SYNERGISTIC EFFECT OF ESSENTIAL OILS AND SILVER NANOPARTICLES SYNTHESIZED USING GELATIN FOR ANTIBACTERIAL, SOIL RESPIRATION AND SOIL ENZYME ACTIVITIES

Year 2022, , 732 - 749, 01.09.2022

Büşra Esirgenler Fatih Erci

https://doi.org/10.36306/konjes.1106086

Abstract

This study aims to investigate the synthesis of gelatin (Gel) and gelatin-glucose (Gel-Glu) mediated silver nanoparticles (AgNPs) and to investigate their synergies with different essential oils (EO) for antibacterial activity as well as their effects on soil respiration and soil enzyme activities. The antibacterial activities were evaluated using the agar diffusion test. The results of STEM analysis revealed that Gel-Glu-AgNPs in the range of 5–25 nm had a smaller size than Gel-AgNPs. Furthermore, we found that both AgNPs were positively charged by zeta analysis. In addition, at least one of the combinations of Gel-AgNPs and Gel-Glu-AgNPs with EO increased the antibacterial activity. The results also showed that AgNPs reduced soil respiration at the end of 120 h and that combinations of AgNPs and essential oils caused a significant reduction in alkaline phosphatase activities of soil samples compared to dehydrogenase activity, particularly at higher exposure times and concentrations. In conclusion, gelatin played an important role as a reducing and stabilizing agent in the synthesis of AgNPs. Finally, it was evaluated that combining nanoparticles and essential oil led to different results in the interaction of AgNPs with bacteria, which was additionally confirmed by soil respiration and enzyme analysis. The results justify further developing new strategies to uncover the effects of silver nanoparticles in different applications.

Keywords

Silver nanoparticles, Gelatin, Essential oils, Antibacterial activity, Soil enzymes

Supporting Institution

Necmettin Erbakan Üniversitesi Bilimsel Araştırma Projeleri Koordinatörlüğü

Project Number

201315003

Thanks

This study arose from a part of B. Esirgenler’s Master’s thesis. The authors thank Vildan ERCI for soil analysis and Necmettin Erbakan University Science and Technology Research and Application Center (BITAM) for their research infrastructure.

Jelatin Kullanılarak Sentezlenen Gümüş Nanopartiküller ile Esansiyel Yağların Antibakteriyel, Toprak Solunum Ve Toprak Enzim Aktivitelerinde Sinerjistik Etkisi

Abstract

Bu çalışma, jelatin (Jel) ve jelatin-glukoz (Gel-Glu) aracılı gümüş nanopartiküllerin (AgNP'ler) sentezini araştırmayı ve bunların esansiyel yağlar (EO) ile sinerjilerinin toprak solunumu ve toprak enzim aktiviteleri üzerine etkilerini araştırmayı amaçlamaktadır. Antibakteriyel aktiviteler, agar difüzyon testi kullanılarak değerlendirildi. STEM analizinin sonuçları, 5-25 nm aralığındaki Gel-Glu-AgNP'lerin Gel-AgNP'lerden daha küçük bir boyuta sahip olduğunu ortaya koydu. Buna ilaveten, zeta analizi ile her iki AgNP'nin de pozitif yüke sahip olduğunu bulduk. Ayrıca, Gel-AgNP'ler ve Gel-Glu-AgNP'lerin EO ile kombinasyonlarından en az biri antibakteriyel aktiviteyi arttırdı. Sonuçlar, AgNP'lerin 120 saat sonunda toprak solunumunu azalttığını ve AgNP'ler ile uçucu yağların kombinasyonlarının, özellikle daha yüksek maruz kalma süreleri ve konsantrasyonlarında, dehidrogenaz aktivitesine kıyasla toprak numunelerinin alkalin fosfataz aktivitelerinde önemli bir azalmaya neden olduğunu gösterdi. Sonuç olarak jelatin, AgNP'lerin sentezinde indirgeyici ve stabilize edici bir ajan olarak önemli bir rol oynamıştır. Son olarak, nanopartiküller ve uçucu yağ kombinasyonunun, AgNP'lerin bakterilerle etkileşiminde farklı sonuçlara yol açtığı değerlendirilmiş, ayrıca bu toprak solunumu ve enzim analizi ile de doğrulanmıştır. Elde edilen sonuçlar, farklı uygulamalarda gümüş nanopartiküllerin etkilerini ortaya çıkarmak için yeni stratejilerin daha da geliştirilmesini doğrulamaktadır.

Keywords

Gümüş nanopartiküller, Jelatin, Uçucu yağlar, Antibakteriyel aktivite, Toprak enzimleri

Project Number

201315003

References

• Aewsiri, T., Benjakul, S., Visessanguan, W. 2009, “Functional Properties of Gelatin from Cuttlefish (Sepia pharaonis) Skin as Affected by Bleaching Using Hydrogen Peroxide”, Food Chemistry, Vol. 115, No. 1, pp. 243–249.
• Aruguete, D. M., Hochella, M. F. 2010, “Bacteria–Nanoparticle Interactions and Their Environmental Implications”, Environmental Chemistry, Vol. 7, No. 1, pp. 3–9.
• Behravan, M., Hossein Panahi, A., Naghizadeh, A., Ziaee, M., Mahdavi, R., Mirzapour, A. 2019, “Facile Green Synthesis of Silver Nanoparticles Using Berberis vulgaris Leaf and Root Aqueous Extract and Its Antibacterial Activity”, International Journal of Biological Macromolecules, Vol. 124, pp. 148–154.
• Burdușel, A.-C., Gherasim, O., Grumezescu, A. M., Mogoantă, L., Ficai, A., Andronescu, E. 2018, “Biomedical Applications of Silver Nanoparticles: An up-to-Date Overview”, Nanomaterials, Vol. 8, No. 9, p. 681.
• Burt, J. L., Gutiérrez-Wing, C., Miki-Yoshida, M., José-Yacamán, M. 2004, “Noble-Metal Nanoparticles Directly Conjugated to Globular Proteins”, Langmuir, Vol. 20, No. 26, pp. 11778–11783.
• Caldwell, B. A. 2005, “Enzyme Activities as a Component of Soil Biodiversity: A Review”, Pedobiologia, Vol. 49, No. 6, pp. 637–644.
• Cao, C., Huang, J., Cai, W.-S., Yan, C.-N., Liu, J.-L., Jiang, Y.-D. 2017, “Effects of Silver Nanoparticles on Soil Enzyme Activity of Different Wetland Plant Soil Systems”, Soil and Sediment Contamination: An International Journal, Vol. 26, No. 5, pp. 558–567.
• Cornelis, G., Hund-Rinke, K., Kuhlbusch, T., van den Brink, N., Nickel, C. 2014, “Fate and Bioavailability of Engineered Nanoparticles in Soils: A Review”, Critical Reviews in Environmental Science and Technology, Vol. 44, No. 24, pp. 2720–2764.
• Das, P., Williams, C. J., Fulthorpe, R. R., Hoque, M. E., Metcalfe, C. D., Xenopoulos, M. A. 2012, “Changes in Bacterial Community Structure after Exposure to Silver Nanoparticles in Natural Waters”, Environmental Science & Technology, Vol. 46, No. 16, 2012, pp. 9120–9128.
• Ealia, S. A. M., Saravanakumar, M. P. 2017. "A review on the classification, characterization, synthesis of nanoparticles and their application". In IOP Conference Series: Materials Science and Engineering (Vol. 263, p. 032019). IOP Publishing.
• Erci, F., Cakir-Koc, R. 2021, "Rapid Green Synthesis of Noncytotoxic Iron Oxide Nanoparticles Using Aqueous Leaf Extract of Thymbra spicata and Evaluation of Their Antibacterial, Antibiofilm, And Antioxidant Activity", Inorganic and Nano-Metal Chemistry, Vol. 51, No. 5, pp. 683-692.
• Erci, F., Cakir-Koc, R., Yontem, M., Torlak, E. 2020, "Synthesis of Biologically Active Copper Oxide Nanoparticles as Promising Novel Antibacterial-Antibiofilm Agents", Preparative Biochemistry & Biotechnology, Vol. 50, No. 6, pp. 538–548.
• Erci, F., Koc, R., Isıldak, I., 2018, "Green Synthesis of Silver Nanoparticles Using Thymbra spicata L. Var. spicata (Zahter) Aqueous Leaf Extract and Evaluation of Their Morphology-Dependent Antibacterial and Cytotoxic Activity", Artificial Cells, Nanomedicine, and Biotechnology, Vol. 46, No. sup1, 2018, pp. 150–158.
