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Destructive extraction of phospholipids from Escherichia coli membranes by graphene nanosheets

Nature Nanotechnology volume 8, pages 594–601 (2013)Cite this article

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A Corrigendum to this article was published on 04 December 2013

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Abstract

Understanding how nanomaterials interact with cell membranes is related to how they cause cytotoxicity and is therefore critical for designing safer biomedical applications. Recently, graphene (a two-dimensional nanomaterial) was shown to have antibacterial activity on Escherichia coli, but its underlying molecular mechanisms remain unknown. Here we show experimentally and theoretically that pristine graphene and graphene oxide nanosheets can induce the degradation of the inner and outer cell membranes of Escherichia coli, and reduce their viability. Transmission electron microscopy shows three rough stages, and molecular dynamics simulations reveal the atomic details of the process. Graphene nanosheets can penetrate into and extract large amounts of phospholipids from the cell membranes because of the strong dispersion interactions between graphene and lipid molecules. This destructive extraction offers a novel mechanism for the molecular basis of graphene's cytotoxicity and antibacterial activity.

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Figure 1: Morphology of E. coli exposed to graphene oxide nanosheets.
Figure 2: Graphene nanosheet insertion and lipid extraction.
Figure 3: Interaction energy profiles.
Figure 4: Lipid extraction by graphene in docking simulations.
Figure 5: Robustness of lipid extraction by graphene.
Figure 6: Lipid extraction by graphene oxide nanosheets.

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  • 26 November 2013

    In the version of this Article originally published, it was not made clear that the two Escherichia coli cells in the bottom left of Fig. 1a are from a different TEM image to the others. The figure and caption have now been corrected in the PDF and HTML versions of the Article.

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Acknowledgements

The authors thank B. Berne, Yuliang Zhao, Guosheng Shi, Huan Zhang, Jingyuan Li, Seung-gu Kang, