Abstract
Recombinant Escherichia coli (E. coli) strain that produces phytochelatin (PC) and/or metallothionein (MT) can synthesize various metal nanoparticles (NPs) by reducing metal ions. Here we report in vivo biosynthesis of iron oxide nanocomposites (NCs) using recombinant E. coli. We designed a strategy of biosynthesizing iron oxide NCs by first internalizing chemically synthesized iron oxide NPs, followed by the reduction of added metal ions on the surface of internalized NPs by PC and/or MT in E. coli. For this, chemically synthesized Fe3O4 NPs were internalized by recombinant E. coli, and then, Au and Ag ions were added for the biosynthesis of AuFe3O4 and AgFe3O4 NCs, respectively. The NCs synthesized were analyzed by transmission electron microscopy, UV–vis spectrophotometry, and X-ray diffractometry to characterize their shape, optical property, and crystallinity. The Fe3O4 NPs in the biosynthesized NCs allowed easy purification of the biosynthesized NCs by applying a magnetic field. The AuFe3O4 NCs were used for enzyme-linked immunosorbent assay to detect prostate-specific antigen protein, while AgFe3O4 NCs were utilized for the antimicrobial application with low minimum inhibitory concentration. As recombinant E. coli can uptake and reduce various NPs and metal ions, biosynthesis of a wide range of NCs as new nanomaterials will be possible for diverse applications.
Key points
• AuFe3O4 and AgFe3O4 nanocomposites were synthesized by recombinant E. coli.
• Escherichia coli synthesized different iron oxide NCs depending on the metal ions to be added.
• Biosynthesized AuFe3O4 NC was used for ELISA and AgFe3O4 NC for antimicrobial tests.
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Additional information is provided in the Supplementary Information.
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References
Bell G, Bogart LK, Southern P, Olivo M, Pankhurst QA, Parkin IP (2017) Enhancing the magnetic heating capacity of iron oxide nanoparticles through their postproduction incorporation into iron oxide-gold nanocomposites. Eur J Inorg Chem 18:2386–2395. https://doi.org/10.1002/ejic.201601432
Chang SH, Yang PY, Lai CM, Lu SC, Li GA, Chang WC, Tuan HY (2016) Synthesis of Cu/ZnO core/shell nanocomposites and their use as efficient photocatalysts. Cryst Eng Comm 18(4):616–621. https://doi.org/10.1039/C5CE01944C
Chen M, Zhang L, Gao M, Zhang X (2017) High-sensitive bioorthogonal SERS tag for live cancer cell imaging by self-assembling core-satellites structure gold-silver nanocomposite. Talanta 172:176–181. https://doi.org/10.1016/j.talanta.2017.05.033
Choi Y, Lee SY (2020) Biosynthesis of inorganic nanomaterials using microbial cells and bacteriophages. Nat Rev Chem 4:638–656. https://doi.org/10.1038/s41570-020-00221-w
Choi Y, Hwang JH, Lee SY (2018a) Recent trends in nanomaterials-based colorimetric detection of pathogenic bacteria and viruses. Small Methods 2(4):1700351. https://doi.org/10.1002/smtd.201700351
Choi Y, Park TJ, Lee DC, Lee SY (2018b) Recombinant Escherichia coli as a biofactory for various single- and multi-element nanomaterials. PNAS 115(23):5944–5949. https://doi.org/10.1073/pnas.1804543115
Cui W, Li J, Zhang Y, Rong H, Lu W, Jiang L (2012) Effects of aggregation and the surface properties of gold nanoparticles on cytotoxicity and cell growth. Nanomedicine 8(1):46–53. https://doi.org/10.1016/j.nano.2011.05.005
Guo S, Lakshmipriya T, Gopinath SC, Anbu P, Feng Y (2019) Complementation of ELISA and an interdigitated electrode surface in gold nanoparticle functionalization for effective detection of human blood clotting defects. Nanoscale Res Lett 14(1):1–10. https://doi.org/10.1186/s11671-019-3058-z
Jeong Y, Kook YM, Lee K, Koh WG (2018) Metal enhanced fluorescence (MEF) for biosensors: general approaches and a review of recent developments. Biosens Bioelectron 111:102–116. https://doi.org/10.1016/j.bios.2018.04.007
