journal article·2023-07-01Open access

An Evaluation of the Usability of Argon Plasma-Treated Bacterial Cellulose as a Carrier for Controlled Releases of Glycoside Hydrolases PelAh and PslGh, Which Are Able to Eradicate Biofilm

Magdalena Charęza, Ewa Ekiert, Dariusz Moszyński, Mariusz Madej, Magdalena Jędrzejczak-Silicka, Radosław Drozd

Applied Sciences· Volume 13· Issue 13

Abstract

Bacterial cellulose is a unique biopolymer that has found numerous biomedical applications, such as being an excellent wound-dressing material or a carrier for delivering active compounds. The purpose of this study was to analyze the ability of modified bacterial cellulose (BC) using low-pressure Ar plasma to control the release of glycoside hydrolases with antibiofilm activity, namely PelAh and PslGh, from Pseudomonas aeruginosa. The chemical composition and morphology of the BC surfaces were characterized using photoelectron spectroscopy (XPS), Fourier transform infrared spectroscopy (FTIR), and scanning electron microscopy (SEM). The analyses revealed significant changes in the chemical composition of the BC surface due to the introduction of charged functional groups and the conversion of its well-ordered structure into a more amorphous form. The release profiles of enzymes from both forms of the carrier were different and depended on their structural properties. However, a significant impact of BC modification on protein release behavior from the carrier was observed only for PslGh. Both enzymes, when immobilized on pristine and argon plasma-modified BC, retained their ability to effectively reduce biofilm levels, similarly to their soluble form. Ar plasma-modified BC with immobilized specific hydrolases can be used as an effective tool for inhibiting P. aeruginosa biofilm development.
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Research context

OpenAlex topics: Advanced Cellulose Research Studies · Enzyme Production and Characterization · Polysaccharides and Plant Cell Walls

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Microbiology and Biotechnology, Faculty of Biotechnology and Animal Husbandry, West Pomeranian University of Technology in Szczecin, 45 Piastow Avenue, 71-311 Szczecin, Poland

Department of Inorganic Chemical Technology and Environment Engineering, Faculty of Chemical Technology and Engineering, West Pomeranian University of Technology in Szczecin, 42 Piastow Avenue, 71-065 Szczecin, Poland

Department of Microbiology, Faculty of Biochemistry, Biophysics, and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Kraków, Poland

Laboratory of Cytogenetics, West Pomeranian University of Technology in Szczecin, Klemensa Janickiego 29, 71-270 Szczecin, Poland

References (57)

