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Evaluation of the inhibitory effects of TiO2 nanoparticle and Ganoderma lucidum extract against biofilm-producing bacteria isolated from clinical samples

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Abstract

The emergence of multidrug-resistant pathogens leads to treatment failure. So, the need for new antibacterial drugs is urgent. We evaluated the antibacterial and antibiofilm effects of titanium dioxide (TiO2) nanoparticles (NPs) and Ganoderma extract against biofilm-producing Pseudomonas aeruginosa and methicillin-resistant Staphylococcus aureus (MRSA) by microbroth dilution and crystal violet assays. The combined effect of these compounds was studied using the checkerboard method. The OD260 was measured to assess the destruction of the membrane permeability. The expression of biofilm-related genes (iacA and algD) was investigated by real-time PCR. MRSA isolate was more susceptible to test compounds. The OD260 increased and algD gene was down-regulated after treatment with TiO2 NPs and a combination of TiO2 NPs and Ganoderma extract. iacA gene did not affect by test compounds. Overall, these findings revealed that nanoparticles and natural substances might represent the potential candidates to develop promising antibacterial agents, especially against Gram-positive bacteria.

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All data generated or analyzed during this study are available from the corresponding author upon request.

References

  • Ahmed FY, Aly UF, Abd RM, El-Baky, and Nancy GFM Waly. (2020) Comparative study of antibacterial effects of titanium dioxide nanoparticles alone and in combination with antibiotics on MDR pseudomonas aeruginosa strains. Int J Nanomed 15:3393

    Article  CAS  Google Scholar 

  • Alavi M, Karimi N (2019) Biosynthesis of Ag and Cu NPs by secondary metabolites of usnic acid and thymol with biological macromolecules aggregation and antibacterial activities against multi drug resistant (MDR) bacteria. Int J Biol Macromol 128:893–901

    Article  CAS  PubMed  Google Scholar 

  • Alizadeh-Sani M, Hamishehkar H, Khezerlou A, Maleki M, Azizi-Lalabadi M, Bagheri V, Safaei P, Azimi T, Hashemi M, Ehsani A (2020) Kinetics analysis and susceptibility coefficient of the pathogenic bacteria by titanium dioxide and zinc oxide nanoparticles. Advanced Pharmaceutical Bulletin 10:56

    Article  CAS  PubMed  Google Scholar 

  • Arciola CR, Campoccia D, Ravaioli S, Montanaro L (2015) Polysaccharide intercellular adhesin in biofilm: structural and regulatory aspects. Front Cell Infect Microbiol 5:7

    Article  PubMed  PubMed Central  Google Scholar 

  • Béatrice J, Maud P, Stéphane A, François C, Frédéric G, Benoit G, Marie-Odile H (2005) Relative expression of Pseudomonas aeruginosa virulence genes analyzed by a real time RT-PCR method during lung infection in rats. FEMS Microbiol Lett 243:271–278

    Article  Google Scholar 

  • Behera SS, Das U, Kumar A, Bissoyi A, Singh AK (2017) Chitosan/TiO2 composite membrane improves proliferation and survival of L929 fibroblast cells: Application in wound dressing and skin regeneration. Int J Biol Macromol 98:329–340

    Article  CAS  PubMed  Google Scholar 

  • Cör D, Knez Ž, Hrnčič MK (2018) Antitumour, antimicrobial, antioxidant and antiacetylcholinesterase effect of Ganoderma lucidum terpenoids and polysaccharides: A review. Molecules 23:649

    Article  PubMed  PubMed Central  Google Scholar 

  • Foti C, Piperno A, Scala A, Giuffrè O (2021) Oxazolidinone antibiotics: chemical, biological and analytical aspects. Molecules 26:4280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao Y, Zhou S, Huang M, Anlong Xu (2003) Antibacterial and antiviral value of the genus Ganoderma P. Karst. species (Aphyllophoromycetideae): a review. Inter J Med Mushroom. 5:231

    Article  Google Scholar 

  • Gheidar H, Haddadi A, Kalani BS, Amirmozafari N (2018) Nanoparticles impact the expression of the genes involved in biofilm formation in S. aureus, a model antimicrobial-resistant species. J Med Bacteriol 7:30–41

