Role of Nonadsorbing Polymers in Bacterial AggregationClick to copy article linkArticle link copied!
Abstract
Bacteria exhibit properties similar to those of nonbiological colloids and can display pairwise attractions when in close proximity. This interaction is governed by the surface chemistry of the cells. We seek to understand bacterial aggregation at the cellular level using Escherichiacoli (E. coli) AB1157. Aggregation studies were carried out using 0.5 to 2.5 wt % E. coli AB1157 harvested in different growth phases with varying concentrations of a nonadsorbing polymer, sodium polystyrene sulfonate (SPS). The electrophoretic mobility of E. coli AB1157 in different growth phases was determined using phase-amplitude light scattering. E. coli AB1157 was found to be negatively charged, and the cell surface properties changed in different growth phases. The electrokinetic results correlated well with the different concentrations of nonadsorbing polymer needed to induce depletion aggregation. This shows that a difference in aggregation properties is due to changes in the bacteria electrokinetic properties during their growth.
*
Corresponding author. E-mail: [email protected]. Tel: (+44) 01142227510. Fax: (+44) 01142227501.
Cited By
This article is cited by 53 publications.
- Binqian Yang, Feng Gao, Zhiyuan Li, Mingyang Li, Liang Chen, Yong Guan, Gang Liu, Lihua Yang. Selective Entropy Gain-Driven Adsorption of Nanospheres onto Spherical Bacteria Endows Photodynamic Treatment with Narrow-Spectrum Activity. The Journal of Physical Chemistry Letters 2020, 11
(8)
, 2788-2796. https://doi.org/10.1021/acs.jpclett.0c00287
- Felipe D. Castro, Jacqueline Sedman, Ashraf A. Ismail, Bahareh Asadishad, and Nathalie Tufenkji . Effect of Dissolved Oxygen on Two Bacterial Pathogens Examined using ATR-FTIR Spectroscopy, Microelectrophoresis, and Potentiometric Titration. Environmental Science & Technology 2010, 44
(11)
, 4136-4141. https://doi.org/10.1021/es903692u
- Elena P. Ivanova, Vi Khanh Truong, James Y. Wang, Christopher C. Berndt, Robert T. Jones, Iman I. Yusuf, Ian Peake, Heinrich W. Schmidt, Christopher Fluke, David Barnes and Russell J. Crawford . Impact of Nanoscale Roughness of Titanium Thin Film Surfaces on Bacterial Retention. Langmuir 2010, 26
(3)
, 1973-1982. https://doi.org/10.1021/la902623c
- Kevin E. Eboigbodin and Catherine A. Biggs. Characterization of the Extracellular Polymeric Substances Produced by Escherichia coli Using Infrared Spectroscopic, Proteomic, and Aggregation Studies. Biomacromolecules 2008, 9
(2)
, 686-695. https://doi.org/10.1021/bm701043c
- Nicolas Pasquier,, Helmut Keul,, Elisabeth Heine, and, Martin Moeller. From Multifunctionalized Poly(ethylene imine)s toward Antimicrobial Coatings. Biomacromolecules 2007, 8
(9)
, 2874-2882. https://doi.org/10.1021/bm070353r
- Kevin E. Eboigbodin,, Jesus J. Ojeda, and, Catherine A. Biggs. Investigating the Surface Properties of Escherichia coli under Glucose Controlled Conditions and Its Effect on Aggregation. Langmuir 2007, 23
(12)
, 6691-6697. https://doi.org/10.1021/la063404z
- Sebastian Gonzalez La Corte, Corey A. Stevens, Gerardo Cárcamo-Oyarce, Katharina Ribbeck, Ned S. Wingreen, Sujit S. Datta. Morphogenesis of bacterial cables in polymeric environments. Science Advances 2025, 11
(3)
https://doi.org/10.1126/sciadv.adq7797
- Clayton O. Jarrett, Jacqueline M. Leung, Suzuki Motoshi, Daniel E. Sturdevant, Yixiang Zhang, Forrest H. Hoyt, B. Joseph Hinnebusch, . Role of the
Yersinia pestis
phospholipase D (Ymt) in the initial aggregation step of biofilm formation in the flea. mBio 2024, 15
(6)
https://doi.org/10.1128/mbio.00124-24