• Erci, F., Torlak, E., 2019, "Antimicrobial and Antibiofilm Activity of Green Synthesized Silver Nanoparticles by Using Aqueous Leaf Extract of Thymus serpyllum", Sakarya University Journal of Science, Vol. 23, No. 3, pp. 333-339.
• Fabrega, J., Fawcett, S. R., Renshaw, J. C., Lead, J. R., 2009, “Silver Nanoparticle Impact on Bacterial Growth: Effect of PH, Concentration, and Organic Matter”, Environmental Science & Technology, Vol. 43, No. 19, pp. 7285–7290.
• Galvez, A. M., Ramos, K. M., Teja, A. J., Baculi, R., 2021, "Bacterial Exopolysaccharide-Mediated Synthesis of Silver Nanoparticles and Their Application on Bacterial Biofilms”, Journal of Microbiology, Biotechnology and Food Sciences, Vol. 2021, pp. 970–978.
• Gee, G. W., Bauder, J. W., 1986, “Particle‐Size Analysis”, Methods of Soil Analysis: Part 1 Physical and Mineralogical Methods, Vol. 5, Editor: Arnold, K., the American Society of Agronomy, Inc. Soil Science Society of America, Inc., 383–411.
• Gomaa, E. Z., 2017, "Antimicrobial, Antioxidant and Antitumor Activities of Silver Nanoparticles Synthesized by Allium cepa Extract: A Green Approach", Journal of Genetic Engineering and Biotechnology, Vol. 15, No. 1, pp. 49–57.
• Gugino, B.K., Idowu, O.J., Schindelbeck, R.R., van Es, H.M., Wolfe, D.W., Moebius-Clune, B.N., Thies, J.E., Abawi, G.S., 2009, Cornell Soil Health Assessment Training Manual, Edition 2.0, Cornell University, Geneva, NY.
• Gurunathan, S., Han, J., Park, J. H., Kim, J.-H., 2014, "A Green Chemistry Approach for Synthesizing Biocompatible Gold Nanoparticles", Nanoscale Research Letters, Vol. 9, No. 1, pp. 248.
• Jeevanandam, J., Barhoum, A., Chan, Y. S., Dufresne, A., Danquah, M. K., 2018, " Review on Nanoparticles and Nanostructured Materials: History, Sources, Toxicity and Regulations", Beilstein Journal of Nanotechnology, Vol. 9, No. 1, pp. 1050–1074.
• Klute, A., 1986, "Water Retention: Laboratory Methods", In A. Klute (Ed.), Methods of Soil Analysis: Part 1—Physical and Mineralogical Methods (Second Edi,), Madison, Wisconsin USA: American Society of Agronomy, Inc. Soil Science Society of America, Inc. 635–662.
• Lavanya, K., Kalaimurugan, D., Shivakumar, M. S., Venkatesan, S., 2020, "Gelatin Stabilized Silver Nanoparticle Provides Higher Antimicrobial Efficiency as Against Chemically Synthesized Silver Nanoparticle", Journal of Cluster Science, Vol. 31, No. 1, pp. 265–275.
• Lee, C., Zhang*, P., 2013, "Facile Synthesis of Gelatin-Protected Silver Nanoparticles for SERS Applications", Journal of Raman Spectroscopy, Vol. 44, No.6, pp.823–826.
• Mahmoud, K. H., Abbo, M,. 2013, "Synthesis, Characterization and Optical Properties of Gelatin Doped with Silver Nanoparticles", Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, Vol. 116, pp. 610–615.
• McLean, E. O., 1983, "Soil pH and Lime Requirement". Methods of Soil Analysis: Part 2 Chemical and Microbiological Properties, 199–224.
• Mishra, P., Xue, Y., Eivazi, F., Afrasiabi, Z., 2021, "Size, Concentration, Coating, and Exposure Time Effects of Silver Nanoparticles on the Activities of Selected Soil Enzymes", Geoderma, Vol. 381, pp. 114682.
• Moebius-Clune, B.N., Moebius-Clune, D.J., Gugino, B.K., Idowu, O.J., Schindelbeck, R.R., Ristow, A.J., van Es, H.M., Thies, J.E., Shayler, H.A., McBride, M.B., Kurtz, K.S.M., Wolfe, D.W., Abawi, G.S., 2016, Comprehensive Assessment of Soil Health – The Cornell Framework, Edition 3.2, Cornell University, Geneva, NY.
• Morones-Ramirez, J. R., Winkler, J. A., Spina, C. S., Collins, J. J., 2013, "Silver Enhances Antibiotic Activity Against Gram-Negative Bacteria", Science Translational Medicine, Vol. 5, No.190, pp. 190ra81-190ra81.
• Nagarajan, M., Benjakul, S., Prodpran, T., Songtipya, P., Kishimura, H., 2012, "Characteristics and Functional Properties of Gelatin from Splendid Squid (Loligo formosana) Skin as Affected by Extraction Temperatures", Food Hydrocolloids, Vol. 29, No. 2, pp. 389–397.
• Nannipieri, P., Kandeler, E., Ruggiero, P., Burns, R. G., Dick, R. P., 2002, "Enzymes in the Environment: Activity, Ecology, and Applications", Enzyme Activities and Microbiological and Biochemical Processes in Soil. New York (NY): Marcel Dekker, 1–33.
• Nasiriboroumand, M., Montazer, M., Barani, H., 2018, "Preparation and Characterization of Biocompatible Silver Nanoparticles Using Pomegranate Peel Extract", Journal of Photochemistry and Photobiology B: Biology, Vol. 179, pp. 98–104.
• Nelson, D. W., Sommers, L., 1982, "Total Carbon, Organic Carbon, and Organic Matter 1". Methods Of Soil Analysis. Part 2. Chemical and Microbiological Properties, (methodsofsoilan2), 539–579.
• Perugini Biasi-Garbin, R., Saori Otaguiri, E., Morey, A. T., Fernandes da Silva, M., Belotto Morguette, A. E., Armando Contreras Lancheros, C., Kian, D., Perugini, MR., Nakazato, G., Durán, N., Nakamura, C. V., Yamauchi, L. M., Yamada-Ogatta, S. F., 2015. "Effect of Eugenol against Streptococcus agalactiae and Synergistic Interaction with Biologically Produced Silver Nanoparticles", Evidence-Based Complementary and Alternative Medicine, Vol. 2015, pp861497.
• Peyrot, C., Wilkinson, K. J., Desrosiers, M., Sauvé, S., 2014, "Effects of Silver Nanoparticles on Soil Enzyme Activities with and Without Added Organic Matter", Environmental Toxicology and Cchemistry, Vol. 33, No. 1, pp. 115–125.
• Pourjavadi, A., Soleyman, R., 2011, "Silver Nanoparticles with Gelatin Nanoshells: Photochemical Facile Green Synthesis and Their Antimicrobial Activity", Journal of Nanoparticle Research, Vol. 13, No. 10, pp. 4647–4658.
• Prabhu, S., Poulose, E. K., 2012, "Silver Nanoparticles: Mechanism of Antimicrobial Action, Synthesis, Medical Applications, and Toxicity Effects", International Nano Letters, Vol. 2, No. 1, pp. 32.
• Rahmatpour, S., Shirvani, M., Mosaddeghi, M. R., Nourbakhsh, F., Bazarganipour, M., 2017, "Dose–Response Effects of Silver Nanoparticles and Silver Nitrate on Microbial and Enzyme Activities in Calcareous Soils", Geoderma, Vol. 285, pp. 313–322.
• Rath, G., Hussain, T., Chauhan, G., Garg, T., Kumar Goyal, A., 2016, "Fabrication and Characterization of Cefazolin-Loaded Nanofibrous Mats for the Recovery of Post-Surgical Wound", Artificial Cells, Nanomedicine, and Biotechnology, Vol. 44, No. 8, pp. 1783–1792.
