Bacterial Synthesis of Metallic Nanoparticles for Biomedical Applications

Document Type : Review Article

Authors

1 Department of Otorhinolaryngology,The Dingli Clinical College of Wenzhou Medical University(The Second Affiliated Hospital of Shanghai University,Wenzhou Central Hospital), Wenzhou, Zhejiang Province 325000,China

2 Department of Infectious Diseases, Wenzhou Central Hospital, The Dingli Clinical College of Wenzhou Medical University, The Second Affiliated Hospital of Shanghai University, Wenzhou, Zhejiang Province 325000, China

3 Laboratory of Infectious Diseases, Wenzhou Central Hospital, The Dingli Clinical College of Wenzhou Medical University, The Second Affiliated Hospital of Shanghai University, Wenzhou, Zhejiang Province 325000, China

Abstract

Metallic nanoparticles, especially silver and gold, have promising applications in biomedicine due to their unique optical, electronic, and chemical properties. Conventionally, physical and chemical methods have been used to synthesize these nanoparticles; however, bacterial synthesis has recently emerged as an environmentally friendly, cost-effective, and facile alternative. In this review, we summarize recent progress in understanding the mechanisms underlying microbial nanoparticle biosynthesis and highlight key bacterial strains that have been exploited for efficient, controlled nanoparticle fabrication, including Escherichia coli, Bacillus subtilis, and Geobacillus sp. We discuss current genetic and process engineering strategies to improve the quality, yield, and mono-dispersity of bacterially synthesized metallic nanoparticles. Furthermore, we overview promising biomedical uses of these nanoparticles being actively explored, ranging from drug delivery vehicles, bioimaging tracers, diagnostics, and biosensors, to antibacterial agents and materials with accelerated wound healing capacity. Finally, we outline prospects and challenges toward scale-up, regulation, and adoption of green, biosynthesized metallic nanomaterials for various healthcare applications.