- Sebastian Gonzalez La Corte, Corey A. Stevens, Gerardo Cárcamo-Oyarce, Katharina Ribbeck, Ned S. Wingreen, Sujit S. Datta. Morphogenesis of bacterial colonies in polymeric environments. 2024https://doi.org/10.1101/2024.04.18.590088
- Hong Zhang, Dongyang Kong, Wenchao Zhang, Huaqing Liu. Depletion attraction in colloidal and bacterial systems. Frontiers in Materials 2023, 10 https://doi.org/10.3389/fmats.2023.1206819
- Kinga Skrzyniarz, Javier Sanchez-Nieves, F. Javier de la Mata, Małgorzata Łysek-Gładysińska, Karolina Lach, Karol Ciepluch. Mechanistic insight of lysozyme transport through the outer bacteria membrane with dendronized silver nanoparticles for peptidoglycan degradation. International Journal of Biological Macromolecules 2023, 237 , 124239. https://doi.org/10.1016/j.ijbiomac.2023.124239
- Iztok Dogsa, Rok Kostanjšek, David Stopar. eDNA Provides a Scaffold for Autoaggregation of B. subtilis in Bacterioplankton Suspension. Microorganisms 2023, 11
(2)
, 332. https://doi.org/10.3390/microorganisms11020332
- Abdul Hakeem Anwer, Nishat Khan, Mohammad Zain Khan. Nanomaterials supporting direct electron transport. 2023, 221-240. https://doi.org/10.1016/B978-0-323-90404-9.00016-4
- Wuqi Amy Niu, Morgan N. Smith, Maria M. Santore. Depletion attractions drive bacterial capture on both non-fouling and adhesive surfaces, enhancing cell orientation. Soft Matter 2022, 18
(48)
, 9205-9215. https://doi.org/10.1039/D2SM01248K
- Xiaoling Wang, Raphael Blumenfeld, Xi-Qiao Feng, David A. Weitz. ‘Phase transitions’ in bacteria – From structural transitions in free living bacteria to phenotypic transitions in bacteria within biofilms. Physics of Life Reviews 2022, 43 , 98-138. https://doi.org/10.1016/j.plrev.2022.09.004
- Maria M. Santore. Interplay of physico-chemical and mechanical bacteria-surface interactions with transport processes controls early biofilm growth: A review. Advances in Colloid and Interface Science 2022, 304 , 102665. https://doi.org/10.1016/j.cis.2022.102665
- Samridhi Rana, Arun Kumar. Toxicity of nanoparticles to algae-bacterial co-culture: Knowns and unknowns. Algal Research 2022, 62 , 102641. https://doi.org/10.1016/j.algal.2022.102641
- Julia Isenring, Annelies Geirnaert, Christophe Lacroix, Marc J. A. Stevens. Bistable auto-aggregation phenotype in Lactiplantibacillus plantarum emerges after cultivation in in vitro colonic microbiota. BMC Microbiology 2021, 21
(1)
https://doi.org/10.1186/s12866-021-02331-x
- Narendra K. Dewangan, Nhi Tran, Jing Wang-Reed, Jacinta C. Conrad. Bacterial aggregation assisted by anionic surfactant and calcium ions. Soft Matter 2021, 17
(37)
, 8474-8482. https://doi.org/10.1039/D1SM00479D
- Wuqi Amy Niu, Sylvia L. Rivera, M. Sloan Siegrist, Maria M. Santore. Depletion forces drive reversible capture of live bacteria on non-adhesive surfaces. Soft Matter 2021, 17
(35)
, 8185-8194. https://doi.org/10.1039/D1SM00631B
- Francisco Javier Lobo-Cabrera, Alessandro Patti, Fernando Govantes, Alejandro Cuetos. Polymer-induced microcolony compaction in early biofilms: A computer simulation study. Physical Review E 2021, 103
(5)
https://doi.org/10.1103/PhysRevE.103.052407
- B. Joseph Hinnebusch, Clayton O. Jarrett, David M. Bland. Molecular and Genetic Mechanisms That Mediate Transmission of Yersinia pestis by Fleas. Biomolecules 2021, 11
(2)
, 210. https://doi.org/10.3390/biom11020210
- Helen Bridle. Nanotechnology for detection of waterborne pathogens. 2021, 293-326. https://doi.org/10.1016/B978-0-444-64319-3.00009-5
- Weigang Wang, Yuan Yan, Yuhao Zhao, Qin Shi, Yayi Wang. Characterization of stratified EPS and their role in the initial adhesion of anammox consortia. Water Research 2020, 169 , 115223. https://doi.org/10.1016/j.watres.2019.115223
