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Influences and mechanisms of nanofullerene on the horizontal transfer of plasmid-encoded antibiotic resistance genes between E. coli strains

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Abstract

The spread and development of antibiotic resistance globally have led to severe public health problems. It has been shown that some non-antibiotic substances can also promote the diffusion and spread of antibiotic resistance genes (ARGs). Nanofullerene (nC60) is a type of nanomaterial widely used around the world, and some studies have discovered both the biological toxicity and environmental toxicity of nC60. In this study, cellular and molecular biology techniques were employed to investigate the influences of nC60 at sub-minimum inhibitory concentrations (sub-MICs) on the conjugation of ARGs between the E. coli strains. Compared with the control group, nC60 significantly increased the conjugation rates of ARGs by 1.32–10.82 folds within the concentration range of 7.03–1800 µg/L. This study further explored the mechanism of this phenomenon, finding that sub-MICs of nC60 could induce the production of reactive oxygen species (ROS), trigger SOS-response and oxidative stress, affect the expression of outer membrane proteins (OMPs) genes, increase membrane permeability, and thus promote the occurrence of conjugation. This research enriches our understanding of the environmental toxicity of nC60, raises our risk awareness toward nC60, and may promote the more rational employment of nC60 materials.

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References

  • Alargova R G, Deguchi S, Tsujii K (2001). Stable colloidal dispersions of fullerenes in polar organic solvents. Journal of the American Chemical Society, 123(43): 10460–10467

    Article  CAS  Google Scholar 

  • Andersson D I, Hughes D (2010). Antibiotic resistance and its cost: Is it possible to reverse resistance? Nature Reviews. Microbiology, 8(4): 260–271

    CAS  Google Scholar 

  • Andersson D I, Hughes D (2014). Microbiological effects of sublethal levels of antibiotics. Nature Reviews. Microbiology, 12(7): 465–478

    Article  CAS  Google Scholar 

  • Andrievsky G V, Klochkov V K, Karyakina E L, Mchedlov-Petrossyan N O (1999). Studies of aqueous colloidal solutions of fullerene C60 by electron microscopy. Chemical Physics Letters, 300(3–4): 392–396

    Article  CAS  Google Scholar 

  • Bezzu C G, Burt L A, Mcmonagle C J, Moggach S A, Kariuki B M, Allan D R, Warren M, Mckeown N B (2019). Highly stable fullerene-based porous molecular crystals with open metal sites. Nature Materials, 18(7): 740–745

    Article  CAS  Google Scholar 

  • Castro E, Hernandez Garcia A, Zavala G, Echegoyen L (2017). Fullerenes in biology and medicine. Journal of Materials Chemistry B, 5(32): 6523–6535

    Article  CAS  Google Scholar 

  • Ding C, Pan J, Jin M, Yang D, Shen Z, Wang J, Zhang B, Liu W, Fu J, Guo X, Wang D, Chen Z, Yin J, Qiu Z, Li J (2016). Enhanced uptake of antibiotic resistance genes in the presence of nanoalumina. Nanotoxicology, 10(8): 1051–1060

    Article  CAS  Google Scholar 

  • Eisenbrandt R, Kalkum M, Lurz R, Lanka E (2000). Maturation of IncP Pilin precursors resembles the catalytic dyad-like mechanism of leader peptidases. Journal of Bacteriology, 182(23): 6751–6761

    Article  CAS  Google Scholar 

  • Farré M, Pérez S, Gajda-Schrantz K, Osorio V, Kantiani L, Ginebreda A, Barceló D (2010). First determination of C60 and C70 fullerenes and N-methylfulleropyrrolidine C60 on the suspended material of wastewater effluents by liquid chromatography hybrid quadrupole linear ion trap tandem mass spectrometry. Journal of Hydrology (Amsterdam), 383(1–2): 44–51

    Article  Google Scholar 

  • Han S, Lemire J, Appanna V P, Auger C, Castonguay Z, Appanna V D (2013). How aluminum, an intracellular ROS generator promotes hepatic and neurological diseases: the metabolic tale. Cell Biology and Toxicology, 29(2): 75–84

    Article  CAS  Google Scholar 

  • Imlay J A (2003). Pathways of oxidative damage. Annual Review of Microbiology, 57(1): 395–418

    Article  CAS  Google Scholar 

  • Kabir M M, Shimizu K (2006). Investigation into the effect of soxR and soxS genes deletion on the central metabolism of Escherichia coli based on gene expressions and enzyme activities. Biochemical Engineering Journal, 30(1): 39–47

    Article  CAS  Google Scholar 

  • Koebnik R, Locher K P, Van Gelder P (2000). Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Molecular Microbiology, 37(2): 239–253

    Article  CAS  Google Scholar 

  • Kostelidou K, Jones A C, Thomas C M (1999). Conserved C-terminal region of global repressor korA of broad-host-range plasmid RK2 is required for co-operativity between korA and a second RK2 global regulator, korB. Journal of Molecular Biology, 289(2): 0–221

    Article  CAS  Google Scholar 

  • Lyon D Y, Fortner J D, Sayes C M, Colvin V L, Hughes J B (2005). Bacterial cell association and antimicrobial activity of a C60 water suspension. Environmental Toxicology and Chemistry, 24(11): 2757–2762

    Article  CAS  Google Scholar 

  • Nel A E, Madler L, Velegol D, Xia T, Hoek E M, Somasundaran P, Klaessig F, Castranova V, Thompson M (2009). Understanding biophysicochemical interactions at the nano-bio interface. Nature Materials, 8(7): 543–557