Graphical Abstract

Bacterial Synthesis of Metallic Nanoparticles for Biomedical Applications

Keywords


[1] G. Heidari, M. Hassanpour, F. Nejaddehbashi, M.R. Sarfjoo, S. Yousefiasl, E. Sharifi, A. Bigham, T. Agarwal, A. Borzacchiello, E. Lagreca, C. Di Natale, N. Nikfarjam, Y. Vasseghian, Materials Chemistry Horizons REVIEW Biosynthesized Nanomaterials with Antioxidant and Antimicrobial Properties, Mater. Chem. Horizons. 2022 (2022) 35–48.
[2] E. Alizadeh, H. Baseri, Photocatalytic Degradation of Sumatriptan Succinate by ZnO, Fe Doped ZnO and TiO2-ZnO Nanocatalysts, Mater. Chem. Horizons. 1 (2022) 7–21.
[3] A. Guerrero-Martínez, S. Barbosa, I. Pastoriza-Santos, L.M. Liz-Marzán, Nanostars shine bright for you: colloidal synthesis, properties and applications of branched metallic nanoparticles, Colloid. Synth. Plasmonic Nanometals. (2020) 285–320.
[4] L.D. Trino, E.S. Bronze-Uhle, A. Ramachandran, P.N. Lisboa-Filho, M.T. Mathew, A. George, Titanium surface bio-functionalization using osteogenic peptides: surface chemistry, biocompatibility, corrosion and tribocorrosion aspects, J. Mech. Behav. Biomed. Mater. 81 (2018) 26–38.
[5] K. Hatami Kahkesh, Z. Baghbantaraghdari, D. Jamaledin, F. Dabbagh Moghaddam, N. Kaneko, M. Ghovvati, Synthesis, Characterization, Antioxidant and Antibacterial Activities of Zinc Ferrite and Copper Ferrite Nanoparticles, Mater. Chem. Horizons. 2 (2023) 49–56.
[6] L.A. Anderson, M.A. Islam, K.L.J. Prather, Synthetic biology strategies for improving microbial synthesis of “green” biopolymers, J. Biol. Chem. 293 (2018) 5053–5061.
[7] S.F. Ahmed, M. Mofijur, N. Rafa, A.T. Chowdhury, S. Chowdhury, M. Nahrin, A.B.M.S. Islam, H.C. Ong, Green approaches in synthesising nanomaterials for environmental nanobioremediation: Technological advancements, applications, benefits and challenges, Environ. Res. 204 (2022) 111967.
[8] P.P. Gan, S.F.Y. Li, Potential of plant as a biological factory to synthesize gold and silver nanoparticles and their applications, Rev. Environ. Sci. Bio/Technology. 11 (2012) 169–206.
[9] D. Lombardo, P. Calandra, L. Pasqua, S. Magazù, Self-assembly of organic nanomaterials and biomaterials: The bottom-up approach for functional nanostructures formation and advanced applications, Materials (Basel). 13 (2020) 1048.
[10] M.A.S. Amulya, H.P. Nagaswarupa, M.R.A. Kumar, C.R. Ravikumar, K.B. Kusuma, Sonochemical synthesis of MnFe2O4 nanoparticles and their electrochemical and photocatalytic properties, J. Phys. Chem. Solids. 148 (2021) 109661.
[11] T.-Y. Kim, M.G. Kim, J.-H. Lee, H.-G. Hur, Biosynthesis of nanomaterials by Shewanella species for application in lithium ion batteries, Front. Microbiol. 9 (2018) 2817.
[12] H.W. Harris, I. Sánchez-Andrea, J.S. McLean, E.C. Salas, W. Tran, M.Y. El-Naggar, K.H. Nealson, Redox sensing within the genus Shewanella, Front. Microbiol. 8 (2018) 2568.
[13] A.J. Murray, J. Zhu, J. Wood, L.E. Macaskie, A novel biorefinery: biorecovery of precious metals from spent automotive catalyst leachates into new catalysts effective in metal reduction and in the hydrogenation of 2-pentyne, Miner. Eng. 113 (2017) 102–108.
[14] R. Ahmad, S. Srivastava, S. Ghosh, S.K. Khare, Phytochemical delivery through nanocarriers: A review, Colloids Surfaces B Biointerfaces. 197 (2021) 111389.
[15] P.G. Jamkhande, N.W. Ghule, A.H. Bamer, M.G. Kalaskar, Metal nanoparticles synthesis: An overview on methods of preparation, advantages and disadvantages, and applications, J. Drug Deliv. Sci. Technol. 53 (2019) 101174.
[16] P. Khandel, R.K. Yadaw, D.K. Soni, L. Kanwar, S.K. Shahi, Biogenesis of metal nanoparticles and their pharmacological applications: present status and application prospects, J. Nanostructure Chem. 8 (2018) 217–254.
[17] J.P. Audia, C.C. Webb, J.W. Foster, Breaking through the acid barrier: an orchestrated response to proton stress by enteric bacteria, Int. J. Med. Microbiol. 291 (2001) 97–106.
