Two Birds with One Stone Strategy for Controlling Environmental Antibiotic Resistance: Dual Function of Magnetic Nanosilver in Inhibiting Multidrug-Resistant Bacteria and Catalyzing Antibiotic Degradation
Publication: Journal of Environmental Engineering
Volume 148, Issue 11
Abstract
Antibiotic resistance has become a complicated environmental problem. Controlling the emission of antibiotics, antibiotic-resistant bacteria (ARB), and their antibiotic-resistance genes (ARGs) at hotspots is important for reducing environmental antibiotic resistance. Here, a (PDA)-Ag nanocomposite was successfully fabricated via hydrothermal synthesis, polydopamine coating, and in situ Ag reduction. The nanocomposite exhibited a core-shell structure with a nanosized magnetic core () coated with one layer of nanosilver Ag nanoparticles (Ag NPs) decorated polydopamine. Its application potential as a bifunctional material for the removal of multidrug-resistant (MDR) bacteria, ARGs, and antibiotics was investigated. The showed a good performance on inhibiting the MDR bacteria and effectively reduced the abundance of ARGs. The removal of ciprofloxacin (CIP) via catalytic reduction with this composite was evaluated. The optimized results showed that nearly 82.3% of CIP () was removed within 30 min with the amount of of and the concentration of of 10 mM. Furthermore, the catalytic activity of the composite did not decrease even after five cycles, indicating its good reusability as the catalyst. This study provided a preliminary two birds with one stone strategy for solving the environmental problem of antibiotic-resistance pollution.
Practical Applications
Antibiotic resistance has become a comprehensive and complicated environmental pollution problem. The selective pressure exerted by antibiotics and the proliferation of ARB and ARGs can promote the bloom of environmental antibiotic resistance. Single control of the emission of a certain kind of pollutant (antibiotics, ARB, or ARGs) at hotspots will not effectively solve the environmental pollution problem of antibiotic resistance. Here, we provided a one stone, two birds strategy for solving this problem of environmental antibiotic resistance in virtue of the dual function of a magnetic nanosilver composite in inhibiting multidrug-resistant bacteria and catalyzing antibiotic degradation.
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Data Availability Statement
All data, models, and code generated or used during the study appear in the published article.
Acknowledgments
This work was funded by the National Natural Science Foundation of China (Nos. 21677104 and 22176133).
References
Abramenko, N. B., T. B. Demidova, E. V. Abkhalimov, B. G. Ershov, E. Y. Krysanov, and L. M. Kustov. 2018. “Ecotoxicity of different-shaped silver nanoparticles: Case of zebrafish embryos.” J. Hazard. Mater. 347 (Dec): 89–94. https://doi.org/10.1016/j.jhazmat.2017.12.060.
Alhokbany, N. S., R. Mousa, M. Naushad, S. M. Alshehri, and T. Ahamad. 2020. “Fabrication of Z-scheme photocatalysts g-/chitosan for the photocatalytic degradation of ciprofloxacin.” Int. J. Biol. Macromol. 164 (Aug): 3864–3872. https://doi.org/10.1016/j.ijbiomac.2020.08.133.
Amarjargal, A., L. D. Tijing, I.-T. Im, and C. S. Kim. 2013. “Simultaneous preparation of Ag/ core–shell nanocomposites with enhanced magnetic moment and strong antibacterial and catalytic properties.” Chem. Eng. J. 226 (Aug): 243–254. https://doi.org/10.1016/j.cej.2013.04.054.
Andersson, D. I., and D. Hughes. 2010. “Antibiotic resistance and its cost: Is it possible to reverse resistance?” Nat. Rev. Microbiol. 8 (4): 260–271. https://doi.org/10.1038/nrmicro2319.
Baby, T. T., and S. Ramaprabhu. 2010. “ coated magnetic nanoparticle dispersed multiwalled carbon nanotubes based amperometric glucose biosensor.” Talanta 80 (5): 2016–2022. https://doi.org/10.1016/j.talanta.2009.11.010.
Chamosa, L. S., V. E. Alvarez, M. Nardelli, M. P. Quiroga, M. H. Cassini, and D. Centron. 2017. “Lateral antimicrobial resistance genetic transfer is active in the open environment.” Sci. Rep. 7 (1): 513. https://doi.org/10.1038/s41598-017-00600-2.
Chen, X., Z. Wang, S. Bi, K. Li, R. Du, and C. Wu. 2016. “Combining catalysis and separation on a PVDF/Ag composite membrane allows timely separation of products during reaction process.” Chem. Eng. J. 295 (Aug): 518–529. https://doi.org/10.1016/j.cej.2016.03.043.
Cheng, C., S. Li, W. Zhao, Q. Wei, S. Nie, and S. Sun. 2012. “The hydrodynamic permeability and surface property of polyethersulfone ultrafiltration membranes with mussel-inspired polydopamine coatings.” J. Membr. Sci. 417–418 (May): 228–236. https://doi.org/10.1016/j.memsci.2012.06.045.
Chi, Y., Q. Yuan, Y. Li, J. Tu, L. Zhao, and N. Li. 2012. “Synthesis of -Ag magnetic nanocomposite based on small-sized and highly dispersed silver nanoparticles for catalytic reduction of 4-nitrophenol.” J. Colloid Interface Sci. 383 (1): 96–102. https://doi.org/10.1016/j.jcis.2012.06.027.
Cui, K., B. Yan, Y. Xie, H. Qian, X. Wang, and Q. Huang. 2018. “Regenerable urchin-like -Ag hollow microspheres as catalyst and adsorbent for enhanced removal of organic dyes.” J. Hazard. Mater. 350 (2): 66–75. https://doi.org/10.1016/j.jhazmat.2018.02.011.
D’Costa, V. M., K. M. McGrann, D. W. Hughes, and G. D. Wright. 2006. “Sampling the antibiotic resistome.” Science 311 (5759): 374–377. https://doi.org/10.1126/science.1120800.
Deng, H., X. Li, Q. Peng, X. Wang, J. Chen, and Y. Li. 2005. “Monodisperse magnetic single-crystal ferrite microspheres.” Angew. Chem. Int. Ed. 44 (18): 2782–2785. https://doi.org/10.1002/anie.200462551.
Devi, A. P., D. K. Padhi, P. M. Mishra, and A. K. Behera. 2021. “Bio-Surfactant assisted room temperature synthesis of cubic Ag/RGO nanocomposite for enhanced photoreduction of Cr (VI) and antibacterial activity.” J. Environ. Chem. Eng. 9 (2): 104778. https://doi.org/10.1016/j.jece.2020.104778.
Forsberg, K. J., A. Reyes, B. Wang, E. M. Selleck, M. O. Sommer, and G. Dantas. 2012. “The shared antibiotic resistome of soil bacteria and human pathogens.” Science 337 (6098): 1107–1111. https://doi.org/10.1126/science.1220761.
Hernando-Amado, S., T. M. Coque, F. Baquero, and J. L. Martinez. 2019. “Defining and combating antibiotic resistance from One Health and Global Health perspectives.” Nat. Microbiol. 4 (9): 1432–1442. https://doi.org/10.1038/s41564-019-0503-9.
Holbrook, K. 1971. “Hydrolysis of the borohydride ion catalysed by metal-boron alloys.” J. Chem. Soc. A 90 (9): 890–894. https://doi.org/10.1039/J19710000890.
Jana, N. R., T. K. Sau, and T. Pal. 1999. “Growing small silver particle as redox catalyst.” J. Phys. Chem. B 103 (1): 115–121. https://doi.org/10.1021/jp982731f.
Jeon, K. E., E. Seo, and L. Eunhee. 2013. “Mussel-inspired green synthesis of silver nanoparticles on graphene oxide nanosheets for enhanced catalytic applications.” Chem. Commun. 49 (33): 3392–3394. https://doi.org/10.1039/c3cc00115f.
Karki, H. P., D. P. Ojha, M. K. Joshi, and H. J. Kim. 2018. “Effective reduction of p-nitrophenol by silver nanoparticle loaded on magnetic nano-composite.” Appl. Surf. Sci. 435 (Mar): 599–608. https://doi.org/10.1016/j.apsusc.2017.11.166.
Karkman, A., K. Parnanen, and D. G. J. Larsson. 2019. “Fecal pollution can explain antibiotic resistance gene abundances in anthropogenically impacted environments.” Nat. Commun. 10 (1): 80. https://doi.org/10.1038/s41467-018-07992-3.
