The DOI matches its Crossref record; 96 of the 96 references it cites were found in a registry or an index.
EPS—Then and Now
Open accessAbstract
“Slime” played a brief and spectacular role in the 19th century founded by the theory of primordial slime by Ernst Haeckel. However, that substance was never found and eventually abandoned. Further scientific attention slowly began in the 1930s referring to slime as a microbial product and then was inspired by “How bacteria stick” by Costerton et al. in 1978, and the matrix material was considered to be polysaccharides. Later, it turned out that proteins, nucleic acids and lipids were major other constituents of the extracellular polymeric substances (EPS), an acronym which was highly discussed. The role of the EPS matrix turns out to be fundamental for biofilms, in terms of keeping cells in proximity and allowing for extended interaction, resource capture, mechanical strength and other properties, which emerge from the life of biofilm organisms, including enhanced tolerance to antimicrobials and other stress. The EPS components are extremely complex and dynamic and fulfil many functional roles, turning biofilms into the most ubiquitous and successful form of life on Earth.
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“EPS play a fundamental role in formation of biofilm matrix, and cell aggregation or adhesion mechanisms to both the abiotic and biotic surface (i.e., intestinal mucosa).”
From Lactic Acid Bacteria Exopolysaccharides Producers: A Sustainable Tool for Functional Foods (2021) · cites this paper as [3]
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Citations
Cites
Flemming, H.-C., & Wingender, J. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2415 · Cited by 10,137
Self-citationBiofilms: an emergent form of bacterial life
Flemming, H.-C., Wingender, J., Szewzyk, U., Steinberg, P., Rice, S. A., & Kjelleberg, S. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.94 · Cited by 5,979
Self-citationExtracellular 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
Biofilm exopolysaccharides: a strong and sticky framework
Sutherland, I. W. (2001) · Microbiology · doi:10.1099/00221287-147-1-3 · Cited by 1,807
The EPS Matrix: The “House of Biofilm Cells”
Flemming, H., Neu, T. R., & Wozniak, D. J. (2007) · Journal of Bacteriology · doi:10.1128/jb.00858-07 · Cited by 1,801
Self-citationPrinciples of c-di-GMP signalling in bacteria
Hengge, R. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2109 · Cited by 1,617
Distinguishing between resistance, tolerance and persistence to antibiotic treatment
Brauner, A., Fridman, O., Gefen, O., & Balaban, N. Q. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.34 · Cited by 1,612
A field guide to bacterial swarming motility
Kearns, D. B. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2405 · Cited by 1,483
Costerton, J. W., Geesey, G. G., & Cheng, K.-J. (1978) · Scientific American · doi:10.1038/scientificamerican0178-86 · Cited by 1,443
Watnick, P. I., & Kolter, R. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.10.2675-2679.2000 · Cited by 1,434
Flagged first, then by citations
Research works printed but not linked: 10
- Geesey, 1982, Microbial exopolymers: Ecological and economic considerations, ASM News, 48, 9
- Characklis, W.G., and Wilderer, P.A. (1989). Structure and Function of Biofilms, Wiley-Blackwell.
- Wingender, J., Neu, T.R., and Flemming, H.C. (1999). Microbial Extracellular Polymeric Substances, Springer. · DOI
- Wingender, J., Neu, T., and Flemming, H.-C. (1999). Microbial Extracellular Polymeric Substances, Springer. · DOI
- Flemming, H.-C., Neu, T.R., and Wingender, J. (2016). The Perfect Slime: Microbial Extracellular Polymeric Substances (EPS), IWA publishing. · DOI
- Moran, A., Brenan, P., Holst, O., and von Itzstein, M. (2009). Microbial Glycobiology: Structures, Relevance and Applications, Elsevier.
- Flemming, H.-C., Wingender, J., and Neu, T.R. (2016). The Perfect Slime—Microbial Extracellular Substances, IWA Publishing. · DOI
- Flemming, H.-C., Wingender, J., and Neu, T. (2016). The Perfect Slime—Microbial Extracellular Polymeric Substances, IWA Publishing. · DOI
- Flemming, H.-C., Neu, T.R., and Wingender, J. (2016). The Perfect Slime: Microbial Extracellular Polymeric Substances, Springer. · DOI
- Flemming, H.-C., Wingender, J., and Neu, T.R. (2016). The Perfect Slime—Microbial Extracellular Substances, IWA Publishing. · DOI
Cited by
Sorted by citations
Antimicrobial Peptides: Classification, Design, Application and Research Progress in Multiple Fields
Huan, Y., Kong, Q., Mou, H., & Yi, H. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.582779 · Cited by 1,693
Beyond Risk: Bacterial Biofilms and Their Regulating Approaches
Muhammad, M. H., Idris, A. L., Fan, X., Guo, Y., Yu, Y., Jin, X., Qiu, J., Guan, X., & Huang, T. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.00928 · Cited by 888
Amarasiri, M., Sano, D., & Suzuki, S. (2019) · Critical Reviews in Environmental Science and Technology · doi:10.1080/10643389.2019.1692611 · Cited by 660
Bacterial biopolymers: from pathogenesis to advanced materials
Moradali, M. F., & Rehm, B. H. A. (2020) · Nature Reviews Microbiology · doi:10.1038/s41579-019-0313-3 · Cited by 476
Extracellular polymeric substances, a key element in understanding biofilm phenotype
Martino, P. D., & Groupe Biofilm et Comportement Microbien aux Interfaces, L. E.-E. (2018) · AIMS Microbiology · doi:10.3934/microbiol.2018.2.274 · Cited by 457
Metadata
- Authors
- Flemming, H.-C.
- Affiliations
- Nanyang Technological University (SG)
- Corresponding author
- Flemming, Hans-Curt
- ORCID
- Flemming, Hans-Curt
- Venue
- Microorganisms
- Publisher
- MDPI AG
- Published
- 2016-11-18
- Volume
- 4
- Issue
- 4
- Pages
- 41
- ISSN
- 2076-2607 (ISSN-L)
- PMC
- PMC5192524
- OpenAlex
- W2557171271
- Cited by
- 374
- References
- 96
- Citations by year
- 2026: 31 · 2025: 49 · 2024: 55 · 2023: 38 · 2022: 50 · 2021: 35 · 2020: 52 · 2019: 32 · 2018: 20 · 2017: 12
- FWCI
- 1.93
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Microorganisms (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Physical Sciences › Environmental Science › Pollution › Wastewater Treatment and Nitrogen Removal
- Life Sciences › Agricultural and Biological Sciences › Food Science › Polysaccharides Composition and Applications
- Keywords
- extracellular polymeric substances, slime, biofilm, biofilm matrix, polysaccharides, extracellular proteins, extracellular nucleic acids, extracellular lipids, antimicrobial tolerance, Ernst Haeckel
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