    CAS  Google Scholar 

  • Hajipour MJ, Fromm KM, Ashkarran AA, Jimenez D, de Aberasturi I, de Larramendi R, Rojo T, Serpooshan V, Parak WJ, Mahmoudi M (2012) Antibacterial properties of nanoparticles. Trends Biotechnol 30:499–511

    Article  CAS  PubMed  Google Scholar 

  • Hapuarachchi KK, Elkhateeb WA, Karunarathna SC, Cheng CR, Bandara AR, Kakumyan P, Hyde KD, Daba GM, Wen TC (2018) Current status of global Ganoderma cultivation, products, industry and market. Mycosphere 9:1025–1052

    Article  Google Scholar 

  • Heleno SA, Ferreira ICFR, Esteves AP, Ćirić A, Glamočlija J, Martins A, Soković M, Maria João RP, Queiroz. (2013) Antimicrobial and demelanizing activity of Ganoderma lucidum extract, p-hydroxybenzoic and cinnamic acids and their synthetic acetylated glucuronide methyl esters. Food Chem Toxicol 58:95–100

    Article  CAS  PubMed  Google Scholar 

  • Humphries R, Bobenchik AM, Hindler JA, Schuetz AN (2021) Overview of changes to the clinical and laboratory standards institute performance standards for antimicrobial susceptibility testing, M100. J Clin Microbiol 59:e00213-e221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ismail NA, Amin KAM, Majid FAA, Razali MH (2019) Gellan gum incorporating titanium dioxide nanoparticles biofilm as wound dressing: Physicochemical, mechanical, antibacterial properties and wound healing studies. Mater Sci Eng, C 103:109770

    Article  CAS  Google Scholar 

  • Jesline A, John NP, Narayanan PM, Vani C, Murugan S (2015) Antimicrobial activity of zinc and titanium dioxide nanoparticles against biofilm-producing methicillin-resistant Staphylococcus aureus. Appl Nanosci 5:157–162

    Article  CAS  Google Scholar 

  • Jokar MH, Mohamadkhani F, Moradzadeh M, Beygi S, Mohamadkhani A (2022) Nickel Nanoparticles/Recycled Polyethylene Terephthalate Nanofibers Reduce AlgD Expression in Pseudomonas aeruginosa. Medical Laboratory Journal 16:21–26

    Google Scholar 

  • Kamali E, Jamali A, Ardebili A, Ezadi F, Mohebbi A (2020) Evaluation of antimicrobial resistance, biofilm forming potential, and the presence of biofilm-related genes among clinical isolates of Pseudomonas aeruginosa. BMC Res Notes 13:1–6

    Article  Google Scholar 

  • Karaca B, Cihan AÇ, Akata I, Altuner EM (2020) Anti-biofilm and antimicrobial activities of five edible and medicinal macrofungi samples on some biofilm producing multi drug resistant Enterococcus strains. Turkish J Agri-Food Sci Technol 8:69–80

    Article  Google Scholar 

  • Kırmusaoğlu S (2019) The methods for detection of biofilm and screening antibiofilm activity of agents. Antimicrobials 33:1–17

    Google Scholar 

  • Kotlhao K, Madiseng MDT, Mtunzi FM, Pakade VE, Modise SJ, Laloo N, Klink MJ (2017) The synthesis of silver, zinc oxide and titanium dioxide nanoparticles and their antimicrobial activity. In Adv Mater Proc. 2:479–484

    Article  Google Scholar 

  • Lowy FD (2003) Antimicrobial resistance: the example of Staphylococcus aureus. J Clin Investig 111:1265–1273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masoumi S, Shakibaie MR, Gholamrezazadeh M, Monirzadeh F (2018) Evaluation synergistic effect of TiO2, ZnO nanoparticles and amphiphilic peptides (Mastoparan-B, indolicidin) against drug-resistant pseudomonas aeruginosa klebsiella pneumoniae and acinetobacter baumannii. Archive Pediatric Infect Dis. 6:31

    Article  Google Scholar 

  • Maurya A, Chauhan P, Mishra A, Pandey AK (2012) Surface functionalization of TiO2 with plant extracts and their combined antimicrobial activities against E. faecalis and E. coli. J Res Update Poly Sci 1:43–51