- Xiaoling Wang, Xing Shen, Zhaocan Wang, Yuhao Kong. Viscoelasticity variation in a biofilm-mediated Bacillus subtilis suspension induced by adding polyethylene glycol. European Biophysics Journal 2019, 48
(7)
, 599-608. https://doi.org/10.1007/s00249-019-01385-0
- Nauman Nazeer, Marya Ahmed. Hydrophilic and salt responsive polymers promote depletion aggregation of bacteria. European Polymer Journal 2019, 119 , 148-154. https://doi.org/10.1016/j.eurpolymj.2019.07.033
- Agnieszka Chylewska, Małgorzata Ogryzek, Mariusz Makowski. Modern Approach to Medical Diagnostics - the Use of Separation Techniques in Microorganisms Detection. Current Medicinal Chemistry 2019, 26
(1)
, 121-165. https://doi.org/10.2174/0929867324666171023164813
- Thomas Trunk, Hawzeen S. Khalil, Jack C. Leo, . Bacterial autoaggregation. AIMS Microbiology 2018, 4
(1)
, 140-164. https://doi.org/10.3934/microbiol.2018.1.140
- Klemen Bohinc, Guilherme Volpe Bossa, Sylvio May. Incorporation of ion and solvent structure into mean-field modeling of the electric double layer. Advances in Colloid and Interface Science 2017, 249 , 220-233. https://doi.org/10.1016/j.cis.2017.05.001
- Zhang Zhengwen, Herbert J. Meiselman, Björn Neu. Effects of neutral polymers on the mechanics of red blood cell adhesion onto coated glass surfaces. Biorheology 2016, 52
(5-6)
, 379-389. https://doi.org/10.3233/BIR-15044
- Shafeer Kalathil, Deepak Pant. Nanotechnology to rescue bacterial bidirectional extracellular electron transfer in bioelectrochemical systems. RSC Advances 2016, 6
(36)
, 30582-30597. https://doi.org/10.1039/C6RA04734C
- Helen Bridle. Nanotechnology for Detection of Waterborne Pathogens. 2014, 291-318. https://doi.org/10.1016/B978-0-444-59543-0.00009-8
- Xiaohui Sun, Qingye Lu, Yaman Boluk, Yang Liu. The impact of cellulose nanocrystals on the aggregation and initial adhesion of Pseudomonas fluorescens bacteria. Soft Matter 2014, 10
(44)
, 8923-8931. https://doi.org/10.1039/C4SM00946K
- Xiaohui Sun, Christophe Danumah, Yang Liu, Yaman Boluk. Flocculation of bacteria by depletion interactions due to rod-shaped cellulose nanocrystals. Chemical Engineering Journal 2012, 198-199 , 476-481. https://doi.org/10.1016/j.cej.2012.05.114
- Huihui Liu, Lingyu Wang, Zhixiong Xie, Ping Shen. Involvement of DNA in biofilm formation II: From bacterial adhesion to biofilm formation. Wuhan University Journal of Natural Sciences 2012, 17
(2)
, 162-168. https://doi.org/10.1007/s11859-012-0822-7
- Jan Petr, Vítězslav Maier. Analysis of microorganisms by capillary electrophoresis. TrAC Trends in Analytical Chemistry 2012, 31 , 9-22. https://doi.org/10.1016/j.trac.2011.07.013
- Joy Mukherjee, Esther Karunakaran, Catherine A. Biggs. Using a multi-faceted approach to determine the changes in bacterial cell surface properties influenced by a biofilm lifestyle. Biofouling 2012, 28
(1)
, 1-14. https://doi.org/10.1080/08927014.2011.639067
- Guanglai Li, Pamela J. B. Brown, Jay X. Tang, Jing Xu, Ellen M. Quardokus, Clay Fuqua, Yves V. Brun. Surface contact stimulates the just‐in‐time deployment of bacterial adhesins. Molecular Microbiology 2012, 83
(1)
, 41-51. https://doi.org/10.1111/j.1365-2958.2011.07909.x
- Esther Karunakaran, Joy Mukherjee, Bharathi Ramalingam, Catherine A. Biggs. “Biofilmology”: a multidisciplinary review of the study of microbial biofilms. Applied Microbiology and Biotechnology 2011, 90
(6)
, 1869-1881. https://doi.org/10.1007/s00253-011-3293-4
- Xiuqiong Deng, Xinsheng Chai, Chaohai Wei, Limin Fu. Rapid Determination of Quinoline and 2-Hydroxyquinoline in Quinoline Biodegradation Process by Tri-Wavelength UV/Vis Spectroscopy. Analytical Sciences 2011, 27
(5)
, 493-497. https://doi.org/10.2116/analsci.27.493