Show source-provided references
1. Preparation of biocompatible wound dressings with long-term antimicrobial activity through covalent bonding of antibiotic agents to natural polymers10.1016/j.ijbiomac.2018.09.122 ↗
2. Application of conducting polymers to wound care and skin tissue engineering: A review10.1016/j.bios.2019.04.001 ↗
3. Vivcharenko, V., and Przekora, A. (2021). Modifications of Wound Dressings with Bioactive Agents to Achieve Improved Pro-Healing Properties. Appl. Sci., 11.10.3390/app11094114 ↗
4. Bacterial cellulose as a material for wound treatment: Properties and modifications. A review10.1016/j.biotechadv.2015.07.009 ↗
5. Improving bacterial cellulose films by ex-situ and in-situ modifications: A review10.1016/j.foodhyd.2020.106514 ↗
6. Plasma-modified biomaterials for self-antimicrobial applications10.1021/am2003944 ↗
7. In situ and ex situ modifications of bacterial cellulose for applications in tissue engineering10.1016/j.msec.2016.11.121 ↗
8. Silicone polyether surfactant enhances bacterial cellulose synthesis and water holding capacity10.1016/j.ijbiomac.2022.03.124 ↗
9. Biofilm grown on wood waste pretreated with cold low-pressure nitrogen plasma: Utilization for toluene remediation10.1016/j.ibiod.2019.03.003 ↗
10. Surface modification of bacterial cellulose by nitrogen-containing plasma for improved interaction with cells10.1016/j.carbpol.2010.05.037 ↗
11. Argon plasma-modified bacterial cellulose filters for protection against respiratory pathogens10.1016/j.carbpol.2022.120322 ↗
12. Surface modification of bacterial cellulose membrane by oxygen plasma treatment10.1016/j.surfcoat.2016.06.035 ↗
13. Atmospheric pressure plasmas: Infection control and bacterial responses10.1016/j.ijantimicag.2014.01.025 ↗
14. Effects of plasma treatments on the controlled drug release from poly(ethylene-co-vinyl acetate)10.1016/j.surfcoat.2012.11.064 ↗
15. Regulating the antibiotic drug release from β-tricalcium phosphate ceramics by atmospheric plasma surface engineering10.1039/C6BM00411C ↗
16. Challenges and solutions in polymer drug delivery for bacterial biofilm treatment: A tissue-by-tissue account10.1016/j.addr.2021.113973 ↗
17. Chronic wound infections: The role of Pseudomonas aeruginosa and Staphylococcus aureus10.1586/14787210.2015.1023291 ↗
18. The evolution of virulence in Pseudomonas aeruginosa during chronic wound infection
19. Confocal Laser Scanning Microscopy for Analysis of Pseudomonas aeruginosa Biofilm Architecture and Matrix Localization10.3389/fmicb.2019.00677 ↗
20. Updates on the pathogenicity status of Pseudomonas aeruginosa10.1016/j.drudis.2018.07.003 ↗
21. Pathogenic factors of Pseudomonas aeruginosa—The role of biofilm in pathogenicity and as a target for phage therapy10.5604/01.3001.0010.3792 ↗
22. The Pseudomonas aeruginosa lectin LecB binds to the exopolysaccharide Psl and stabilizes the biofilm matrix10.1038/s41467-019-10201-4 ↗
23. Characterization of the Pseudomonas aeruginosa Glycoside Hydrolase PslG Reveals That Its Levels Are Critical for Psl Polysaccharide Biosynthesis and Biofilm Formation10.1074/jbc.M115.674929 ↗
24. Genetic regulation, biosynthesis and applications of extracellular polysaccharides of the biofilm matrix of bacteria10.1016/j.carbpol.2022.119536 ↗
25. The Pel polysaccharide is predominantly composed of a dimeric repeat of α-1,4 linked galactosamine and N-acetylgalactosamine10.1038/s42003-022-03453-2 ↗
26. Glycoside hydrolase (PelAh) immobilization prevents Pseudomonas aeruginosa biofilm formation on cellulose-based wound dressing10.1016/j.carbpol.2020.116625 ↗
27. Exopolysaccharide biosynthetic glycoside hydrolases can be utilized to disrupt and prevent Pseudomonas aeruginosa biofilms10.1126/sciadv.1501632 ↗
28. Treatment with the Pseudomonas aeruginosa Glycoside Hydrolase PslG Combats Wound Infection by Improving Antibiotic Efficacy and Host Innate Immune Activity10.1128/AAC.00234-19 ↗
29. Microbial glycoside hydrolases as antibiofilm agents with cross-kingdom activity10.1073/pnas.1702798114 ↗
30. Preventing Pseudomonas aeruginosa Biofilms on Indwelling Catheters by Surface-Bound Enzymes10.1021/acsabm.1c00794 ↗