[18] T.L. Turner, S.D. Mitra, T.J. Kochan, N.B. Pincus, M. Lebrun-Corbin, B.H. Cheung, S.W. Gatesy, T. Afzal, S.H. Nozick, E.A. Ozer, Taxonomic characterization of Pseudomonas hygromyciniae sp. nov., a novel species discovered from a commercially purchased antibiotic, Microbiol. Spectr. 11 (2023) e01838-21.
[19] M. Saravanan, S.K. Barik, D. MubarakAli, P. Prakash, A. Pugazhendhi, Synthesis of silver nanoparticles from Bacillus brevis (NCIM 2533) and their antibacterial activity against pathogenic bacteria, Microb. Pathog. 116 (2018) 221–226.
[20] L. Wu, G. Zhu, X. Zhang, Y. Si, Silver nanoparticles inhibit denitrification by altering the viability and metabolic activity of Pseudomonas stutzeri, Sci. Total Environ. 706 (2020) 135711.
[21] I. Ghiuță, D. Cristea, C. Croitoru, J. Kost, R. Wenkert, I. Vyrides, A. Anayiotos, D. Munteanu, Characterization and antimicrobial activity of silver nanoparticles, biosynthesized using Bacillus species, Appl. Surf. Sci. 438 (2018) 66–73.
[22] C. Anning, J. Wang, P. Chen, I. Batmunkh, X. Lyu, Determination and detoxification of cyanide in gold mine tailings: A review, Waste Manag. Res. 37 (2019) 1117–1126.
[23] S.A. Wadhwani, U.U. Shedbalkar, R. Singh, P. Vashisth, V. Pruthi, B.A. Chopade, Kinetics of synthesis of gold nanoparticles by Acinetobacter sp. SW30 isolated from environment, Indian J. Microbiol. 56 (2016) 439–444.
[24] A. Rónavári, N. Igaz, D.I. Adamecz, B. Szerencsés, C. Molnar, Z. Kónya, I. Pfeiffer, M. Kiricsi, Green silver and gold nanoparticles: Biological synthesis approaches and potentials for biomedical applications, Molecules. 26 (2021) 844.
[25] A.A. Elkhawaga, M.M. Khalifa, O. El-Badawy, M.A. Hassan, W.A. El-Said, Rapid and highly sensitive detection of pyocyanin biomarker in different Pseudomonas aeruginosa infections using gold nanoparticles modified sensor, PLoS One. 14 (2019) e0216438.
[26] S. Samanta, S. Agarwal, K.K. Nair, R.A. Harris, H. Swart, Biomolecular assisted synthesis and mechanism of silver and gold nanoparticles, Mater. Res. Express. 6 (2019) 82009.
[27] J. Li, T.J. Webster, B. Tian, Functionalized nanomaterial assembling and biosynthesis using the extremophile Deinococcus radiodurans for multifunctional applications, Small. 15 (2019) 1900600.
[28] J. Li, Q. Li, X. Ma, B. Tian, T. Li, J. Yu, S. Dai, Y. Weng, Y. Hua, Biosynthesis of gold nanoparticles by the extreme bacterium Deinococcus radiodurans and an evaluation of their antibacterial properties, Int. J. Nanomedicine. (2016) 5931–5944.
[29] D. Jain, Shivani, A.A. Bhojiya, H. Singh, H.K. Daima, M. Singh, S.R. Mohanty, B.J. Stephen, A. Singh, Microbial fabrication of zinc oxide nanoparticles and evaluation of their antimicrobial and photocatalytic properties, Front. Chem. 8 (2020) 778.
[30] H. Mohd Yusof, N. Abdul Rahman, R. Mohamad, U.H. Zaidan, A.A. Samsudin, Biosynthesis of zinc oxide nanoparticles by cell-biomass and supernatant of Lactobacillus plantarum TA4 and its antibacterial and biocompatibility properties, Sci. Rep. 10 (2020) 19996.
[31] C. Jayaseelan, A.A. Rahuman, A.V. Kirthi, S. Marimuthu, T. Santhoshkumar, A. Bagavan, K. Gaurav, L. Karthik, K.V.B. Rao, Novel microbial route to synthesize ZnO nanoparticles using Aeromonas hydrophila and their activity against pathogenic bacteria and fungi, Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 90 (2012) 78–84.
[32] M. Alavi, M. Moradi, Different antibacterial and photocatalyst functions for herbal and bacterial synthesized silver and copper/copper oxide nanoparticles/nanocomposites: A review, Inorg. Chem. Commun. 142 (2022) 109590.
[33] M. Fatemi, N. Mollania, M. Momeni-Moghaddam, F. Sadeghifar, Extracellular biosynthesis of magnetic iron oxide nanoparticles by Bacillus cereus strain HMH1: Characterization and in vitro cytotoxicity analysis on MCF-7 and 3T3 cell lines, J. Biotechnol. 270 (2018) 1–11.
[34] S. Kumari, N. Tehri, A. Gahlaut, V. Hooda, Actinomycetes mediated synthesis, characterization, and applications of metallic nanoparticles, Inorg. Nano-Metal Chem. 51 (2020) 1386–1395.
[35] B.R. Singh, S. Dwivedi, A.A. Al-Khedhairy, J. Musarrat, Synthesis of stable cadmium sulfide nanoparticles using surfactin produced by Bacillus amyloliquifaciens strain KSU-109, Colloids Surfaces B Biointerfaces. 85 (2011) 207–213.
