Please wait a minute...
Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

Postal Subscription Code 80-973

2018 Impact Factor: 3.883

Front. Environ. Sci. Eng.    2020, Vol. 14 Issue (6) : 108    https://doi.org/10.1007/s11783-020-1287-0
RESEARCH ARTICLE
Influences and mechanisms of nanofullerene on the horizontal transfer of plasmid-encoded antibiotic resistance genes between E. coli strains
Qingkun Ji1, Caihong Zhang2(), Dan Li1()
1. Shanghai Key Laboratory of Atmospheric Particle Pollution and Prevention (LAP3), Department of Environmental Science and Engineering, Fudan University, Shanghai 200433, China
2. Department of Obstetrics and Gynecology, Changhai Hospital, Second Military Medical University, Shanghai 200433, China
 Download: PDF(1595 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

• 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.

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 mg/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.

Keywords Nanofullerene      Sub-minimum inhibitory concentrations      Antibiotic resistance genes      Conjugation      Molecular biological techniques     
Corresponding Author(s): Caihong Zhang,Dan Li   
Issue Date: 28 June 2020
 Cite this article:   
Qingkun Ji,Caihong Zhang,Dan Li. Influences and mechanisms of nanofullerene on the horizontal transfer of plasmid-encoded antibiotic resistance genes between E. coli strains[J]. Front. Environ. Sci. Eng., 2020, 14(6): 108.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-020-1287-0
https://academic.hep.com.cn/fese/EN/Y2020/V14/I6/108
Fig.1  Fold changes between E. coli strains in conjugation frequency upon exposure to nC60. nC60 had significant influences on the conjugation of plasmid-encoded ARGs (ANOVA, P?<?0.05). Significant differences between nC60 + TU or individual nC60 treated groups and the control (0 mg/L of nC60) were tested with ANOVA (LSD).
Fig.2  Exposure to nC60 increases intra-ROS formation that significantly correlates with conjugation of plasmid-encoded ARGs. The intra-ROS levels in E. coli K12 (a) and E. coli S17 (b) induced by nC60. Correlations between the conjugation rates (fold changes) and intra-ROS formation levels (fold changes) in E. coli K12 (c) and E. coli S17 (d). Significant differences between the non-exposed control group and nC60-exposed groups were tested with ANOVA (LSD).
Fig.3  TEM pictures of nC60 (a), E. coli in the test group (no nC60 exposure) (b), E. coli afterwards exposure to nC60 (450 μg/L) (c), and E. coli after exposure to nC60 (1800 μg/L) (d). The red arrows refer to nC60 and the green arrows refer to the pores formed after exposure to nC60.
Fig.4  Impacts of nC60 on the mRNA expression levels of genes involved in the OMPs, Global regulation, Oxidative stress, Mpf system, SOS-response, and Dtr system during conjugation. The radial axis depicts the log2-fold absolute values of genes relative to the control group.
Fig.5  Impacts of nC60 on the mRNA expression levels of genes involved in soxR (a), soxS (b), rpoS (c), oxyR (d), lexA (e), recA (f), umuD (g), ompF (h), ompC (i), ompA (j), trbA (k), korA (l), korB (m), traF (n), trbBp (o), traJ (p), and trfAp (q), during conjugation. Significant differences between the non-exposed control group and nC60-exposed groups were tested with ANOVA (LSD).
1 R G Alargova, S Deguchi, K Tsujii (2001). Stable colloidal dispersions of fullerenes in polar organic solvents. Journal of the American Chemical Society, 123(43): 10460–10467
https://doi.org/10.1021/ja010202a
2 D I Andersson, D Hughes (2010). Antibiotic resistance and its cost: Is it possible to reverse resistance? Nature Reviews. Microbiology, 8(4): 260–271
