Skip to main content
Log in

Effects of non-ionic surfactant on the formation of pellicles by Pseudomonas aeruginosa

  • Original Contribution
  • Published:
Rheologica Acta Aims and scope Submit manuscript

Abstract

It has been previously shown that biological attachment mechanisms are supplemented by surface tension mediated attachment for pellicles formed by Pseudomonas aeruginosa. To further examine the role of surface tension on pellicle formation, non-ionic polyoxyethylene alcohol surfactants were added to growth media. Pellicle attachment and growth is delayed, and moduli are weakened when surfactant is added to growth media at concentrations close to and above the CMC. However, these effects are not primarily due to changes in surface tension. This can be observed by continuing modification of pellicle behavior above the CMC and distinct surfactants at identical surface tensions modifying pellicle moduli differently. Based on changes to bacteria wettability, it is determined that these surfactants modify pellicle formation by adsorbing to bacteria surfaces. Such adsorption is known to increase repulsive forces between gram negative bacteria like Pseudomonas Aeruginosa, which weakens aggregation between bacteria, affecting pellicle formation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abbasnezhad H, Foght JM, Gray MR (2011) Adhesion to the hydrocarbon phase increases phenanthrene degradation by Pseudomonas fluorescens LP6a. Biodegradation 22:485–496

    Article  CAS  Google Scholar 

  • Andersson S, Kuttuva Rajarao G, Land CJ, Dalhammar G (2008) Biofilm formation and interactions of bacterial strains found in wastewater treatment systems. FEMS Microbiol Lett 283:83–90

    Article  CAS  Google Scholar 

  • Armitano J, Méjean V, Jourlin-Castelli C (2014) Gram-negative bacteria can also form pellicles. Environmental Microbiology Reports 6:534–544

    Article  Google Scholar 

  • Bachmann RT, Johnson AC, Edyvean RGJ (2014) Biotechnology in the petroleum industry: an overview. Int Biodeterior Biodegradation 86:225–237. https://doi.org/10.1016/j.ibiod.2013.09.011

    Article  CAS  Google Scholar 

  • Bajaj S, Singh DK (2015) Biodegradation of persistent organic pollutants in soil, water and pristine sites by cold-adapted microorganisms: mini review. Int Biodeterior Biodegradation 100:98–105. https://doi.org/10.1016/j.ibiod.2015.02.023

    Article  CAS  Google Scholar 

  • Berry JD, Neeson MJ, Dagastine RR, Chan DY, Tabor RF (2015) Measurement of surface and interfacial tension using pendant drop tensiometry. J Colloid Interface Sci 454:226–237

    Article  CAS  Google Scholar 

  • Branda SS, Vik Å, Friedman L, Kolter R (2005) Biofilms: the matrix revisited. Trends Microbiol 13:20–26

    Article  CAS  Google Scholar 

  • Brooijmans RJ, Pastink MI, Siezen RJ (2009) Hydrocarbon-degrading bacteria: the oil-spill clean-up crew. Microb Biotechnol 2:587–594

    Article  CAS  Google Scholar 

  • Brooks JD, Flint SH (2008) Biofilms in the food industry: problems and potential solutions. Int J Food Sci Technol 43:2163–2176

    Article  CAS  Google Scholar 

  • Brown DG, Al Nuaimi KS (2005) Nonionic surfactant sorption onto the bacterial cell surface: a multi-interaction isotherm. Langmuir 21:11368–11372

    Article  CAS  Google Scholar 

  • Brown DG, Jaffé PR (2006) Effects of nonionic surfactants on the cell surface hydrophobicity and apparent Hamaker constant of a Sphingomonas sp. Environ Sci Technol 40:195–201. https://doi.org/10.1021/es051183y

    Article  CAS  Google Scholar 

  • Das N, Chandran P (2011) Microbial degradation of petroleum hydrocarbon contaminants: an overview. Biotechnology research international 2011

  • Davies D (2003) Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discovery 2:114–122

    Article  CAS  Google Scholar 

  • Eastoe J, Dalton JS, Rogueda PGA, Crooks ER, Pitt AR, Simister EA (1997) Dynamic surface tensions of nonionic surfactant solutions. J Colloid Interface Sci 188:423–430

    Article  CAS  Google Scholar 

  • Flemming H-C (2002) Biofouling in water systems–cases, causes and countermeasures. Appl Microbiol Biotechnol 59:629–640

    Article  CAS  Google Scholar 

  • Flemming H-C, Wingender J (2010) The Biofilm Matrix Nature Reviews Microbiology 8:623–633

    Article  CAS  Google Scholar 

  • Flemming H-C, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S (2016) Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14:563

    Article  CAS  Google Scholar 

  • Fuentes S, Mendez V, Aguila P, Seeger M (2014) Bioremediation of petroleum hydrocarbons: catabolic genes, microbial communities, and applications. Appl Microbiol Biotechnol 98:4781–4794. https://doi.org/10.1007/s00253-014-5684-9

    Article  CAS  Google Scholar 

  • Hollenbeck EC, Fong JC, Lim JY, Yildiz FH, Fuller GG, Cegelski L (2014) Molecular determinants of mechanical properties of V. cholerae biofilms at the air-liquid interface. Biophys J 107:2245–2252. https://doi.org/10.1016/j.bpj.2014.10.015

    Article  CAS  Google Scholar 

  • Houari A, Picard J, Habarou H, Galas L, Vaudry H, Heim V, Di Martino P (2008) Rheology of biofilms formed at the surface of NF membranes in a drinking water production unit. Biofouling 24:235–240

    Article  CAS  Google Scholar 

  • Hu G, Li J, Zeng G (2013) Recent development in the treatment of oily sludge from petroleum industry: a review. J Hazard Mater 261:470–490

    Article  CAS  Google Scholar 

  • Kim JK, Rühs PA, Fischer P, Hong JS (2013) Interfacial localization of nanoclay particles in oil-in-water emulsions and its reflection in interfacial moduli. Rheol Acta 52:327–335

    Article  CAS  Google Scholar 

  • King GM, Kostka JE, Hazen TC, Sobecky PA (2015) Microbial responses to the deepwater horizon oil spill: from coastal wetlands to the deep sea. Ann Rev Mar Sci 7:377–401. https://doi.org/10.1146/annurev-marine-010814-015543

    Article  CAS  Google Scholar 

  • Klapper I, Dockery J (2010) Mathematical description of microbial biofilms. SIAM Rev 52:221–265

    Article  Google Scholar 

  • Klapper I, Rupp CJ, Cargo R, Purvedorj B, Stoodley P (2002) Viscoelastic fluid description of bacterial biofilm material properties. Biotechnology Bioengineering 80:289–296

    Article  CAS  Google Scholar 

  • Koza A, Hallett PD, Moon CD, Spiers AJ (2009) Characterization of a novel air–liquid interface biofilm of Pseudomonas fluorescens SBW25. Microbiology 155:1397–1406. https://doi.org/10.1099/mic.0.025064-0

    Article  CAS  Google Scholar 

  • Lin S-Y, Lin Y-Y, Chen E-M, Hsu C-T, Kwan C-C (1999) A study of the equilibrium surface tension and the critical micelle concentration of mixed surfactant solutions. Langmuir 15:4370–4376

    Article  CAS  Google Scholar 

  • Mahapatra A, Padhi N, Mahapatra D, Bhatt M, Sahoo D, Jena S, Dash D, Chayani N (2015) Study of biofilm in bacteria from water pipelines. Journal of Clinical and Diagnostic Research: JCDR 9: DC09

  • Morse M, Huang A, Li G, Maxey MR, Tang JX (2013) Molecular adsorption steers bacterial swimming at the air/water interface. Biophys J 105:21–28. https://doi.org/10.1016/j.bpj.2013.05.026

    Article  CAS  Google Scholar 

  • Nielsen CK, Kjems J, Mygind T, Snabe T, Meyer RL (2016) Effects of Tween 80 on growth and biofilm formation in laboratory media. Front Microbiol 7:1878

    Article  Google Scholar 

  • Qi L, Christopher GF (2019) Role of flagella, type IV pili, biosurfactants, and extracellular polymeric substance polysaccharides on the formation of pellicles by Pseudomonas aeruginosa. Langmuir 35:5294–5304

    Article  CAS  Google Scholar 

  • Qi L, Christopher GF (2021) Rheological variability of Pseudomonas aeruginosa biofilms. Rheol Acta 60:219–230

    Article  CAS  Google Scholar 

  • Rosenberg E, Balows A, Truper H, Dworkin M, Harder W, Schleifer K (1992) The hydrocarbon-oxidizing bacteria. The Prokaryotes: a Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications I:446–459