[36] S.S. Abd Elsalam, R.H. Taha, A.M. Tawfeik, A. El-Monem, O. Mohamed, H.A. Mahmoud, Antimicrobial activity of bio and chemical synthesized cadmium sulfide nanoparticles, Egypt. J. Hosp. Med. 70 (2018) 1494–1507.
[37] S. Ghosh, R. Ahmad, M. Zeyaullah, S.K. Khare, Microbial nano-factories: synthesis and biomedical applications, Front. Chem. 9 (2021) 626834.
[38] D. Medina Cruz, G. Mi, T.J. Webster, Synthesis and characterization of biogenic selenium nanoparticles with antimicrobial properties made by Staphylococcus aureus, methicillin‐resistant Staphylococcus aureus (MRSA), Escherichia coli, and Pseudomonas aeruginosa, J. Biomed. Mater. Res. Part A. 106 (2018) 1400–1412.
[39] M.A. Abostate, Y. Saleh, H. Mira, M. Amin, M. Al Kazindar, B.M. Ahmed, Characterization, kinetics and thermodynamics of biosynthesized uranium nanoparticles (UNPs), Artif. Cells, Nanomedicine, Biotechnol. 46 (2018) 147–159.
[40] R.A. Hamouda, M.H. Hussein, R.A. Abo-Elmagd, S.S. Bawazir, Synthesis and biological characterization of silver nanoparticles derived from the cyanobacterium Oscillatoria limnetica, Sci. Rep. 9 (2019) 13071.
[41] S. Husain, S. Afreen, D. Yasin, B. Afzal, T. Fatma, Cyanobacteria as a bioreactor for synthesis of silver nanoparticles-an effect of different reaction conditions on the size of nanoparticles and their dye decolorization ability, J. Microbiol. Methods. 162 (2019) 77–82.
[42] R.S. Hamida, N.E. Abdelmeguid, M.A. Ali, M.M. Bin-Meferij, M.I. Khalil, Synthesis of silver nanoparticles using a novel cyanobacteria Desertifilum sp. extract: Their antibacterial and cytotoxicity effects, Int. J. Nanomedicine. (2020) 49–63.
[43] S. Al Rashed, S. Al Shehri, N.M.S. Moubayed, Extracellular biosynthesis of silver nanoparticles from Cyanobacteria, Biomed. Res. 29 (2018) 2859–2862.
[44] R.S. Hamida, M.A. Ali, A. Redhwan, M.M. Bin-Meferij, Cyanobacteria–a promising platform in green nanotechnology: a review on nanoparticles fabrication and their prospective applications, Int. J. Nanomedicine. 15 (2020) 6033–6066.
[45] C.P. Mandhata, C.R. Sahoo, R.N. Padhy, Biomedical applications of biosynthesized gold nanoparticles from cyanobacteria: An overview, Biol. Trace Elem. Res. 200 (2022) 5307–5327.
[46] K. AbdelRahim, S.Y. Mahmoud, A.M. Ali, K.S. Almaary, A.E.-Z.M.A. Mustafa, S.M. Husseiny, Extracellular biosynthesis of silver nanoparticles using Rhizopus stolonifer, Saudi J. Biol. Sci. 24 (2017) 208–216.
[47] T. Mabey, D. Andrea Cristaldi, P. Oyston, K.P. Lymer, E. Stulz, S. Wilks, C. William Keevil, X. Zhang, Bacteria and nanosilver: the quest for optimal production, Crit. Rev. Biotechnol. 39 (2019) 272–287.
[48] M.R. AbdelGawwad, E. Mahmutović, D.A. Al Farraj, M.S. Elshikh, In silico prediction of silver nitrate nanoparticles and Nitrate Reductase A (NARA) interaction in the treatment of infectious disease causing clinical strains of E. coli, J. Infect. Public Health. 13 (2020) 1580–1585.
[49] Z.-Y. Yan, Q.-Q. Du, J. Qian, D.-Y. Wan, S.-M. Wu, Eco-friendly intracellular biosynthesis of CdS quantum dots without changing Escherichia coli’s antibiotic resistance, Enzyme Microb. Technol. 96 (2017) 96–102.
[50] J. Sun, G. Liu, S. Fu, F. Cai, H. Yin, H. Lv, J. He, Gold Nanoparticles of Multiple Shapes Synthesized in L-Tryptophan Aqueous Solution, Trans. Tianjin Univ. 24 (2018) 401–414.
[51] A.B.A. Mohammed, A.E. Hegazy, A. Salah, Novelty of synergistic and cytotoxicity activities of silver nanoparticles produced by Lactobacillus acidophilus, Appl. Nanosci. 13 (2023) 633–640.
[52] X. Fang, Y. Wang, Z. Wang, Z. Jiang, M. Dong, Microorganism assisted synthesized nanoparticles for catalytic applications, Energies. 12 (2019) 190.
[53] N.M. Abdelmaksoud, H.A. El-Mahdy, A. Ismail, E.G.E. Elsakka, A.A. El-Husseiny, E.G. Khidr, E.M. Ali, M.H. Rashed, F.E.-S. El-Demerdash, A.S. Doghish, The role of miRNAs in the pathogenesis and therapeutic resistance of endometrial cancer:
a spotlight on the convergence of signaling pathways, Pathol. Pract. 244 (2023) 154411.