https://doi.org/10.1038/nrmicro2319
3 D I Andersson, D Hughes (2014). Microbiological effects of sublethal levels of antibiotics. Nature Reviews. Microbiology, 12(7): 465–478
https://doi.org/10.1038/nrmicro3270
4 G V Andrievsky, V K Klochkov, E L Karyakina, N O Mchedlov-Petrossyan (1999). Studies of aqueous colloidal solutions of fullerene C60 by electron microscopy. Chemical Physics Letters, 300(3–4): 392–396
https://doi.org/10.1016/S0009-2614(98)01393-1
5 C G Bezzu, L A Burt, C J Mcmonagle, S A Moggach, B M Kariuki, D R Allan, M Warren, N B Mckeown (2019). Highly stable fullerene-based porous molecular crystals with open metal sites. Nature Materials, 18(7): 740–745
https://doi.org/10.1038/s41563-019-0361-0
6 E Castro, A Hernandez Garcia, G Zavala, L Echegoyen (2017). Fullerenes in biology and medicine. Journal of Materials Chemistry B, 5(32): 6523–6535
https://doi.org/10.1039/C7TB00855D
7 C Ding, J Pan, M Jin, D Yang, Z Shen, J Wang, B Zhang, W Liu, J Fu, X Guo, D Wang, Z Chen, J Yin, Z Qiu, J Li (2016). Enhanced uptake of antibiotic resistance genes in the presence of nanoalumina. Nanotoxicology, 10(8): 1051–1060
https://doi.org/10.3109/17435390.2016.1161856
8 R Eisenbrandt, M Kalkum, R Lurz, E Lanka (2000). Maturation of IncP Pilin precursors resembles the catalytic dyad-like mechanism of leader peptidases. Journal of Bacteriology, 182(23): 6751–6761
https://doi.org/10.1128/JB.182.23.6751-6761.2000
9 M Farré, S Pérez, K Gajda-Schrantz, V Osorio, L Kantiani, A Ginebreda, D Barceló (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
https://doi.org/10.1016/j.jhydrol.2009.08.016
10 S Han, J Lemire, V P Appanna, C Auger, Z Castonguay, V D Appanna (2013). How aluminum, an intracellular ROS generator promotes hepatic and neurological diseases: the metabolic tale. Cell Biology and Toxicology, 29(2): 75–84
https://doi.org/10.1007/s10565-013-9239-0
11 J A Imlay (2003). Pathways of oxidative damage. Annual Review of Microbiology, 57(1): 395–418
https://doi.org/10.1146/annurev.micro.57.030502.090938
12 M M Kabir, K Shimizu (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
https://doi.org/10.1016/j.bej.2006.01.015
13 R Koebnik, K P Locher, P Van Gelder (2000). Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Molecular Microbiology, 37(2): 239–253
https://doi.org/10.1046/j.1365-2958.2000.01983.x
14 K Kostelidou, A C Jones, C M Thomas (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
15 D Y Lyon, J D Fortner, C M Sayes, V L Colvin, J B Hughes (2005). Bacterial cell association and antimicrobial activity of a C60 water suspension. Environmental Toxicology and Chemistry, 24(11): 2757–2762
https://doi.org/10.1897/04-649R.1
16 A E Nel, L Madler, D Velegol, T Xia, E M Hoek, P Somasundaran, F Klaessig, V Castranova, M Thompson (2009). Understanding biophysicochemical interactions at the nano-bio interface. Nature Materials, 8(7): 543–557
https://doi.org/10.1038/nmat2442
17 C C Nguyen, C N Hugie, M L Kile, T Navab-Daneshmand (2019). Association between heavy metals and antibiotic-resistant human pathogens in environmental reservoirs: A review. Frontiers of Environmental Science & Engineering, 13(3): 46
https://doi.org/10.1007/s11783-019-1129-0
18 Z Qiu, Y Yu, Z Chen, M Jin, D Yang, Z Zhao, J Wang, Z Shen, X Wang, D Qian, A Huang, B Zhang, J W Li (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
https://doi.org/10.1073/pnas.1107254109
19 H Sakai, T Komano (1996). DNA replication of IncQ broad-host-range plasmids in gram-negative bacteria. Bioscience, Biotechnology, and Biochemistry, 60(3): 377–382
https://doi.org/10.1271/bbb.60.377
20 G Schröder, E Lanka (2005). The mating pair formation system of conjugative plasmids-A versatile secretion machinery for transfer of proteins and DNA. Plasmid, 54(1): 1–25