    Article  CAS  Google Scholar 

  • Nguyen C C, Hugie C N, Kile M L, Navab-Daneshmand T (2019). Association between heavy metals and antibiotic-resistant human pathogens in environmental reservoirs: A review. Frontiers of Environmental Science & Engineering, 13(3): 46

    Article  Google Scholar 

  • Qiu Z, Yu Y, Chen Z, Jin M, Yang D, Zhao Z, Wang J, Shen Z, Wang X, Qian D, Huang A, Zhang B, Li J W (2012). Nanoalumina promotes the horizontal transfer of multiresistance genes mediated by plasmids across genera. Proceedings of the National Academy of Sciences of the United States of America, 109(13): 4944–4949

    Article  CAS  Google Scholar 

  • Sakai H, Komano T (1996). DNA replication of IncQ broad-host-range plasmids in gram-negative bacteria. Bioscience, Biotechnology, and Biochemistry, 60(3): 377–382

    Article  CAS  Google Scholar 

  • Schröder G, Lanka E (2005). The mating pair formation system of conjugative plasmids-A versatile secretion machinery for transfer of proteins and DNA. Plasmid, 54(1): 1–25

    Article  Google Scholar 

  • Tan Z, Zhang D, Tian H R, Wu Q, Hou S, Pi J, Sadeghi H, Tang Z, Yang Y, Liu J, Tan Y Z, Chen Z B, Shi J, Xiao Z, Lambert C, Xie S Y, Hong W (2019). Atomically defined angstrom-scale all-carbon junctions. Nature Communications, 10(1): 1748

    Article  Google Scholar 

  • Thauvin C, Rickling S, Schultz P, Celia H, Meunier S, Mioskowski C (2008). Carbon nanotubes as templates for polymerized lipid assemblies. Nature Nanotechnology, 3(12): 743–748

    Article  CAS  Google Scholar 

  • Thomas C M, Nielsen K M (2005). Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nature Reviews. Microbiology, 3(9): 711–721

    Article  CAS  Google Scholar 

  • UNEP (2017). Frontiers 2017: Emerging Issues of Environmental Concern. Geneva: United Nations Environment Programme

    Google Scholar 

  • Vikesland P, Garner E, Gupta S, Kang S, Maile-Moskowitz A, Zhu N (2019). Differential drivers of antimicrobial resistance across the world. Accounts of Chemical Research, 52(4): 916–924

    Article  CAS  Google Scholar 

  • Wang Y, Lu J, Mao L, Li J, Yuan Z, Bond P L, Guo J (2019). Antiepileptic drug carbamazepine promotes horizontal transfer of plasmid-borne multi-antibiotic resistance genes within and across bacterial genera. ISME Journal, 13(2): 509–522

    Article  CAS  Google Scholar 

  • WHO (2017). Global Health Case Challenge: fighting antibiotic resistance. Geneva: World Health Organization

    Google Scholar 

  • Yin L, Zhou H, Lian L, Yan S, Song W (2016). Effects of C60 on the photochemical formation of reactive oxygen species from natural organic matter. Environmental Science & Technology, 50(21): 11742–11751

    Article  CAS  Google Scholar 

  • Yu Y, Zhu X, Wu G, Wang C, Yuan X (2019). Analysis of antibiotic resistance of Escherichia coli isolated from the Yitong River in North-east China. Frontiers of Environmental Science & Engineering, 13(3): 39

    Article  CAS  Google Scholar 

  • Zhang S, Wang Y, Song H, Lu J, Yuan Z, Guo J (2019). Copper nanoparticles and copper ions promote horizontal transfer of plasmid-mediated multi-antibiotic resistance genes across bacterial genera. Environment International, 129: 478–487

    Article  CAS  Google Scholar 

  • Zhang Y, Gu A Z, Cen T, Li X, Li D, Chen J (2018). Petrol and diesel exhaust particles accelerate the horizontal transfer of plasmid-mediated antimicrobial resistance genes. Environment International, 114: 280–287

    Article  CAS  Google Scholar 

  • Zhang Y, Gu A Z, He M, Li D, Chen J (2017). Subinhibitory concentrations of disinfectants promote the horizontal transfer of multidrug resistance genes within and across genera. Environmental Science & Technology, 51(1): 570–580

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (Grant Nos. 91843301, 21527814 and 91643106).

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Authors and Affiliations

  1. Shanghai Key Laboratory of Atmospheric Particle Pollution and Prevention (LAP3), Department of Environmental Science and Engineering, Fudan University, Shanghai, 200433, China

    Qingkun Ji & Dan Li

  2. Department of Obstetrics and Gynecology, Changhai Hospital, Second Military Medical University, Shanghai, 200433, China

    Caihong Zhang

Authors
  1. Qingkun Ji
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  2. Caihong Zhang
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  3. Dan Li
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Correspondence to Caihong Zhang or Dan Li.

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Highlights

• Sub-inhibitory levels of nC60 promote conjugative transfer of ARGs.

• nC60 can induce ROS generation, oxidative stress and SOS response.

• nC60 can increase cell membrane permeability and alter gene expression.

• Results provide evidence of nC60 promoting antibiotic resistance dissemination.

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Ji, Q., Zhang, C. & Li, D. Influences and mechanisms of nanofullerene on the horizontal transfer of plasmid-encoded antibiotic resistance genes between E. coli strains. Front. Environ. Sci. Eng. 14, 108 (2020). https://doi.org/10.1007/s11783-020-1287-0

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  • DOI: https://doi.org/10.1007/s11783-020-1287-0

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