Khin, M. M., A. S. Nair, V. J. Babu, R. Murugan, and S. Ramakrishna. 2012. “A review on nanomaterials for environmental remediation.” Energy Environ. Sci. 5 (8): 8075–8109. https://doi.org/10.1039/c2ee21818f.
Knapp, C. W., J. Dolfing, P. A. Ehlert, and D. W. Graham. 2010. “Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940.” Environ. Sci. Technol. 44 (2): 580–587. https://doi.org/10.1021/es901221x.
Kumar, S. R., L. Marianna, S. Gianni, A. J. Nathanael, S. I. Hong, and T. H. Oh. 2014. “Hydrophilic polymer coated monodispersed nanostructures and their cytotoxicity.” Mater. Res. Express 1 (1): 015015. https://doi.org/Artn015015.
Lee, H., D. H. Lee, J. M. Ha, and D. H. Kim. 2018. “Plasma assisted oxidative coupling of methane (OCM) over and subsequent regeneration at low temperature.” Appl. Catal. A 557 (14): 39–45. https://doi.org/10.1016/j.apcata.2018.03.007.
Lee, K., D. W. Kim, D. H. Lee, Y. S. Kim, J. H. Bu, and J. H. Cha. 2020. “Mobile resistome of human gut and pathogen drives anthropogenic bloom of antibiotic resistance.” Microbiome 8 (1): 2. https://doi.org/10.1186/s40168-019-0774-7.
Li, Y., Y. Wang, H. Lu, and X. Li. 2020. “Preparation of –P4VP@Ag NPs as effective and recyclable catalysts for the degradation of organic pollutants with in water.” Int. J. Hydrogen Energy 45 (32): 16080–16093. https://doi.org/10.1016/j.ijhydene.2020.04.002.
Lin, Y., X. Dong, J. Wu, D. Rao, L. Zhang, and Y. Faraj. 2020. “Metadata analysis of MCR-1-bearing plasmids inspired by the sequencing evidence for horizontal transfer of antibiotic resistance genes between polluted river and wild birds.” Front. Microbiol. 11 (5): 352. https://doi.org/10.3389/fmicb.2020.00352.
Liu, W., T. He, Y. Wang, G. Ning, Z. Xu, and X. Chen. 2020. “Synergistic adsorption-photocatalytic degradation effect and norfloxacin mechanism of ZnO/ZnS@BC under UV-light irradiation.” Sci. Rep. 10 (1): 11903. https://doi.org/10.1038/s41598-020-68517-x.
Liu, Y. Y., Y. Wang, T. R. Walsh, L. X. Yi, R. Zhang, and J. Spencer. 2016. “Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: A microbiological and molecular biological study.” Lancet Infect. Dis. 16 (2): 161–168. https://doi.org/10.1016/S1473-3099(15)00424-7.
Mao, H., C. Ji, M. Liu, Z. Cao, D. Sun, and Z. Xing. 2018. “Enhanced catalytic activity of Ag nanoparticles supported on polyacrylamide/polypyrrole/graphene oxide nanosheets for the reduction of 4-nitrophenol.” Appl. Surf. Sci. 434 (10): 522–533. https://doi.org/10.1016/j.apsusc.2017.10.209.
Michael-Kordatou, I., P. Karaolia, and D. Fatta-Kassinos. 2018. “The role of operating parameters and oxidative damage mechanisms of advanced chemical oxidation processes in the combat against antibiotic-resistant bacteria and resistance genes present in urban wastewater.” Water Res. 129 (Jun): 208–230. https://doi.org/10.1016/j.watres.2017.10.007.
Pruden, A., D. G. Larsson, A. Amezquita, P. Collignon, K. K. Brandt, and D. W. Graham. 2013. “Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment.” Environ. Health Perspect. 121 (8): 878–885. https://doi.org/10.1289/ehp.1206446.
Pruden, A., R. Pei, H. Storteboom, and K. H. Carlson. 2006. “Antibiotic resistance genes as emerging contaminants: Studies in northern Colorado.” Environ. Sci. Technol. 40 (23): 7445–7450. https://doi.org/10.1021/es060413l.
Qiao, D., Z. Li, J. Duan, and X. He. 2020. “Adsorption and photocatalytic degradation mechanism of magnetic graphene oxide/ZnO nanocomposites for tetracycline contaminants.” Chem. Eng. J. 400 (12): 125952. https://doi.org/10.1016/j.cej.2020.125952.
Rabbi, M. A., M. M. Rahman, H. Minami, N. Yamashita, M. R. Habib, and H. Ahmad. 2021. “Magnetically responsive antibacterial nanocrystalline jute cellulose nanocomposites with moderate catalytic activity.” Carbohydr. Polym. 251 (Apr): 117024. https://doi.org/10.1016/j.carbpol.2020.117024.
Rakap, M., and S. Özkar. 2012. “Hydroxyapatite-supported cobalt(0) nanoclusters as efficient and cost-effective catalyst for hydrogen generation from the hydrolysis of both sodium borohydride and ammonia-borane.” Catal. Today 183 (1): 17–25. https://doi.org/10.1016/j.cattod.2011.04.022.
Sivaselvam, S., P. Premasudha, C. Viswanathan, and N. Ponpandian. 2020. “Enhanced removal of emerging pharmaceutical contaminant ciprofloxacin and pathogen inactivation using morphologically tuned MgO nanostructures.” J. Environ. Chem. Eng. 8 (5): 104256. https://doi.org/10.1016/j.jece.2020.104256.
Sivaselvam, S., R. Selvakumar, C. Viswanathan, and N. Ponpandian. 2021. “Rapid one-pot synthesis of PAM-GO-Ag nanocomposite hydrogel by gamma-ray irradiation for remediation of environment pollutants and pathogen inactivation.” Chemosphere 275 (13): 130061. https://doi.org/10.1016/j.chemosphere.2021.130061.
Stokes, H. W., and M. R. Gillings. 2011. “Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into Gram-negative pathogens.” FEMS Microbiol. Rev. 35 (5): 790–819. https://doi.org/10.1111/j.1574-6976.2011.00273.x.
Tomitaka, A., A. Hirukawa, T. Yamada, S. Morishita, and Y. Takemura. 2009. “Biocompatibility of various ferrite nanoparticles evaluated by in vitro cytotoxicity assays using HeLa cells.” J. Magn. Magn. Mater. 321 (10): 1482–1484. https://doi.org/10.1016/j.jmmm.2009.02.058.
Van Goethem, M. W., R. Pierneef, O. K. I. Bezuidt, Y. Van De Peer, D. A. Cowan, and T. P. Makhalanyane. 2018. “A reservoir of ‘historical’ antibiotic resistance genes in remote pristine Antarctic soils.” Microbiome 6 (1): 40. https://doi.org/10.1186/s40168-018-0424-5.
Walsh, C. 2003. “Where will new antibiotics come from?” Nat. Rev. Microbiol. 1 (1): 65–70. https://doi.org/10.1038/nrmicro727.
Wang, H., J. Li, P. Huo, Y. Yan, and Q. Guan. 2016. “Preparation of /MWNTs composite photocatalysts for enhancement of ciprofloxacin degradation.” Appl. Surf. Sci. 366 (Dec): 1–8. https://doi.org/10.1016/j.apsusc.2015.12.229.
Wang, J. L., and R. Zhuan. 2020. “Degradation of antibiotics by advanced oxidation processes: An overview.” Sci. Total Environ. 701 (Jan): 135023. https://doi.org/10.1016/ARTN135023.
Wang, L., J. Luo, S. Shan, E. Crew, J. Yin, and C. Zhong. 2011. “Bacterial inactivation using silver-coated magnetic nanoparticles as functional antimicrobial agents.” Anal. Chem. 83 (22): 8688–8695. https://doi.org/10.1021/ac202164p.
Wang, W., Y. Jiang, S. Wen, L. Liu, and L. Zhang. 2012. “Preparation and characterization of polystyrene/Ag core-shell microspheres—A bio-inspired poly(dopamine) approach.” J. Colloid Interface Sci. 368 (1): 241–249. https://doi.org/10.1016/j.jcis.2011.10.047.
Wang, Y., L. He, Y. Li, L. Jing, J. Wang, and X. Li. 2020a. “Ag NPs supported on the magnetic Al-MOF/PDA as nanocatalyst for the removal of organic pollutants in water.” J. Alloys Compd. 828 (Jan): 154340. https://doi.org/10.1016/j.jallcom.2020.154340.