    Google Scholar 

  • Rühs PA, Böcker L, Inglis RF, Fischer P (2014) Studying bacterial hydrophobicity and biofilm formation at liquid–liquid interfaces through interfacial rheology and pendant drop tensiometry. Colloids Surf, B 117:174–184

    Article  Google Scholar 

  • Rühs PA, Böni L, Fuller GG, Inglis RF, Fischer P (2013) In-situ quantification of the interfacial rheological response of bacterial biofilms to environmental stimuli. PLoS One 8:e78524

    Article  Google Scholar 

  • Schroyen B, Gunes DZ, Vermant J (2017) A versatile subphase exchange cell for interfacial shear rheology. Rheol Acta 56:1–10

    Article  CAS  Google Scholar 

  • Schultz M, Bendick J, Holm E, Hertel W (2011) Economic impact of biofouling on a naval surface ship. Biofouling 27:87–98

    Article  CAS  Google Scholar 

  • Shaw T, Winston M, Rupp CJ, Klapper I, Stoodley P (2004) Commonality of elastic relaxation times in biofilms. Phys Rev Lett 93:098102

    Article  CAS  Google Scholar 

  • Sloup RE, Cieza RJ, Needle DB, Abramovitch RB, Torres AG, Waters CM (2016) Polysorbates prevent biofilm formation and pathogenesis of Escherichia coli O104:H4. Biofouling 32:1131–1140. https://doi.org/10.1080/08927014.2016.1230849

    Article  CAS  Google Scholar 

  • Toutain-Kidd CM, Kadivar SC, Bramante CT, Bobin SA, Zegans ME (2009) Polysorbate 80 inhibition of Pseudomonas aeruginosa biofilm formation and its cleavage by the secreted lipase LipA. Antimicrob Agents Chemother 53:136–145

    Article  CAS  Google Scholar 

  • Vaccari L, Allan DB, Sharifi-Mood N, Singh AR, Leheny RL, Stebe KJ (2015) Films of bacteria at interfaces: three stages of behaviour. Soft Matter 11:6062–6074

    Article  CAS  Google Scholar 

  • Van Houdt R, Michiels C (2010) Biofilm formation and the food industry, a focus on the bacterial outer surface. J Appl Microbiol 109:1117–1131

    Article  Google Scholar 

  • Vandebril S, Franck A, Fuller GG, Moldenaers P, Vermant J (2010) A double wall-ring geometry for interfacial shear rheometry. Rheol Acta 49:131–144

    Article  CAS  Google Scholar 

  • Vargaftik N, Volkov B, Voljak L (1983) International tables of the surface tension of water. J Phys Chem Ref Data 12:817–820

    Article  CAS  Google Scholar 

  • Vasiljević J, Simončič B, Kert M (2015) The influence of a surfactant’s structure and the mode of its action during reactive wool dyeing. Tekstilec 58:301–313. https://doi.org/10.14502/Tekstilec2015.58.301-313

    Article  Google Scholar 

  • Wilking JN, Angelini TE, Seminara A, Brenner MP, Weitz DA (2011) Biofilms as Complex Fluids MRS Bulletin 36:385

    CAS  Google Scholar 

  • Wingender J, Neu TR, Flemming H-C (1999) What are bacterial extracellular polymeric substances?Microbial extracellular polymeric substances. Springer, pp 1–19

  • Wu C, Lim JY, Fuller GG, Cegelski L (2013) Disruption of Escherichia coli amyloid-integrated biofilm formation at the air–liquid interface by a polysorbate surfactant. Langmuir 29:920–926

    Article  CAS  Google Scholar 

  • Zhang Z, Christopher G (2016) Effect of particulate contaminants on the development of biofilms at air/water interfaces. Langmuir 32:2724–2730

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We wish to acknowledge the NSF CMMI for funding this work (#1635245). The authors would also like to thank Dr. Michael San Francisco of TTU, Dr. Kendra Rumbaugh of TTU HSC, and Dr. Vernita Gordon of UT for all their help in supplying bacteria, educating the authors in bacteria culturing technique, and a wide range of useful discussions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gordon F. Christopher.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 137 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qi, L., Christopher, G.F. Effects of non-ionic surfactant on the formation of pellicles by Pseudomonas aeruginosa. Rheol Acta 61, 59–68 (2022). https://doi.org/10.1007/s00397-021-01313-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00397-021-01313-0

Keywords

Navigation