31. Non-eluting, surface-bound enzymes disrupt surface attachment of bacteria by continuous biofilm polysaccharide degradation10.1016/j.biomaterials.2018.03.016 ↗
32. Charęza, M., Przygrodzka, K., Żywicka, A., Grygorcewicz, B., Sobolewski, P., Mozia, S., Śmiglak, M., and Drozd, R. (2023). Enhancement of Inhibition of the Pseudomonas sp. Biofilm Formation on Bacterial Cellulose-Based Wound Dressing by the Combined Action of Alginate Lyase and Gentamicin. Int. J. Mol. Sci., 24.10.3390/ijms24054740 ↗
33. Beamson, G., and Briggs, D. (1992). High Resolution XPS of Organic Polymers: The Scienta ESCA300 Database, Wiley.
34. Przygrodzka, K., Charęza, M., Banaszek, A., Zielińska, B., Ekiert, E., and Drozd, R. (2022). Bacterial Cellulose Production by Komagateibacter xylinus with the Use of Enzyme-Degraded Oligo- and Polysaccharides as the Substrates. Appl. Sci., 12.10.3390/app122412673 ↗
35. Jedrzejczak-Silicka, M., Kordas, M., Konopacki, M., and Rakoczy, R. (2021). Modulation of Cellular Response to Different Parameters of the Rotating Magnetic Field (RMF)-An In Vitro Wound Healing Study. Int. J. Mol. Sci., 22.10.3390/ijms22115785 ↗
36. Biocompatible alginate silica supported silver nanoparticles composite films for wound dressing with antibiofilm activity10.1016/j.msec.2020.110863 ↗
37. Exposure to non-continuous rotating magnetic field induces metabolic strain-specific response of Komagataeibacter xylinus10.1016/j.bej.2020.107855 ↗
38. Studies on bacterial cellulose produced by a novel strain of Lactobacillus genus10.1016/j.carbpol.2019.115513 ↗
39. Characterization of compressed bacterial cellulose nanopaper film after exposure to dry and humid conditions10.1016/j.jmrt.2021.01.057 ↗
40. Effect of media components on cell growth and bacterial cellulose production from Acetobacter aceti MTCC 262310.1016/j.carbpol.2013.01.018 ↗
41. Bacterial Cellulose Production by Komagataeibacter xylinus Using Rice-washed Water and Tofu Processing Wastewater with the Addition of Sodium Glutamate10.1007/s12221-022-4729-4 ↗
42. The study of the coating adhesion on PP surface modified in different plasma/acrylic acid solution10.1016/j.ijadhadh.2012.09.008 ↗
43. Mechanisms of oxygen- and argon-RF-plasma-induced surface chemistry of cellulose10.1007/BF02766154 ↗
44. Characterization of Cellulose Nanocrystals Produced by Acid-Hydrolysis from Sugarcane Bagasse as Agro-Waste10.12691/jmpc-2-1-1 ↗
45. Bacterial cellulose membrane used as biological dressings on third-degree burns in rats
46. Ion-Induced Nanopatterning of Bacterial Cellulose Hydrogels for Biosensing and Anti-Biofouling Interfaces10.1021/acsanm.0c01151 ↗
47. Novel Effects of Surface Modification on Activated Carbon Fibers Using a Low Pressure Plasma Treatment10.1021/jp065907j ↗
48. Vasil’kov, A., Budnikov, A., Gromovykh, T., Pigaleva, M., Sadykova, V., Arkharova, N., and Naumkin, A. (2022). Effect of Bacterial Cellulose Plasma Treatment on the Biological Activity of Ag Nanoparticles Deposited Using Magnetron Deposition. Polymers, 14.10.3390/polym14183907 ↗
49. A new surface for immobilizing and maintaining the function of enzymes in a freeze-dried state10.1021/bm900523m ↗
50. How sugars protect proteins in the solid state and during drying (review): Mechanisms of stabilization in relation to stress conditions10.1016/j.ejpb.2017.01.024 ↗
51. Theory and applications of differential scanning fluorimetry in early-stage drug discovery10.1007/s12551-020-00619-2 ↗
52. UCSF Chimera—A visualization system for exploratory research and analysis10.1002/jcc.20084 ↗
53. PROPKA3: Consistent Treatment of Internal and Surface Residues in Empirical pKa Predictions10.1021/ct100578z ↗
54. Ex-situ modification of bacterial cellulose for immediate and sustained drug release with insights into release mechanism10.1016/j.carbpol.2020.116816 ↗
55. Comparison of drug release behavior of bacterial cellulose loaded with ibuprofen and propranolol hydrochloride10.1039/D1RA07761A ↗
56. The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix10.1111/j.1462-2920.2011.02657.x ↗
57. Thi, M.T.T., Wibowo, D., and Rehm, B.H.A. (2020). Pseudomonas aeruginosa Biofilms. Int. J. Mol. Sci., 21.10.3390/ijms21228671 ↗