Jung JH, Park TJ, Lee SY, Seo TS (2012) Homogeneous biogenic paramagnetic nanoparticle synthesis based on a microfluidic droplet generator. Angew Chem Int Ed 51(23):5634–5637. https://doi.org/10.1002/anie.201108977
Jung JH, Lee SY, Seo TS (2018) In vivo synthesis of nanocomposites using the recombinant Escherichia coli. Small 14(42):1803133. https://doi.org/10.1002/smll.201803133
Karthiga P, Rajeshkumar S, Annadurai G (2018) Mechanism of larvicidal activity of antimicrobial silver nanoparticles synthesized using Garcinia mangostana bark extract. J Clust Sci 29(6):1233–1241. https://doi.org/10.1007/s10876-018-1441-z
Kubo AL, Capjak I, Vrček IV, Bondarenko OM, Kurvet I, Vija H, Ivask A, Kasemets K, Kahru A (2018) Antimicrobial potency of differently coated 10 and 50 nm silver nanoparticles against clinically relevant bacteria Escherichia coli and Staphylococcus aureus. Colloids Surf B 170:401–410. https://doi.org/10.1016/j.colsurfb.2018.06.027
Lakshmipriya T, Gopinath SC, Hashim U, Tang TH (2016) Signal enhancement in ELISA: Biotin-streptavidin technology against gold nanoparticles. J Taibah Univ Medical Sci 11(5):432–438. https://doi.org/10.1016/j.jtumed.2016.05.010
Le Ouay B, Stellacci F (2015) Antibacterial activity of silver nanoparticles: a surface science insight. Nano Today 10(3):339–354. https://doi.org/10.1016/j.nantod.2015.04.002
Liu Z, Zhao B, Shi Y, Guo C, Yang H, Li Z (2010) Novel nonenzymatic hydrogen peroxide sensor based on iron oxide-silver hybrid submicrospheres. Talanta 81(4–5):1650–1654. https://doi.org/10.1016/j.talanta.2010.03.019
Ma J, Du Q, Ge H, Zhang Q (2019) Fabrication of core–shell TiO2@ CuS nanocomposite via a bifunctional linker-assisted synthesis and its photocatalytic performance. J Mater Sci 54(4):2928–2939. https://doi.org/10.1007/s10853-018-3054-1
Markova Z, Siskova K, Filip J, Safarova K, Prucek R, Panacek A, Kolar M, Zboril R (2012) Chitosan-based synthesis of magnetically-driven nanocomposites with biogenic magnetite core, controlled silver size, and high antimicrobial activity. Green Chem 14(9):2550–2558. https://doi.org/10.1039/C2GC35545K
Martínez-Mera I, Espinosa-Pesqueira ME, Pérez-Hernández R, Arenas-Alatorre J (2007) Synthesis of magnetite (Fe3O4) nanoparticles without surfactants at room temperature. Mater Lett 61(23–24):4447–4451. https://doi.org/10.1016/j.matlet.2007.02.018
Paladini F, Pollini M (2019) Antimicrobial silver nanoparticles for wound healing application: progress and future trends. Materials 12(16):2540. https://doi.org/10.3390/ma12162540
Panacek A, Kvitek L, Prucek R, Kolar M, Vecerova R, Pizurova N, Sharma VK, Nevecna T, Zboril R (2006) Silver colloid nanoparticles: synthesis, characterization, and their antibacterial activity. J Phys Chem B 110(33):16248–16253. https://doi.org/10.1021/jp063826h
Park TJ, Lee SY, Heo NS, Seo TS (2010) In vivo synthesis of diverse metal nanoparticles by recombinant Escherichia coli. Angew Chem Int Ed 49(39):7019–7024. https://doi.org/10.1002/anie.201001524
Pazos E, Sleep E, Rubert Pérez CM, Lee SS, Tantakitti F, Stupp SI (2016) Nucleation and growth of ordered arrays of silver nanoparticles on peptide nanofibers: hybrid nanostructures with antimicrobial properties. J Am Chem Soc 138(17):5507–5510. https://doi.org/10.1021/jacs.6b01570
Prabhawathi V, Sivakumar PM, Boobalan T, Manohar CM, Doble M (2019) Design of antimicrobial polycaprolactam nanocomposite by immobilizing subtilisin conjugated Au/Ag core-shell nanoparticles for biomedical applications. Mater Sci Eng: C 94:656–665. https://doi.org/10.1016/j.msec.2018.10.020
Prucek R, Tucek J, Kilianova M, Panacek A, Kvitek L, Filip J, Kolar M, Tomankova K, Zboril R (2011) The targeted antibacterial and antifungal properties of magnetic nanocomposite of iron oxide and silver nanoparticles. Biomaterials 32(21):4704–4713. https://doi.org/10.1016/j.biomaterials.2011.03.039
