Effect of ZnO Nanoparticles on Biofilm Formation and Gene Expression of the Toxin-antitoxin System in Clinical Isolates of Pseudomonas Aeruginosa

Overview

Journal Ann Clin Microbiol Antimicrob

Publisher Biomed Central

Specialties Infectious Diseases
Microbiology

Date 2023 Oct 5

PMID 37798613

Authors

Hassan Valadbeigi

Nourkhoda Sadeghifard

Vahab Hassan Kaviar

Mohammad Hossein Haddadi

Sobhan Ghafourian

Abbas Maleki

Affiliations

Soon will be listed here.

Abstract

Background: Biofilm formation by Pseudomonas aeruginosa (P. aeruginosa) is known to be characteristic of this organism. This bacterium is considered one of the most life-threatening bacteria and has been identified as a priority pathogen for research by WHO. Biofilm-producing P. aeruginosa is a concern in many parts of the world due to antibiotic resistance. Alginate also plays an important role in the biofilm formation of P. aeruginosa as well as the emergence of antibiotic resistance in biofilms. In addition, the systems of toxin-antitoxin( TA) play an important role in biofilm formation. Metal nanoparticle(NP) such as zinc oxide (ZnO) also have extensive biological properties, especially anti-biofilm properties. Therefore, this study was conducted in relation to the importance of zinc oxide nanoparticles (ZnO NPs) in biofilm formation and also the correlation of gene expression of TA systems in clinical isolates of P. aeruginosa.

Methods: A total of 52 P. aeruginosa isolates were collected from burns (n = 15), UTI (n = 31), and trachea (n = 6) in hospitals in Ilam between May 2020 and October 2020. Biofilm formation was assessed using a microtiter plate assay. MIC and sub-MIC concentrations of ZnO NPs (10-30 nm with purity greater than 99.8%) in P. aeruginosa were determined. Subsequently, biofilm formation was investigated using sub-MIC concentrations of ZnO NPs. Finally, total RNA was extracted and RT- qPCR was used to determine the expression levels of genes of mazEF, mqsRA, and higBA of TA systems.

Results: Six isolates of P. aeruginosa were found to form strong biofilms. The results showed that ZnO NPs were able to inhibit biofilm formation. In our experiments, we found that the sub-MIC concentration of ZnO NPs increased the gene expression of antitoxins mazE and mqsA and toxin higB of TA systems treated with ZnO NPs.

Conclusions: In the present study, ZnO NPs were shown to effectively inhibit biofilm formation in P. aeruginosa. Our results support the relationship between TA systems and ZnO NPs in biofilm formation in P. aeruginosa. Importantly, the expression of antitoxins mazE and mqsA was high after treatment with ZnO NPs, but not that of antitoxin higA.

Citing Articles

Harnessing for Zinc Oxide Nanoparticle Green Synthesis: A Sustainable Solution to Combat Multidrug-Resistant Bacterial Pathogens.

Elabbasy M, El Bayomi R, Abdelkarim E, Hafez A, Othman M, Ghoniem M Nanomaterials (Basel). 2025; 15(5).

PMID: 40072171 PMC: 11901501. DOI: 10.3390/nano15050369.

Eco-friendly zinc oxide nanoparticle biosynthesis powered by probiotic bacteria.

Al-Tameemi A, Masarudin M, Rahim R, Mizzi R, Timms V, Isa N Appl Microbiol Biotechnol. 2025; 109(1):32.

PMID: 39878901 PMC: 11779794. DOI: 10.1007/s00253-024-13355-4.

Synthesis and characterization of hydroxyapatite-zinc oxide nanocomposites incorporating rosemary and thyme essential oils for enhanced bone regeneration and antimicrobial activity.

Burdusel A, Sarchizian D, Niculescu A, Holban A, Popescu R, Trusca R Rom J Morphol Embryol. 2024; 65(3):409-419.

PMID: 39529334 PMC: 11657322. DOI: 10.47162/RJME.65.3.03.

Low-dose zinc oxide nanoparticles trigger the growth and biofilm formation of Pseudomonas aeruginosa: a hormetic response.

Al-Momani H, Aolymat I, Ibrahim L, Albalawi H, Al Balawi D, Albiss B BMC Microbiol. 2024; 24(1):290.

PMID: 39095741 PMC: 11297655. DOI: 10.1186/s12866-024-03441-y.

