FliA-Dependent Surface Macromolecules Promote Initial Biofilm Development of Escherichia coli by Influencing the Bacterial Surface Properties

Year 2023, Volume: 10 Issue: 1, 83 - 90, 31.03.2023

Fatma Pınar Gördesli Duatepe

https://doi.org/10.17350/HJSE19030000295

Cited By: 1

Abstract

FliA is an important regulatory component for the synthesis of surface macromolecules which are involved in motility and biofilm development of Escherichia coli. In this study, the roles of FliA-dependent surface macromolecules in E. coli surface tension, surface heterogeneity and surface roughness, and initial biofilm development consisting of reversible and irreversible adhesion were investigated using E. coli MG1655 wild-type strain and fliA gene deleted mutant strain. Negative Gibbs free energy change values calculated using bacterial surface tensions obtained by a spectrophotometric method showed that both wild-type and mutant cells in water can reversibly adhere to the surface of the model solid, silicon nitride (Si3N4). The calculations further showed that bacterial reversible auto-adhesion and co-adhesion were also thermodynamically favorable. In comparison, the reversible adhesion and auto-adhesion capacities of wild-type cells were higher than the mutant cells. Direct measurements by atomic force microscopy (AFM) and thorough analysis of the recorded adhesion data showed that the irreversible adhesion strength of wild-type cells to Si3N4 in water was at least 2.0-fold greater than that of the mutants due to significantly higher surface heterogeneity resulting in higher surface roughness for the wild-type cells compared to those obtained for the mutants. These results suggest that strategies aimed at preventing E. coli biofilm development should also consider a combined method, such as modifying the surface of interest with a bacterial repellent layer and targeting the FliA and FliA-dependent surface macromolecules to reduce both reversible and irreversible bacterial adhesion and hence the initial biofilm development of E. coli.

Keywords

FliA, E. coli biofilm, Gibbs free energy change, surface heterogeneity, surface roughness, adhesion energy, atomic force microscopy

Thanks

The author would like to thank to Dr. Colin Grant, former HITACHI SPM Product Manager (Europe), for his technical support on the AFM measurements.