Wang, Y., C. Xu, R. Zhang, Y. Chen, Y. Shen, and F. Hu. 2020b. “Changes in colistin resistance and mcr-1 abundance in Escherichia coli of animal and human origins following the ban of colistin-positive additives in China: An epidemiological comparative study.” Lancet Infect. Dis. 20 (10): 1161–1171. https://doi.org/10.1016/S1473-3099(20)30149-3.
Wu, J., X. Dong, L. Zhang, Y. Lin, and K. Yang. 2021. “Reversing antibiotic resistance caused by mobile resistance genes of high fitness cost.” mSphere 6 (3): e0035621. https://doi.org/10.1128/mSphere.00356-21.
Wu, J., Y. Huang, D. Rao, Y. Zhang, and K. Yang. 2018. “Evidence for environmental dissemination of antibiotic resistance mediated by wild birds.” Front. Microbiol. 9 (18): 745. https://doi.org/10.3389/fmicb.2018.00745.
Xia, H., B. Cui, J. Zhou, L. Zhang, J. Zhang, and X. Guo. 2011. “Synthesis and characterization of @C@Ag nanocomposites and their antibacterial performance.” Appl. Surf. Sci. 257 (22): 9397–9402. https://doi.org/10.1016/j.apsusc.2011.06.016.
Xie, Y., B. Yan, H. Xu, J. Chen, Q. Liu, and Y. Deng. 2014. “Highly regenerable mussel-inspired @polydopamine-Ag core-shell microspheres as catalyst and adsorbent for methylene blue removal.” ACS Appl. Mater. Interfaces 6 (11): 8845–8852. https://doi.org/10.1021/am501632f.
Zhang, W. Z., J. F. Gao, W. J. Duan, D. Zhang, J. X. Jia, and Y. W. Wang. 2020a. “Sulfidated nanoscale zero-valent iron is an efficient material for the removal and regrowth inhibition of antibiotic resistance genes.” Environ. Pollut. 263 (Apr): 114508. https://doi.org/10.1016/j.envpol.2020.114508.
Zhang, Y., L. Wang, Z. Xiong, W. Wang, D. Zheng, and T. He. 2020b. “Removal of antibiotic resistance genes from post-treated swine wastewater by mFe/nCu system.” Chem. Eng. J. 400 (Feb): 125953. https://doi.org/10.1016/j.cej.2020.125953.
Zhao, Y., Q. Yang, X. Zhou, F.-H. Wang, J. Muurinen, and M. P. Virta. 2021. “Antibiotic resistome in the livestock and aquaculture industries: Status and solutions.” Crit. Rev. Environ. Sci. Technol. 51 (19): 2159–2196. https://doi.org/10.1080/10643389.2020.1777815.
Zhu, D., F. Zheng, Q. L. Chen, X. R. Yang, P. Christie, and X. Ke. 2018. “Exposure of a soil collembolan to Ag nanoparticles and disturbs its associated microbiota and lowers the incidence of antibiotic resistance genes in the gut.” Environ. Sci. Technol. 52 (21): 12748–12756. https://doi.org/10.1021/acs.est.8b02825.
Zhu, Y. G., Y. Zhao, D. Zhu, M. Gillings, J. Penuelas, and Y. S. Ok. 2019. “Soil biota, antimicrobial resistance and planetary health.” Environ. Int. 131 (12): 105059. https://doi.org/10.1016/j.envint.2019.105059.
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Published In
Journal of Environmental Engineering
Volume 148 • Issue 11 • November 2022
Copyright
© 2022 American Society of Civil Engineers.
History
Received: May 11, 2022
Accepted: Jun 22, 2022
Published online: Sep 7, 2022
Published in print: Nov 1, 2022
Discussion open until: Feb 7, 2023
ASCE Technical Topics:
- Animals
- Bacteria
- Birds
- Composite materials
- Continuum mechanics
- Design (by type)
- Dynamics (solid mechanics)
- Ecosystems
- Engineering fundamentals
- Engineering materials (by type)
- Engineering mechanics
- Environmental engineering
- Forces (type)
- Geology
- Geotechnical engineering
- Industrial wastes
- Load and resistance factor design
- Load factors
- Magnetic fields
- Material mechanics
- Materials engineering
- Nanomechanics
- Pollutants
- Rocks
- Solid mechanics
- Solid wastes
- Structural design
- Wastes
- Wildlife
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