References

Chang C . Surface Sensing for Biofilm Formation in . Front Microbiol. 2018; 8:2671. PMC: 5767216. DOI: 10.3389/fmicb.2017.02671. View

Tuon F, Dantas L, Suss P, Ribeiro V . Pathogenesis of the Biofilm: A Review. Pathogens. 2022; 11(3). PMC: 8950561. DOI: 10.3390/pathogens11030300. View

Moreau-Marquis S, Stanton B, OToole G . Pseudomonas aeruginosa biofilm formation in the cystic fibrosis airway. Pulm Pharmacol Ther. 2008; 21(4):595-9. PMC: 2542406. DOI: 10.1016/j.pupt.2007.12.001. View

Thi M, Wibowo D, Rehm B . Biofilms. Int J Mol Sci. 2020; 21(22). PMC: 7698413. DOI: 10.3390/ijms21228671. View

Bhattacharyya P, Agarwal B, Goswami M, Maiti D, Baruah S, Tribedi P . Zinc oxide nanoparticle inhibits the biofilm formation of Streptococcus pneumoniae. Antonie Van Leeuwenhoek. 2017; 111(1):89-99. DOI: 10.1007/s10482-017-0930-7. View

Lee J, Kim Y, Cho M, Lee J . ZnO nanoparticles inhibit Pseudomonas aeruginosa biofilm formation and virulence factor production. Microbiol Res. 2014; 169(12):888-96. DOI: 10.1016/j.micres.2014.05.005. View

Jothiprakasam V, Sambantham M, Chinnathambi S, Vijayaboopathi S . Candida tropicalis biofilm inhibition by ZnO nanoparticles and EDTA. Arch Oral Biol. 2016; 73:21-24. DOI: 10.1016/j.archoralbio.2016.09.003. View

Campoccia D, Montanaro L, Arciola C . A review of the biomaterials technologies for infection-resistant surfaces. Biomaterials. 2013; 34(34):8533-54. DOI: 10.1016/j.biomaterials.2013.07.089. View

Mirzahosseini H, Hadadi-Fishani M, Morshedi K, Khaledi A . Meta-Analysis of Biofilm Formation, Antibiotic Resistance Pattern, and Biofilm-Related Genes in Isolated from Clinical Samples. Microb Drug Resist. 2020; 26(7):815-824. DOI: 10.1089/mdr.2019.0274. View

10.

Wen Y, Behiels E, Devreese B . Toxin-Antitoxin systems: their role in persistence, biofilm formation, and pathogenicity. Pathog Dis. 2014; 70(3):240-9. DOI: 10.1111/2049-632X.12145. View

11.

Yamaguchi Y, Park J, Inouye M . Toxin-antitoxin systems in bacteria and archaea. Annu Rev Genet. 2011; 45:61-79. DOI: 10.1146/annurev-genet-110410-132412. View

12.

Wood T, Wood T . The HigB/HigA toxin/antitoxin system of Pseudomonas aeruginosa influences the virulence factors pyochelin, pyocyanin, and biofilm formation. Microbiologyopen. 2016; 5(3):499-511. PMC: 4906001. DOI: 10.1002/mbo3.346. View

13.

Sun C, Guo Y, Tang K, Wen Z, Li B, Zeng Z . MqsR/MqsA Toxin/Antitoxin System Regulates Persistence and Biofilm Formation in KT2440. Front Microbiol. 2017; 8:840. PMC: 5422877. DOI: 10.3389/fmicb.2017.00840. View

14.

Say Coskun U, Cicek A, Kilinc C, Guckan R, Dagcioglu Y, Demir O . Effect of mazEF, higBA and relBE toxin-antitoxin systems on antibiotic resistance in Pseudomonas aeruginosa and Staphylococcus isolates. Malawi Med J. 2019; 30(2):67-72. PMC: 6307074. DOI: 10.4314/mmj.v30i2.3. View

15.

Ali S, Ansari M, Alzohairy M, Alomary M, Alyahya S, Jalal M . Biogenic Gold Nanoparticles as Potent Antibacterial and Antibiofilm Nano-Antibiotics against . Antibiotics (Basel). 2020; 9(3). PMC: 7148532. DOI: 10.3390/antibiotics9030100. View

16.

Golpayegani A, Nabizadeh Nodehi R, Rezaei F, Alimohammadi M, Douraghi M . Real-time polymerase chain reaction assays for rapid detection and virulence evaluation of the environmental Pseudomonas aeruginosa isolates. Mol Biol Rep. 2019; 46(4):4049-4061. DOI: 10.1007/s11033-019-04855-y. View

17.

Wei Q, Ma L . Biofilm matrix and its regulation in Pseudomonas aeruginosa. Int J Mol Sci. 2013; 14(10):20983-1005. PMC: 3821654. DOI: 10.3390/ijms141020983. View

18.

Poynton H, Lazorchak J, Impellitteri C, Smith M, Rogers K, Patra M . Differential gene expression in Daphnia magna suggests distinct modes of action and bioavailability for ZnO nanoparticles and Zn ions. Environ Sci Technol. 2010; 45(2):762-8. DOI: 10.1021/es102501z. View

19.

Brayner R, Ferrari-Iliou R, Brivois N, Djediat S, Benedetti M, Fievet F . Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal medium. Nano Lett. 2006; 6(4):866-70. DOI: 10.1021/nl052326h. View

20.

Jones N, Ray B, Ranjit K, Manna A . Antibacterial activity of ZnO nanoparticle suspensions on a broad spectrum of microorganisms. FEMS Microbiol Lett. 2007; 279(1):71-6. DOI: 10.1111/j.1574-6968.2007.01012.x. View