, P. H. (1982) · Antonie van Leeuwenhoek · doi:10.1007/bf00405197 · Cited by 98 · see citing works
Klebensberger, J., Rui, O., Fritz, E., Schink, B., & Philipp, B. (2006) · Archives of Microbiology · doi:10.1007/s00203-006-0111-y · Cited by 85 · see citing works
Self-citationEnhancement of Transformation in Pseudomonas aeruginosa PAO1 by Mg 2+ and Heat
Irani, V. R., & Rowe, J. J. (1997) · BioTechniques · doi:10.2144/97221bm09 · Cited by 56 · see citing works
Shear Stress Affects the Kinetics of Staphylococcus aureus Adhesion to Collagen
Li, Z. J., Mohamed, N., & Ross, J. M. (2000) · Biotechnology Progress · doi:10.1021/bp000117r · Cited by 52 · see citing works
Muscarella, L. F. (2004) · Infection Control and Hospital Epidemiology · doi:10.1086/502402 · Cited by 49 · see citing works
Degradation of and sensitivity to cholate in Pseudomonas sp. strain Chol1
Philipp, B., Erdbrink, H., Suter, M. J. ‐., et al. (2006) · Archives of Microbiology · doi:10.1007/s00203-006-0085-9 · Cited by 46 · see citing works
Self-citationSodium Dodecyl Sulfate Hypersensitivity of clpP and clpB Mutants of Escherichia coli
Rajagopal, S., Sudarsan, N., & Nickerson, K. W. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.8.4117-4121.2002 · Cited by 41 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Trunk, T., Bacterial Cell Surface Group, S. F. G. A. E. B., S. Khalil, H., & C. Leo, J. (2018) · AIMS Microbiology · doi:10.3934/microbiol.2018.1.140 · Cited by 444 · see citing works
“aeruginosa and serves as a survival mechanism when exposed to certain detergents such as sodium dodecyl sulfate (SDS) [106,107].”
BackgroundInfluentialChemotaxis towards autoinducer 2 mediates autoaggregation in Escherichia coli
Laganenka, L., Colin, R., & Sourjik, V. (2016) · Nature Communications · doi:10.1038/ncomms12984 · Cited by 218 · see citing works
Klebensberger, J., Birkenmaier, A., Geffers, R., Kjelleberg, S., & Philipp, B. (2009) · Environmental Microbiology · doi:10.1111/j.1462-2920.2009.02012.x · Cited by 97 · see citing works
Self-citation
- Authors
- Klebensberger, J., Lautenschlager, K., Bressler, D., Wingender, J., & Philipp, B.
- Affiliations
- University of Konstanz (DE)
- University of Duisburg-Essen (DE)
- Corresponding author
- Philipp, Bodo
- Venue
- Environmental Microbiology
- Publisher
- Wiley
- Published
- 2007-05-22
- Volume
- 9
- Issue
- 9
- Pages
- 2247-2259
- ISSN
- 1462-2912 (ISSN-L)
- 1462-2920
- OpenAlex
- W2096050031
- Cited by
- 70
- References
- 57
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 1 · 2022: 4 · 2021: 6 · 2020: 4 · 2019: 3 · 2018: 4 · 2017: 5 · 2016: 5 · 2015: 6 · 2014: 2 · 2013: 2 · 2012: 5
- FWCI
- 1.85
- Type
- journal article
- Language
- en
- Open access
- green
- nbn-resolving.de
- Locations
- Environmental Microbiology (publishedVersion)
- PubMed (publishedVersion)
- KOPS (University of Konstanz) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
- Keywords
- Pseudomonas aeruginosa, cell aggregation, detergent toxicity, sodium dodecyl sulfate, c-di-GMP signalling, exopolysaccharide biosynthesis, diguanylate cyclase, phosphodiesterase, population heterogeneity
- MeSH terms
- Adaptation, Physiological, Detergents, Cyclic GMP, Operon, Pseudomonas aeruginosa, Sodium Dodecyl Sulfate, Signal Transduction, Microscopy, Confocal
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