https://doi.org/10.1016/j.plasmid.2005.02.001
21 Z Tan, D Zhang, H R Tian, Q Wu, S Hou, J Pi, H Sadeghi, Z Tang, Y Yang, J Liu, Y Z Tan, Z B Chen, J Shi, Z Xiao, C Lambert, S Y Xie, W Hong (2019). Atomically defined angstrom-scale all-carbon junctions. Nature Communications, 10(1): 1748
https://doi.org/10.1038/s41467-019-09793-8
22 C Thauvin, S Rickling, P Schultz, H Celia, S Meunier, C Mioskowski (2008). Carbon nanotubes as templates for polymerized lipid assemblies. Nature Nanotechnology, 3(12): 743–748
https://doi.org/10.1038/nnano.2008.318
23 C M Thomas, K M Nielsen (2005). Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nature Reviews. Microbiology, 3(9): 711–721
https://doi.org/10.1038/nrmicro1234
24 UNEP (2017). Frontiers 2017: Emerging Issues of Environmental Concern. Geneva: United Nations Environment Programme
25 P Vikesland, E Garner, S Gupta, S Kang, A Maile-Moskowitz, N Zhu (2019). Differential drivers of antimicrobial resistance across the world. Accounts of Chemical Research, 52(4): 916–924
https://doi.org/10.1021/acs.accounts.8b00643
26 Y Wang, J Lu, L Mao, J Li, Z Yuan, P L Bond, J Guo (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
https://doi.org/10.1038/s41396-018-0275-x
27 WHO (2017). Global Health Case Challenge: fighting antibiotic resistance. Geneva: World Health Organization
28 L Yin, H Zhou, L Lian, S Yan, W Song (2016). Effects of C60 on the photochemical formation of reactive oxygen species from natural organic matter. Environmental Science & Technology, 50(21): 11742–11751
https://doi.org/10.1021/acs.est.6b04488
29 Y Yu, X Zhu, G Wu, C Wang, X Yuan (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
https://doi.org/10.1007/s11783-019-1123-6
30 S Zhang, Y Wang, H Song, J Lu, Z Yuan, J Guo (2019). Copper nanoparticles and copper ions promote horizontal transfer of plasmid-mediated multi-antibiotic resistance genes across bacterial genera. Environment International, 129: 478–487
https://doi.org/10.1016/j.envint.2019.05.054
31 Y Zhang, A Z Gu, T Cen, X Li, D Li, J Chen (2018). Petrol and diesel exhaust particles accelerate the horizontal transfer of plasmid-mediated antimicrobial resistance genes. Environment International, 114: 280–287
https://doi.org/10.1016/j.envint.2018.02.038
32 Y Zhang, A Z Gu, M He, D Li, J Chen (2017). Subinhibitory concentrations of disinfectants promote the horizontal transfer of multidrug resistance genes within and across genera. Environmental Science & Technology, 51(1): 570–580
https://doi.org/10.1021/acs.est.6b03132
[1] FSE-20058-OF-JQK_suppl_1 Download
[1] Yuan Meng, Weiyi Liu, Heidelore Fiedler, Jinlan Zhang, Xinrui Wei, Xiaohui Liu, Meng Peng, Tingting Zhang. Fate and risk assessment of emerging contaminants in reclaimed water production processes[J]. Front. Environ. Sci. Eng., 2021, 15(5): 104-.
[2] Lian Yang, Qinxue Wen, Zhiqiang Chen, Ran Duan, Pan Yang. Impacts of advanced treatment processes on elimination of antibiotic resistance genes in a municipal wastewater treatment plant[J]. Front. Environ. Sci. Eng., 2019, 13(3): 32-.
[3] Qiaowen Tan, Weiying Li, Junpeng Zhang, Wei Zhou, Jiping Chen, Yue Li, Jie Ma. Presence, dissemination and removal of antibiotic resistant bacteria and antibiotic resistance genes in urban drinking water system: A review[J]. Front. Environ. Sci. Eng., 2019, 13(3): 36-.
[4] Menglu Zhang, Sheng Chen, Xin Yu, Peter Vikesland, Amy Pruden. Degradation of extracellular genomic, plasmid DNA and specific antibiotic resistance genes by chlorination[J]. Front. Environ. Sci. Eng., 2019, 13(3): 38-.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed