Biosynthesis of silver nanoparticles by extracellular metabolites of marine Kocuria flava and investigated its role in enhancing of antibacterial activity of ciprofloxacin

Authors

  • Fadhil Jabbar Farhan Department of Biology, College of Education for Pure Science, University of Basrah, Basrah, Iraq. https://orcid.org/0000-0002-4130-8840
  • Ali Aboud Shareef Department of Biology, College of Education for Pure Science, University of Basrah, Basrah, Iraq.

DOI:

https://doi.org/10.21123/bsj.2024.9965

Keywords:

دقائق الفضة النانوية، تعزيز نشاط المضاد الحيوي، Ciprofloxacin، Kocuria flava، البكتيريا المقاومة للمضادات الحيوية MDR

Abstract

The current study aimed to biosynthesize silver nanoparticles (AgNPs) by extracellular metabolites of marine Kocuria flava, and characterization it, then use them to enhance the ciprofloxacin activity against MDR pathogenic bacteria. The seawater was collected from the Iraqi Marine Water in January 2022. The isolate K. flava (F57) was identified by morphological, some biochemical, and molecular identification by 16S rDNA amplification and sequencing. The identity (%) of the F57 16SrDNA gene with those in GenBank was 99.93%, and the phylogenetic tree showed high identity with K. flava ‎strain AUMC‎ B-459. GC/MS spectrometry of the F57 extract revealed the presence of thirty compounds. The extracellular metabolites of F57 are used to biosynthesize of AgNPs., and the production of AgNPs was verified by UV–Vis spectroscopy, FTIR- spectrum, XRD, FESEM, and EDX analysis. The antimicrobial activity of AgNPs was investigated against Klebsiella pneumoniae, Pseudomonas aeruginosa, Staphylococcus haemolyticus, and two isolates of Escherichia coli (1&2), the results showed that AgNPs were effective against these pathogens. The minimal inhibitory concentration (MIC) of AgNPs, ciprofloxacin, and their combination was investigated against these MDR pathogens. The lowest MIC of AgNPs. was 7.81 µg/ml against P. aeruginosa. All pathogenic bacteria were resistant to ciprofloxacin. The combination of ciprofloxacin and AgNPs had a ‎synergistic effect on P. aeruginosa, S. haemolyticus, and E. coli (2). The isolates E. coli (1&2) became sensitive to ciprofloxacin after being mixed with AgNPs. So, the biosynthesized AgNPs. by extracellular metabolites of marine K. flava had antimicrobial properties and contributed to enhancing the effectiveness of ciprofloxacin. 

References

‎ Adebayo-Tayo BC, Ekundayo-Obaba O, Falodun OI. Antimicrobial potential of bioactive ‎metabolites and silver nanoparticles from bacillus spp. and of some antibiotics against multidrug-resistant salmonella spp. Turkish J Pharm Sci. 2020; 17(5): 511-522. https://doi.org/10.4274/tjps.galenos.2019.46548

‎2.‎ Catalano A, Iacopetta D, Ceramella J, Scumaci D, Giuzio F, Saturnino C, et al. Multidrug Resistance (MDR): A widespread phenomenon in ‎pharmacological ‎therapies. Molecules. 2022;‎ 27‎(3): 616-634. https://doi.org/10.3390/molecules27030616

‎3.‎ Singh AA, Singh AK, Nerurkar A. Bacteria associated with marine macroorganisms as potential source of ‎quorum-sensing antagonists. J Basic Microbiol. 2020; 60(9): 799-808. https://doi.org/10.1002/jobm.202000231

‎4.‎ Gahlawat G, Choudhury AR. A review on the biosynthesis of metal and metal salt nanoparticles by microbes. RSC Adv. 2019; 9(23): 12944-12967. https://doi.org/10.1039/c8ra10483b

‎5.‎ Abbas AZ, Abdulrahman RB, Mustafa TA. Preparation and Characterization of Silver Nanoparticles and its ‎Medical Application against Pathogenic Bacteria. Baghdad Sci J. 2024; 21(1): 204-216. https://doi.org/10.21123/bsj.2023.7763

‎6.‎ Li P, Li J, Wu C, Wu Q, Li J. Synergistic antibacterial effects of β-lactam antibiotic combined with silver ‎‎nanoparticles. Nanotechnology. 2005; 16:‎ 1912–1917‎.‎https://doi.org/10.1088/0957-4484/16/9/082

‎7.‎ Singh R, Wagh P, Wadhwani S, Gaidhani S, Kumbhar A, Bellare J, et al. Synthesis, optimization, and characterization of silver nanoparticles from Acinetobacter calcoaceticus and their enhanced antibacterial activity when combined with antibiotics. Int J Nanomedicine. 2013; 8: 4277-90. https://doi.org/10.2147/IJN.S48913

‎8.‎ Tharwat NA, Saleh NM, Hamouda RE, El Shreif RH, Elnagdy SM, Mohamed G. Combination of ciprofloxacin ‎and silver nanoparticles for treatment of multi-drug resistant ‎Pseudomonas aeruginosa in Egypt. Al-Azhar J Pharm ‎Sci. 2019; 59(1): 107-122. https://doi.org/10.21608/ajps.2019.64110

‎9.‎ Khalil MA, El Maghraby GM, Sonbol FI, Allam NG, Ateya PS, Ali SS. Enhanced efficacy of some ‎antibiotics in presence of silver nanoparticles against multidrug resistant Pseudomonas aeruginosa ‎recovered from burn wound infections. Front Microbiol. 2021; 12: 648560. https://doi.org/10.3389/fmicb.2021.648560

‎10.‎ Khalil MA, El-Shanshoury AERR, Alghamdi MA, Sun J, Ali SS. Streptomyces catenulae as a Novel Marine ‎Actinobacterium Mediated Silver Nanoparticles: Characterization, Biological Activities, and Proposed ‎Mechanism of Antibacterial Action. Front Microbiol. 2022; 13: 833154. https://doi.org/10.3389/fmicb.2022.833154

‎11.‎ Khalil MA, El-Shanshoury AER, Alghamdi MA, Alsalmi FA, Mohamed SF, Sun J, et al. Biosynthesis of Silver Nanoparticles by Marine ‎Actinobacterium Nocardiopsis dassonvillei and Exploring Their Therapeutic Potentials. Front Microbiol. ‎‎2022; 12: 705673. https://doi.org/10.3389/fmicb.2021.705673

‎12.‎ Haji SH, Ali FA, Aka STH. Synergistic antibacterial activity of silver nanoparticles biosynthesized by ‎carbapenem-resistant Gram-negative bacilli. Sci Reports. 2022; 12(1):‎ 15254‎. https://doi.org/10.1038/s41598-022-19698-0

‎ Hasson SO, Salman SAK, Hassan SF, Abbas SM. Antimicrobial Effect of Eco-Friendly Silver Nanoparticles ‎Synthesis by Iraqi Date Palm (Phoenix dactylifera) on Gram-Negative Biofilm-Forming Bacteria. Baghdad ‎Sci J. 2021; 18(4): 1149-1156. https://doi.org/10.21123/bsj.2021.18.4.1149

‎14.‎ Syakti AD, Lestari P, Simanora S, Sari LK, Lestari F, Idris F, et al. Culturable hydrocarbonoclastic marine bacterial isolates from Indonesian seawater in the Lombok Strait and Indian Ocean. Heliyon. 2019; 5(5): e01594. https://doi.org/10.1016/j.heliyon.2019.e01594

‎15.‎ Amdadul Huq M, Akter S. Characterization and genome analysis of Arthrobacter bangladeshi sp. Nov., ‎applied for the green synthesis of silver nanoparticles and their antibacterial efficacy against drug-resistant ‎human pathogens. Pharmaceutics. 2021; 13(10). https://doi.org/10.3390/pharmaceutics13101691

‎16.‎ Prescott H. Laboratory exercises in microbiology. 5th.Ed. McGraw−Hill Companies. New York, USA, 2002;449p.

‎17.‎ Wilson KH, Blitchington RB, Greene RC. Amplification of bacterial 16S ribosomal DNA with polymerase chain reaction. J Clin Microbiol. 1990; 28(9): 1942-1946. https://doi.org/10.1128/jcm.28.9.1942-1946.1990

‎18.‎ Raji AI, Möller C, Litthauer D, van Heerden E, Piater LA. Bacterial diversity of biofilm samples from deep ‎mines in South Africa. Biokemistri. 2008; 20(2): 53-62.

‎19.‎ Tamura K, Stecher G, Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol ‎Evol. 2021; 38(7): 3022-3027. https://doi.org/10.1093/molbev/msab120

‎20.‎ Naveed M, Ishfaq H, Rehman SU, Javed A, Waseem M, Makhdoom SI, et al. GC–MS profiling of Bacillus spp. metabolites with an in ‎vitro biological activity assessment and computational analysis of their impact on epithelial ‎glioblastoma cancer genes. Front Chem. 2023; 11: 1-14. https://doi.org/10.3389/fchem.2023.1287599

Goel N, Ahmad R, Singh R, Sood S, Khare SK. Biologically synthesized silver nanoparticles by Streptomyces ‎sp. EMB24 extracts used against the drug-resistant bacteria. Bioresour Technol Rep. 2021; 15(2): 100753. ‎ https://doi.org/10.1016/j.biteb.2021.100753

‎22.‎ Perez C, Pauli M, Bazerque P. An antibiotic assay by the agar well diffusion method. Acta Biol Med Exp. ‎‎1990; 15(1): 113-115. https://www.researchgate.net/publication/303960600

‎ Bellio P, Fagnani L, Nazzicone L, Celenza G ‎. New and simplified method for drug combination studies by ‎checkerboard ‎assay. MethodsX. 2021; 8:‎ 101543‎. https://doi.org/10.1016/j.mex.2021.101543

‎24.‎ Bayroodi E, Jalal R. Modulation of antibiotic resistance in Pseudomonas aeruginosa by ZnO nanoparticles. ‎Iran J Microbiol. 2016; 8(2): 85-92.

‎25.‎ Fadwa AO, Alkoblan DK, Mateen A, Albarag AM. Synergistic effects of zinc oxide nanoparticles and various ‎antibiotics combination against Pseudomonas aeruginosa clinically isolated bacterial strains. Saudi J Biol Sci. ‎‎2021; 28(1): 928-935. https://doi.org/10.1016/j.sjbs.2020.09.064

‎26.‎ Omer NH. Water Quality Parameters. In: Summers JK, ed. Water Quality - Science, Assessments ‎and Policy. IntechOpen; 2020. https://doi.org/10.5772/intechopen.89657

‎ Shareef NF, Mahdi MM‎. Studying of recent environments in Faw, Khor Al-Zubair and Um-Qaser areas, ‎‎Southwestern Arabian Gulf, Basrah, Iraq. J Basrah Rese ((Sci))‎. 2015; 41(2): 1-14.

‎28.‎ Jaafar RS, Al-Taee A, Al-Kanany FN. Bacterial Diversity in Different Positions in the Iraqi Marine Area. ‎Baghdad Sci J. 2023; 20(1): 1-6. https://doi.org/10.21123/bsj.2022.6610

‎29.‎ Aertsen A, Meersman F, Hendrick MEG, Vogel RF, Michiels CW‎. Biotechnology under high pressure: ‎Applications and implications‎. Trends Biotechnol‎. 2009; 27: ‎434-441‎. https://doi.org/10.1016/j.tibtech.2009.04.001

‎30.‎ Zhou G, Luo X, Tang Y, Zhang L, Yang Q. Kocuria flava sp. nov. and Kocuria turfanensis sp. nov., airborne ‎actinobacteria isolated from Xinjiang, China. Int J Syst Evol Microbiol. 2008; 1: 1304-1307. https://doi.org/10.1099/ijs.0.65323-0

‎31.‎ Sun W, Liu C, Zhang F, Zhao M, Li Z. Comparative genomics provides insights into the marine adaptation in ‎sponge-derived Kocuria flava S43. Front Microbiol. 2018; 9: 1257-1268. https://doi.org/10.3389/fmicb.2018.01257

‎32.‎ Deutsch Y, Samara M, Nasser A, Berman-Frank I, Ezra D. Kocuria flava, a Bacterial Endophyte of the Marine ‎Macroalga Bryopsis plumosa, Emits 8-Nonenoic Acid Which Inhibits the Aquaculture Pathogen Saprolegnia ‎parasitica. Mar Drugs. 2023; 21(9): 476-488. https://doi.org/10.3390/md21090476