Ramalingmam P, Muthukrishnan S, Thangaraj P (2015) Biosynthesis of silver nanoparticles using an endophytic fungus, Curvularialunata and its antimicrobial potential. J Nanosci Nanoeng 1(4):241–247
Ranoszek-Soliwoda K, Tomaszewska E, Małek K, Celichowski G, Orlowski P, Krzyzowska M, Grobelny J (2019) The synthesis of monodisperse silver nanoparticles with plant extracts. Colloids Surf B 177:19–24. https://doi.org/10.1016/j.colsurfb.2019.01.037
Shin HY, Kim BG, Cho S, Lee J, Na HB, Kim MI (2017) Visual determination of hydrogen peroxide and glucose by exploiting the peroxidase-like activity of magnetic nanoparticles functionalized with a poly(ethylene glycol) derivative. Microchim Acta 184(7):2115–2122. https://doi.org/10.1007/s00604-017-2198-z
Trang VT, Van Quy N, Huy TQ, Thuy NT, Tri DQ, Cuong ND, Tuan PA, Van Tuan H, Le A-T, Phan VN (2017) Functional iron oxide–silver hetero-nanocomposites: controlled synthesis and antibacterial activity. J Electron Mater 46(6):3381–3389. https://doi.org/10.1007/s11664-017-5314-2
Vallabani NVS, Karakoti AS, Singh S (2017) ATP-mediated intrinsic peroxidase-like activity of Fe3O4-based nanozyme: one step detection of blood glucose at physiological pH. Colloids Surf B Biointerfaces 153:52–60. https://doi.org/10.1016/j.colsurfb.2017.02.004
Woo MA, Kim MI, Jung JH, Park KS, Seo TS, Park HG (2013) A novel colorimetric immunoassay utilizing the peroxidase mimicking activity of magnetic nanoparticles. Int J Mol Sci 14(5):9999–10014. https://doi.org/10.3390/ijms14059999
Yu X, Marks TJ, Facchetti A (2016) Metal oxides for optoelectronic applications. Nat Mater 15(4):383–396. https://doi.org/10.1038/nmat4599
Zhang HZ, Zhang C, Zeng GM, Gong JL, Ou XM, Huan SY (2016) Easily separated silver nanoparticle-decorated magnetic graphene oxide: Synthesis and high antibacterial activity. J Colloid Interface Sci 471:94–102. https://doi.org/10.1016/j.jcis.2016.03.015
Zhang J, Wang L, Zhang B, Zhao H, Kolb U, Zhu Y, Liu L, Han Y, Wang G, Wang C, Su DS, Gates BC, Xiao FS (2018) Sinter-resistant metal nanoparticle catalysts achieved by immobilization within zeolite crystals via seed-directed growth. Nat Catal 1(7):540–546. https://doi.org/10.1038/s41929-018-0098-1
Zhao J, Dong WF, Zhang XD, Chai HX, Huang YM (2018) FeNPs@Co3O4 hollow nanocages hybrids as effective peroxidase mimics for glucose biosensing. Sens Actuators B Chem 263:575–584. https://doi.org/10.1016/j.snb.2018.02.151
Acknowledgements
We thank Dr. Yoojin Choi and Ms. Ji Hye Hyun for their helpful discussion.
Funding
The work was supported by the Bio and Medical Technology Development Program (Grant 2021M3A9I4022740) from the Ministry of Science and ICT (MSIT) through the National Research Foundation of Korea. This work was supported by the Engineering Research Center of Excellence Program of Korea Ministry of Science, ICT & Future Planning (MSIP)/National Research Foundation of Korea (NRF) (2021R1A5A6002853); National Research Foundation of Korea (NRF); and The Ministry of Science and ICT (MSIT) (2020R1A2C1003960). This research was supported by the Main Research Program (E0210701-01) of the Korea Food Research Institute funded by the Ministry of Science and ICT of South Korea.
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J.H.J. and M.J. performed experiments. J.H.J. and T.S.S. designed the study. J.H.J., T.S.S., and S.Y.L. wrote and revised the manuscript. All authors discussed the results and commented on the manuscript.
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Jung, J.H., Cho, M., Seo, T.S. et al. Biosynthesis and applications of iron oxide nanocomposites synthesized by recombinant Escherichia coli. Appl Microbiol Biotechnol 106, 1127–1137 (2022). https://doi.org/10.1007/s00253-022-11779-4
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DOI: https://doi.org/10.1007/s00253-022-11779-4