References

• Bridier A, Briandet R, Thomas V, Dubois-Brissonnet F. Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27 (2011) 1017-1032.
• Davies D. Understanding biofilm resistance to antibacterial agents. Nature Reviews Drug Discovery 2 (2003) 114–122.
• Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clinical Microbiology Reviews 15 (2002) 167-193.
• Sharma G, Sharma S, Sharma P, Chandola D, Dang S, Gupta S, Gabrani R. Escherichia coli biofilm: development and therapeutic strategies. Journal of Applied Microbiology 121 (2016) 309-319.
• Devanga Ragupathi NK, Veeraraghavan B, Karunakaran E, Monk PN. Editorial: Biofilm-mediated nosocomial infections and its association with antimicrobial resistance: detection, prevention, and management. Frontiers in Medicine (Lausanne) 9 (2022) 987011.
• Aslam B, Wang W, Arshad MI, Khurshid M, Muzammil S, Rasool MH, Nisar MA, Alvi RF, Aslam MA, Qamar MU, Salamat MKF, Baloch Z. Antibiotic resistance: a rundown of a global crisis. Infection and Drug Resistance 11 (2018) 1645-1658.
• Wingender J, Flemming HC. Biofilms in drinking water and their role as reservoir for pathogens. International Journal of Hygiene and Environmental Health 214 (2011) 417-423.
• Galié S, García-Gutiérrez C, Miguélez EM, Villar CJ, Lombó F. Biofilms in the food industry: health aspects and control methods. Frontiers in Microbiology 9 (2018) 898.
• Reisner A, Maierl M, Jörger M, Krause R, Berger D, Haid A, Tesic D, Zechner EL. Type 1 fimbriae contribute to catheter-associated urinary tract infections caused by Escherichia coli. Journal of Bacteriology 196 (2014) 931-939.
• Ballén V, Cepas V, Ratia C, Gabasa Y, Soto SM. Clinical Escherichia coli: from biofilm formation to new antibiofilm strategies. Microorganisms 10 (2022) 1103.
• Beloin C, Roux A, Ghigo JM. Escherichia coli biofilms. Current Topics in Microbiology and Immunology 322 (2008) 249-289.
• Buck LD, Paladino MM, Nagashima K, Brezel ER, Holtzman JS, Urso SJ, Ryno LM. Temperature-dependent influence of FliA overexpression on PHL628 E. coli biofilm growth and composition. Frontiers in Cellular and Infection Microbiology 11 (2021) 775270.
• Friedlander RS, Vogel N, Aizenberg J. Role of flagella in adhesion of Escherichia coli to abiotic surfaces. Langmuir 31 (2015) 6137-44.
• Gordesli FP, Abu-Lail NI. Combined Poisson and soft-particle DLVO analysis of the specific and nonspecific adhesion forces measured between L. monocytogenes grown at various temperatures and silicon nitride. Environmental Science & Technology 46 (2012) 10089-98.
• Israelachvili JN. Intermolecular and Surface Forces, third ed. Academic Press, New York, 2011.
• Claret L, Miquel S, Vieille N, Ryjenkov DA, Gomelsky M, Darfeuille-Michaud A. The flagellar sigma factor FliA regulates adhesion and invasion of Crohn disease-associated Escherichia coli via a cyclic dimeric GMP-dependent pathway. The Journal of Biological Chemistry 282 (2007) 33275-33283.
• Fitzgerald DM, Bonocora RP, Wade JT. Comprehensive mapping of the Escherichia coli flagellar regulatory network. PLoS Genetics 10 (2014) e1004649.
• Pesavento C, Becker G, Sommerfeldt N, Possling A, Tschowri N, Mehlis A, Hengge R. Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. Genes & Development 22 (2008) 2434-46.
• Wood TK, Barrios AFG, Herzberg M, Lee J. Motility influences biofilm architecture in Escherichia coli. Applied Microbiology and Biotechnology 72 (2006) 361-367.
• Zhang X, Jiang Z, Li M, Zhang X, Wang G, Chou A, Chen L, Yan H, Zuo YY. Rapid spectrophotometric method for determining surface free energy of microalgal cells. Analytical Chemistry 86 (2014) 8751-8756.
• Zhang X, Zhang Q, Yan T, Jiang Z, Zhang X, Zuo YY. Surface free energy activated high-throughput cell sorting. Analytical Chemistry 86 (2014) 9350-9355.
• Zhang X, Zhang Q, Yan T, Jiang Z, Zhang X, Zuo YY. Quantitatively predicting bacterial adhesion using surface free energy determined with a spectrophotometric method. Environmental Science & Technology 49 (2015) 6164-6171.
• Absolom DR, Lamberti FV, Policova Z, Zingg W, van Oss CJ, Neumann AW. Surface thermodynamics of bacterial adhesion. Applied Environmental Microbiology 46 (1983) 90-97.
• Bos R, van der Mei HC, Busscher HJ. Physico-chemistry of initial microbial adhesive interactions-its mechanisms and methods for study. FEMS Microbiology Reviews 23 (1999) 179–230.
• Carniello V, Peterson BW, van der Mei HC, Busscher HJ. Physico-chemistry from initial bacterial adhesion to surface-programmed biofilm growth. Advances in Colloid and Interface Science 261 (2018) 1-14.
• Park BJ, Abu-Lail NI. The role of the pH conditions of growth on the bioadhesion of individual and lawns of pathogenic Listeria monocytogenes cells. Journal of Colloid and Interface Science 358 (2011) 611-620.
• Kwok DY, Neumann AW. Contact angle measurement and contact angle interpretation. Advances in Colloid and Interface Science 81 (1999) 167−249.
• Abu-Lail NI, Camesano TA. Role of lipopolysaccharides in the adhesion, retention, and transport of Escherichia coli JM109. Environmental Science & Technology 37 (2003) 2173-2183.
• Borer B, Tecon R, Or D. Spatial organization of bacterial populations in response to oxygen and carbon counter-gradients in pore networks. Nature Communications 9 (2018) 769.
• Du X, Lee SS, Blugan G, Ferguson SJ. Silicon nitride as a biomedical material: an overview. International Journal of Molecular Sciences 23 (2022) 6551.
• Ordek A, Gordesli-Duatepe FP. Impact of sodium nitroprusside concentration added to batch cultures of Escherichia coli biofilms on the c-di-GMP levels, morphologies and adhesion of biofilm-dispersed cells. Biofouling 38 (2022) 796–813.
• Moradali MF, Rehm BHA. Bacterial biopolymers: from pathogenesis to advanced materials. Nature Reviews Microbiology 18 (2020) 195–210.
• Park BJ, Abu-Lail NI. Atomic force microscopy investigations of heterogeneities in the adhesion energies measured between pathogenic and non-pathogenic Listeria species and silicon nitride as they correlate to virulence and adherence. Biofouling 27 (2011) 543-559.
• Laskowski D, Strzelecki J, Pawlak K, Dahm H, Balter A. Short communication effect of ampicillin on adhesive properties of bacteria examined by atomic force microscopy. Micron 112 (2018) 84–90.
• Sharma PK, Rao KH. Analysis of different approaches for evaluation of surface energy of microbial cells by contact angle goniometry. Advances in Colloid and Interface Science 98 (2002) 341-463.
• Shao W, Liu H, Liu X, Wang S, Zhang R. Anti-bacterial performances and biocompatibility of bacterial cellulose/graphene oxide composites. RSC Advances 5 (2015) 4795-4803.
• Uzoechi SC, Abu-Lail NI. The effects of β-lactam antibiotics on surface modifications of multidrug-resistant Escherichia coli: a multiscale approach. Microscopy and Microanalysis 25 (2019) 135- 150.
• Vu B, Chen M, Crawford RJ, Ivanova EP. Bacterial extracellular polysaccharides involved in biofilm formation. Molecules 14 (2009) 2535–2554.