    CAS  Google Scholar 

  • Mishra J, Rajput R, Singh K, Puri S, Goyal M, Bansal A, Misra K (2018) Antibacterial natural peptide fractions from Indian Ganoderma lucidum. Int J Pept Res Ther 24:543–554

    Article  CAS  Google Scholar 

  • Mohammed Sadiq I, Chandrasekaran N, Mukherjee AJCN (2010) ’Studies on effect of TiO2 nanoparticles on growth and membrane permeability of Escherichia coli. Pseud Aeruginosa 6:381–387

    Google Scholar 

  • Murray CJL, Ikuta KS, Sharara F, Swetschinski L, Aguilar GR, Gray A, Han C, Bisignano C, Rao P, Wool E (2022) Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet 399:629–655

    Article  CAS  Google Scholar 

  • Odds FC (2003) Synergy, antagonism, and what the chequerboard puts between them. J Antimicrob Chemother 52:1–1

    Article  CAS  PubMed  Google Scholar 

  • Pachori P, Gothalwal R, Gandhi P (2019) Emergence of antibiotic resistance Pseudomonas aeruginosa in intensive care unit; a critical review. Genes Dis 6:109–119

    Article  PubMed  PubMed Central  Google Scholar 

  • Peng K-T, Chen J-L, Kuo L-T, Pei-An Yu, Hsu W-H, Lee C-W, Chang P-J, Huang T-Y (2021) GMI, an immunomodulatory peptide from ganoderma microsporum, restrains periprosthetic joint infections via modulating the functions of myeloid-derived suppressor cells and effector T Cells. Int J Mol Sci 22:6854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porto WF, Irazazabal L, Alves ESF, Ribeiro SM, Matos CO, Pires ÁS, Fensterseifer I, Miranda VJ, Haney EF, Humblot V (2018) In silico optimization of a guava antimicrobial peptide enables combinatorial exploration for peptide design. Nat Commun 9:1–12

    Article  CAS  Google Scholar 

  • Quereshi S, Pandey AK, Sandhu SS (2010) Evaluation of antibacterial activity of different Ganoderma lucidum extracts. J Sci Res 3:9–13

    Google Scholar 

  • Radhika R (2021) Antibacterial Activity Of Ganoderma Lucidum Extracts Against Mdr Pathogens. Inter J Modern Agri 10:3488–3493

    Google Scholar 

  • Roguska A, Belcarz A, Zalewska J, Hołdyński M, Andrzejczuk M, Pisarek M, Ginalska G (2018) Metal TiO2 nanotube layers for the treatment of dental implant infections. ACS Appl Mater Interfaces 10:17089–17099

    Article  CAS  PubMed  Google Scholar 

  • Roy AS, Parveen A, Koppalkar AR, Ambika MVN, Prasad. (2010) Effect of nano-titanium dioxide with different antibiotics against methicillin-resistant Staphylococcus aureus. J Biomater Nanobiotechnol 1:37

    Article  CAS  Google Scholar 

  • Sa-Ard P, Sarnthima R, Khammuang S, Kanchanarach W (2015) Antioxidant, antibacterial and DNA protective activities of protein extracts from Ganoderma lucidum. J Food Sci Technol 52:2966–2973

    Article  CAS  PubMed  Google Scholar 

  • Sagadevan S, Vennila S, Preeti Singh J, Lett A, Won Chun Oh, Paiman S, Mohammad F, Al-Lohedan HA, Fatimah Is, Shahid MM (2020) Exploration of the antibacterial capacity and ethanol sensing ability of Cu-TiO2 nanoparticles. J Exp Nanosci 15:337–349

    Article  CAS  Google Scholar 

  • Savin S, Craciunescu O, Oancea A, Ilie D, Ciucan T, Antohi LS, Toma A, Nicolescu A, Deleanu C, Oancea F (2020) Antioxidant, cytotoxic and antimicrobial activity of chitosan preparations extracted from Ganoderma lucidum mushroom. Chem Biodivers 17:e2000175

    Article  CAS  PubMed  Google Scholar 

  • Senarathna ULNH, Fernando SSN, Gunasekara TDCP, Weerasekera MM, Hewageegana HGSP, Arachchi NDH, Siriwardena HD, Jayaweera PM (2017) Enhanced antibacterial activity of TiO2 nanoparticle surface modified with Garcinia zeylanica extract. Chem Cent J 11:1–8