• Rhoades, J. D., 1982, "in Methods of Soil Analysis. Part2, Chemical and Microbiological Properties". Soluble salts, 167–179.
• Scandorieiro, S., de Camargo, L. C., Lancheros, C. A. C., Yamada-Ogatta, S. F., Nakamura, C. v, de Oliveira, A. G., Andrade C. G. T. J., Duran, N., Nakazato, G., Kobayashi, R. K. T., 2016, "Synergistic and Additive Effect of Oregano Essential Oil and Biological Silver Nanoparticles against Multidrug-Resistant Bacterial Strains ", Frontiers in Microbiology, Vol. 7, pp. 760.
• Singh, J., Dutta, T., Kim, K.-H., Rawat, M., Samddar, P., Kumar, P., 2018, "‘Green’ Synthesis of Metals and Their Oxide Nanoparticles: Applications for Environmental Remediation", Journal of Nanobiotechnology, Vol. 16, No. 1, pp. 84.
• Song, W., Ge, S., 2019, "Application of Antimicrobial Nanoparticles in Dentistry", Molecules, Vol. 24, No. 6, pp. 1033. Su, C. H., Velusamy, P., Kumar, G. V., Adhikary, S., Pandian, K., Anbu, P., 2017, "Studies of Antibacterial Efficacy of Different Biopolymer Protected Silver Nanoparticles Synthesized under Reflux Condition", Journal of Molecular Structure, Vol. 1128, pp. 718–723.
• Tabatabai, M. A., Bremner, J. M., 1969, "Use of P-Nitrophenyl Phosphate for Assay of Soil Phosphatase Activity", Soil Biology and Biochemistry, Vol. 1, No. 4, pp. 301–307.
• Thalmann, A., 1968, "Zur Methodik der Bestimmung der DehydrogenaseaktivitAt im Boden mittels triphenytetrazoliumchlorid (TTC)", Landwirtsch Forsch, Vol. 21, pp. 249–258.
• Wijnhoven, S. W. P., Peijnenburg, W. J. G. M., Herberts, C. A., Hagens, W. I., Oomen, A. G., Heugens, E. H. W., Roszek, B., Bisschops, J., Gosens, I., Van De Meent, D., Dekkers, S., De Jong,W. H., van Zijverden, M., Sips, A. J.A.M., Geertsma, R. E., 2009, " Nano-Silver – a Review of Available Data and Knowledge Gaps in Human and Environmental Risk Assessment”, Nanotoxicology, Vol. 3, No. 2, pp. 109–138.
• Wright, A. F., Bailey, J. S., 2001, “Organic Carbon, Total Carbon, and Total Nitrogen Determinations in Soils of Variable Calcium Carbonate Contents Using a Leco CN-2000 Dry Combustion Analyzer”, Communications in Soil Science and Plant Analysis, Vol. 32, No. 19–20, pp. 3243–58.
• Yılmaz Öztürk, B., Yenice Gürsu, B., Dağ, İ., 2020, "Antibiofilm and Antimicrobial Activities of Green Synthesized Silver Nanoparticles Using Marine Red Algae Gelidium corneum", Process Biochemistry, Vol. 89, pp. 208–219.
• Yiwei, A., Yunxia, Y., Shuanglong, Y., Lihua, D., Guorong, C., 2007, "Preparation of Spherical Silver Particles for Solar Cell Electronic Paste with Gelatin Protection”, Materials Chemistry and Physics, Vol. 104, No. 1, pp. 158–161.
• Yun’an Qing, L. C., Li, R., Liu, G., Zhang, Y., Tang, X., Wang, J., Liu, H., Qin, Y., 2018, " Potential Antibacterial Mechanism of Silver Nanoparticles and the Optimization of Orthopedic Implants by Advanced Modification Technologies”, International Journal of Nanomedicine, Vol. 13, p. 3311.
• Zhang, C., Hu, Z., Deng, B., 2016, “Silver Nanoparticles in Aquatic Environments: Physiochemical Behavior and Antimicrobial Mechanisms”, Water Research, Vol. 88, pp. 403–427.