‎33.‎ Kiran GS, Priyadharsini S, Sajayan A, Ravindran A, Selvin J. An antibiotic agent pyrrolo[1,2-: A] pyrazine-‎‎1,4-dione,hexahydro isolated from a marine bacteria Bacillus tequilensis MSI45 effectively controls multi-‎drug resistant Staphylococcus aureus. RSC Adv. 2018; 8(32): 17837-17846. https://doi.org/10.1039/C8RA00820E

‎34.‎ Ser HL, Palanisamy UD, Yin WF, Abd Malek SN, Chan KG, Goh BH, et al. Presence of antioxidative agent, Pyrrolo[1,2-a]pyrazine-1,4-dione, ‎hexahydro- in newly isolated Streptomyces mangrovisoli sp nov. Front Microbiol. 2015; 6: 854. https://doi.org/10.3389/fmicb.2015.00854

‎35.‎ Raut LS, Rakh RR, Hamde VS. In vitro biocontrol scenarios of Bacillus amyloliquefaciens subsp. ‎amyloliquefaciens strain rls19 in response to Alternaria macrospora, an Alternaria leaf spot phytopathogen of ‎bt cotton. J Appl Biol Biotechnol. 2021; 9(1): 75-82. http://dx.doi.org/10.7324/JABB.2021.9110

‎36.‎ Anwar S, Mahmood F, Tahir NA, Salih GF. Secondary Compounds Released By Rhizospheric Bacteria ‎Exhibit Fungistatic Effects Against Phytopathogenic Fungus. Iraqi J Agric Sci. 2022; 53(5): 1174-1183. https://doi.org/10.36103/ijas.v53i5.1631

‎37.‎ Manimaran M, Kannabiran K. Marine Streptomyces sp. VITMK1 derived Pyrrolo [1, 2-A] Pyrazine-1, 4-‎Dione, Hexahydro-3-(2-Methylpropyl) and its free radical scavenging activity. Open Bioact Compd J. ‎‎2017; 5(1): 23-30. http://dx.doi.org/10.2174/1874847301705010023

‎38.‎ Carcamo-Noriega EN, Sathyamoorthi S, Banerjee S, Gnanamani E, Mendoza-Trujillo M, Mata-Espinosa D, et al. 1,4-Benzoquinone antimicrobial agents against ‎Staphylococcus aureus and Mycobacterium tuberculosis derived from scorpion venom. Proc Natl Acad Sci U ‎S A. 2019; 116(26): 12642-12647. https://doi.org/10.1073/pnas.1812334116

‎39.‎ da Silva RE, Ribeiro FOS, de Carvalho AMA, Daboit TC, Marinho-Filho JDB, Matos TS, et al. Antimicrobial and antibiofilm activity of the ‎benzoquinone oncocalyxone A. Microb Pathog. 2020; 149(September):‎ 104513‎. https://doi.org/10.1016/j.micpath.2020.104513

‎40.‎ Shanshoury AERE, Sabae SZ, Shouny WAE, Shady AMA, Badr HM. Extracellular biosynthesis of ‎silver nanoparticles using aquatic bacterial isolate and its antibacterial and antioxidant potentials. ‎Egypt J Aquat Biol Fish. 2020; 24(7 Special issue): 183-201. http://dx.doi.org/10.21608/EJABF.2020.119399

‎41.‎ Al-Hayanni HSA, Alnuaimi MT, Al-Lami RAH, Zaboon SM. Antibacterial Effect of Silver Nanoparticles ‎Prepared from Sophora flavescens Root Aqueous Extracts against Multidrug-resistance Pseudomonas ‎aeruginosa and Staphylococcus aureus. J Pure Appl Microbiol. 2022; 16(4): 2880-2890. https://doi.org/10.22207/JPAM.16.4.61

‎42.‎ Yassin MT, Mostafa AAF, Al-Askar AA, Al-Otibi FO. Synergistic Antibacterial Activity of Green ‎Synthesized Silver Nanomaterials with Colistin Antibiotic against Multidrug-Resistant Bacterial Pathogens. ‎Crystals. 2022; 12(8): 1057. https://doi.org/10.3390/cryst12081057

‎43.‎ Alsamhary KI. Eco-friendly synthesis of silver nanoparticles by Bacillus subtilis and their antibacterial ‎activity. Saudi J Biol Sci. 2020; 27(8): 2185-2191. https://doi.org/10.1016/j.sjbs.2020.04.026