    Article  Google Scholar 

  • Shakerimoghaddam A, Razavi D, Rahvar F, Khurshid M, Ostadkelayeh SM, Esmaeili S-A, Khaledi A, Eshraghi M (2020) Evaluate the effect of zinc oxide and silver nanoparticles on biofilm and icaA gene expression in methicillin-resistant Staphylococcus aureus isolated from burn wound infection. J Burn Care Res 41:1253–1259

    Article  PubMed  Google Scholar 

  • Sheena N, Ajith TA, Mathew A, Janardhanan KK (2003) ’Antibacterial activity of three macrofungi ganoderma lucidum, navesporus floccosa and phellinus rimosus occurring in South India. Pharma Biol 41:564–567

    Article  Google Scholar 

  • Sheikha El, Farag A (2022) Nutritional Profile and Health Benefits of Ganoderma lucidum “Lingzhi, Reishi, or Mannentake” as Functional Foods: Current Scenario and Future Perspectives. Foods 11:1030

    Article  PubMed  PubMed Central  Google Scholar 

  • Skalicka-Wozniak K, Szypowski J, Los, Siwulski M, Sobieralski K, Glowniak Ka, Malm A (2012) Evaluation of polysaccharides content in fruit bodies and their antimicrobial activity of four Ganoderma lucidum (W Curt: Fr) P Karst strains cultivated on different wood type substrates. Acta Soc Bot Pol 81:212

    Article  Google Scholar 

  • Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M, Monnet DL, Pulcini C, Kahlmeter G, Kluytmans J, Carmeli Y (2018) Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis 18:318–327

    Article  PubMed  Google Scholar 

  • Valle D, Cinzia LV, Santin M, Cigada A, Candiani G, Pezzoli D, Arciola CR, Imbriani M, Chiesa R (2012) A novel antibacterial modification treatment of titanium capable to improve osseointegration. Int J Artif Organs 35:864–875

    Article  PubMed  Google Scholar 

  • Vincent MG, John NP, Narayanan PM, Vani C, Murugan S (2014) In vitro study on the efficacy of zinc oxide and titanium dioxide nanoparticles against metallo beta-lactamase and biofilm producing Pseudomonas aeruginosa. J Applied Pharm Sci 4:041–046

    CAS  Google Scholar 

  • Wanmuang H, Leopairut J, Kositchaiwat C, Wananukul W, Bunyaratvej S (2007) Fatal fulminant hepatitis associated with Ganoderma lucidum (Lingzhi) mushroom powder. J-Med Assoc Thailand 90:179

    Google Scholar 

  • Yadav MK, Go YY, Kim SH, Chae S-W, Song J-J (2017) Antimicrobial and antibiofilm effects of human amniotic/chorionic membrane extract on Streptococcus pneumoniae. Front Microbiol 8:1948

    Article  PubMed  PubMed Central  Google Scholar 

  • Ziental D, Czarczynska-Goslinska B, Mlynarczyk DT, Glowacka-Sobotta A, Stanisz B, Goslinski T, Sobotta L (2020) Titanium dioxide nanoparticles: prospects and applications in medicine. Nanomaterials 10:387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors would like to acknowledge the Kashan University of Medical Sciences, Kashan, Iran for financial supports

Funding

Kashan University of Medical Sciences supported the present study (Grant no. 99230). The support of other organizations was not used in this study.

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Research work design was performed by NA-A and ZM]. Material preparation, data collection and analysis were performed by [ZM and SR]. The first draft of the manuscript was written by [ZM and NA-A] and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Ali Nazari-Alam.

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Communicated by Erko Stackebrandt.

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Marzhoseyni, Z., Rashki, S. & Nazari-Alam, A. Evaluation of the inhibitory effects of TiO2 nanoparticle and Ganoderma lucidum extract against biofilm-producing bacteria isolated from clinical samples. Arch Microbiol 205, 59 (2023). https://doi.org/10.1007/s00203-023-03403-4

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  • DOI: https://doi.org/10.1007/s00203-023-03403-4

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