- Joy Mukherjee, Saw Yen Ow, Josselin Noirel, Catherine A. Biggs. Quantitative protein expression and cell surface characteristics of
Escherichia coli
MG1655 biofilms. PROTEOMICS 2011, 11
(3)
, 339-351. https://doi.org/10.1002/pmic.201000386
- Siddhartha Das, Suman Chakraborty. Transport of Flexible Molecules in Narrow Confinements. International Journal of Micro-Nano Scale Transport 2010, 1
(2)
, 97-137. https://doi.org/10.1260/1759-3093.1.2.97
- J. Schwarz-Linek, G. Dorken, A. Winkler, L. G. Wilson, N. T. Pham, C. E. French, T. Schilling, W. C. K. Poon. Polymer-induced phase separation in suspensions of bacteria. EPL (Europhysics Letters) 2010, 89
(6)
, 68003. https://doi.org/10.1209/0295-5075/89/68003
- Tim Schinner, Adrian Letzner, Stefan Liedtke, Felipe D. Castro, Irwin A. Eydelnant, Nathalie Tufenkji. Transport of selected bacterial pathogens in agricultural soil and quartz sand. Water Research 2010, 44
(4)
, 1182-1192. https://doi.org/10.1016/j.watres.2008.11.038
- Vi Khanh Truong, James Wang, Rimma Lapovok, Yuri Estrin, Francois Malherbe, Christopher Berndt, Russell Crawford, Elena Ivanova. Bacterial Attachment Response on Titanium Surfaces with Nanometric Topographic Features. 2010, 41-45. https://doi.org/10.1007/978-3-642-13461-6_9
- Jana Schwarz-Linek, Alexander Winkler, Laurence G. Wilson, Nhan T. Pham, Tanja Schilling, Wilson C. K. Poon. Polymer-induced phase separation in Escherichia coli suspensions. Soft Matter 2010, 6
(18)
, 4540. https://doi.org/10.1039/c0sm00214c
- Stefan Theiler, Thomas Hövetborn, Helmut Keul, Martin Möller. Synthesis and Characterization of Amphiphilic Polyethers Based on Tetrahydrofuran and Glycidol: Antibacterial Assessment. Macromolecular Chemistry and Physics 2009, 210
(8)
, 614-630. https://doi.org/10.1002/macp.200800502
- Yanwei Wang, Flemming Y. Hansen, Günther H. Peters, Ole Hassager. Proof of the identity between the depletion layer thickness and half the average span for an arbitrary polymer chain. The Journal of Chemical Physics 2008, 129
(7)
https://doi.org/10.1063/1.2970935
- Hui-Hui Liu, Yi-Ran Yang, Xin-Cheng Shen, Zhi-Ling Zhang, Ping Shen, Zhi-Xiong Xie. Role of DNA in Bacterial Aggregation. Current Microbiology 2008, 57
(2)
, 139-144. https://doi.org/10.1007/s00284-008-9166-0
- Muhammad Nazmul Karim, Hugh Graham, Binbing Han, Algird Cibulskas. Flocculation enhanced microfiltration of Escherichia coli lysate. Biochemical Engineering Journal 2008, 40
(3)
, 512-519. https://doi.org/10.1016/j.bej.2008.02.006
- Anushree Malik, Kazuo Kakii. Novel coaggregating microbial consortium: Testing strength for field applications. Bioresource Technology 2008, 99
(11)
, 4627-4634. https://doi.org/10.1016/j.biortech.2007.06.062
- Natasa Mitik‐Dineva, James Wang, Radu C. Mocanasu, Paul R. Stoddart, Russell J. Crawford, Elena P. Ivanova. Impact of nano‐topography on bacterial attachment. Biotechnology Journal 2008, 3
(4)
, 536-544. https://doi.org/10.1002/biot.200700244
- Mark Geoghegan, Johanna S. Andrews, Catherine A. Biggs, Kevin E. Eboigbodin, David R. Elliott, Stephen Rolfe, Julie Scholes, Jesús J. Ojeda, Maria E. Romero-González, Robert G. J. Edyvean, Linda Swanson, Ramune Rutkaite, Rasika Fernando, Yu Pen, Zhenyu Zhang, Steven A. Banwart. The polymer physics and chemistry of microbial cell attachment and adhesion. Faraday Discussions 2008, 139 , 85. https://doi.org/10.1039/b717046g
- K. E. Eboigbodin, J. R. A. Newton, A. F. Routh, C. A. Biggs. Bacterial quorum sensing and cell surface electrokinetic properties. Applied Microbiology and Biotechnology 2006, 73
(3)
, 669-675. https://doi.org/10.1007/s00253-006-0505-4
Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.
Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.
The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.