‎44.‎ Naseer QA, Xue X, Wang X, Dang S, Din SU, Kalsoom Jamil J. Synthesis of silver nanoparticles using Lactobacillus bulgaricus and ‎assessment of their antibacterial potential. Brazilian J Biol. 2022; 82: e232434‎. https://doi.org/10.1590/1519-6984.232434

‎45.‎ Tufail MS, Liaqat I, Andleeb S, Naseem S, Zafar U, Sadiqa A, et al. Biogenic Synthesis, Characterization and Antibacterial Properties of ‎Silver Nanoparticles against Human Pathogens. J Oleo Sci. 2022; 71(2): 257-265. https://doi.org/10.5650/jos.ess21291

‎46.‎ Shareef AA, Farhan FJ, Alriyahee FAA. Green Synthesis of Silver Nanoparticles Using Aqueous Extract of ‎Typha domingensis Pers. Pollen (qurraid) and Evaluate its Antibacterial Activity. Baghdad Sci J. 2024; 21(1): 28-40. https://doi.org/10.21123/bsj.2023.7624

‎47.‎ Naganthran A, Verasoundarapandian G, Khalid FE, Masarudin MJ, Zulkharnain A, Nawawi NM, et al. Synthesis, Characterization and ‎Biomedical Application of Silver Nanoparticles. Materials (Basel). 2022; 15(2): 1-43. https://doi.org/10.3390%2Fma15020427

‎48.‎ Shareef AA, Hassan ZA, Kadhim MA, Al-Mussawi AA. Antibacterial activity of silver nanoparticles ‎synthesized by aqueous extract of Carthamus oxycantha M.Bieb. Against antibiotics resistant bacteria. ‎Baghdad Sci J. 2022; 19(3): 460-468. https://doi.org/10.21123/bsj.2022.19.3.0460

‎49.‎ Nile SH, Baskar V, Selvaraj D, Nile A, Xiao J, Kai G. Nanotechnologies in Food Science: Applications, Recent Trends, and Future Perspectives. Nanomicro Lett. 2020; 12(1): 45-79. https://doi.org/10.1007/s40820-020-0383-9

‎50.‎ Qin W, Wang CY, Ma YX, Shen MJ, Li J, Jiao K, et al. Microbe-mediated extracellular and intracellular mineralization: environmental, industrial, and biotechnological applications. Adv Mater. 2020; 32(22): e1907833. https://doi.org/10.1002/adma.201907833

‎51.‎ Singh S, Bharti A, Meena VK. Green synthesis of multi-shaped silver nanoparticles: optical, morphological ‎and antibacterial properties. J Mater Sci: Mater Electron. 2015; 26(6): 3638-3648. http://dx.doi.org/10.1007/s10854-015-2881-y

‎52.‎ Mohammad D, Al-Jubouri SHK. Comparative Antimicrobial Activity of Silver Nanoparticles ‎Synthesized by Corynebacterium glutamicum and Plant Extracts. Baghdad Sci J. 2019; 16(3): 689-696. https://doi.org/10.21123/bsj.2019.16.3(Suppl.).0689

‎53.‎ Sharma PC, Jain A, Jain S, Pahwa R, Yar MS. Ciprofloxacin: Review on developments in synthetic, analytical, ‎and medicinal aspects. J Enzyme Inhib Med Chem. 2010; 25(4): 577-589. https://doi.org/10.3109/14756360903373350

‎54.‎ Hussein-Al-Ali SH, Abudoleh SM, Abualassal QIA, Abudayeh Z, Aldalahmah Y, Hussein MZ. Preparation ‎and characterisation of ciprofloxacin-loaded silver nanoparticles for drug delivery. IET Nanobiotechnol. ‎‎2022; 16(3): 92-101. https://doi.org/10.1049/nbt2.12081

Downloads

Issue

Section

article

How to Cite

1.
Biosynthesis of silver nanoparticles by extracellular metabolites of marine Kocuria flava and investigated its role in enhancing of antibacterial activity of ciprofloxacin. Baghdad Sci.J [Internet]. [cited 2024 Sep. 27];22(3). Available from: https://bsj.uobaghdad.edu.iq/index.php/BSJ/article/view/9965