[54] Z. Zhou, S. Peng, M. Sui, S. Chen, L. Huang, H. Xu, T. Jiang, Multifunctional nanocomplex for surface-enhanced Raman scattering imaging and near-infrared photodynamic antimicrobial therapy of vancomycin-resistant bacteria, Colloids Surfaces B Biointerfaces. 161 (2018) 394–402.
[55] T. Li, L. Gao, B. Zhang, G. Nie, Z. Xie, H. Zhang, H. Ågren, Material-based engineering of bacteria for cancer diagnosis and therapy, Appl. Mater. Today. 25 (2021) 101212.
[56] A. Arabzadeh, T. Mortezazadeh, T. Aryafar, E. Gharepapagh, M. Majdaeen, B. Farhood, Therapeutic potentials of resveratrol in combination with radiotherapy and chemotherapy during glioblastoma treatment: a mechanistic review, Cancer Cell Int. 21 (2021) 1–15.
[57] M. Miola, C. Multari, E. Vernè, Iron Oxide-Au Magneto-Plasmonic Heterostructures: Advances in Their Eco-Friendly Synthesis, Materials (Basel). 15 (2022) 7036.
[58] M.A. Tahir, N.E. Dina, H. Cheng, V.K. Valev, L. Zhang, Surface-enhanced Raman spectroscopy for bioanalysis and diagnosis, Nanoscale. 13 (2021) 11593–11634.
[59] K. Khanna, S.K. Kohli, P. Bakshi, P. Sharma, J. Kour, T. Bhardwaj, N. Sharma, N. Dogra, P. Ohri, G. Sirhindi, Green biosynthesis of nanoparticles: mechanistic aspects and applications, in: Environ. Appl. Microb. Nanotechnol., Elsevier, 2023: pp. 99–126.
[60] M. Farokhi, F. Mottaghitalab, M.R. Saeb, S. Thomas, Functionalized theranostic nanocarriers with bio-inspired polydopamine for tumor imaging and chemo-photothermal therapy, J. Control. Release. 309 (2019) 203–219.
[61] N.S. Alsaiari, F.M. Alzahrani, A. Amari, H. Osman, H.N. Harharah, N. Elboughdiri, M.A. Tahoon, Plant and microbial approaches as green methods for the synthesis of nanomaterials: Synthesis, applications, and future perspectives, Molecules. 28 (2023) 463.
[62] A. Panáček, L. Kvítek, M. Smékalová, R. Večeřová, M. Kolář, M. Röderová, F. Dyčka, M. Šebela, R. Prucek, O. Tomanec, Bacterial resistance to silver nanoparticles and how to overcome it, Nat. Nanotechnol. 13 (2018) 65–71.
[63] M.S. Alsaggaf, A.F. Elbaz, S. El-baday, S.H. Moussa, Anticancer and antibacterial activity of cadmium sulfide nanoparticles by Aspergillus niger, Adv. Polym. Technol. 2020 (2020) 1–13.
[64] R. Chang, L. Chen, M. Qamar, Y. Wen, L. Li, J. Zhang, X. Li, E. Assadpour, T. Esatbeyoglu, M.S. Kharazmi, The bioavailability, metabolism and microbial modulation of curcumin-loaded nanodelivery systems, Adv. Colloid Interface Sci. 318 (2023) 102933.
[65] H.N. Nguyen, S. Romero Jovel, T.H.K. Nguyen, Nanosized minicells generated by lactic acid bacteria for drug delivery, J. Nanomater. 2017 (2017) 1–10.
[66] F. Maiyo, M. Singh, Selenium nanoparticles: Potential in cancer gene and drug delivery, Nanomedicine. 12 (2017) 1075–1089.
[67] D. McCloskey, S. Xu, T.E. Sandberg, E. Brunk, Y. Hefner, R. Szubin, A.M. Feist, B.O. Palsson, Evolution of gene knockout strains of E. coli reveal regulatory architectures governed by metabolism, Nat. Commun. 9 (2018) 3796.
[68] F. Paladini, M. Pollini, Antimicrobial silver nanoparticles for wound healing application: progress and future trends, Materials (Basel). 12 (2019) 2540.
[69] T.I. Shaheen, M.S. El-Gamal, S.E. Desouky, S.E.D. Hassan, A.M. Alemam, Benign production of AgNPs/bacterial nanocellulose for wound healing dress: antioxidant, cytotoxicity and in vitro studies, J. Clust. Sci. 33 (2021) 1–17.
[70] R.S. Darweesh, N.M. Ayoub, S. Nazzal, Gold nanoparticles and angiogenesis: Molecular mechanisms and biomedical applications, Int. J. Nanomedicine. 14 (2019) 7643–7663.
[71] A. Fouda, S.E.-D. Hassan, A.M. Eid, M.A. Awad, K. Althumayri, N.F. Badr, M.F. Hamza, Endophytic bacterial strain, Brevibacillus brevis-mediated green synthesis of copper oxide nanoparticles, characterization, antifungal, in vitro cytotoxicity, and larvicidal activity, Green Process. Synth. 11 (2022) 931–950.
[72] D. Bhattacharya, B. Ghosh, M. Mukhopadhyay, Development of nanotechnology for advancement and application in wound healing: A review, IET Nanobiotechnology. 13 (2019) 778–785.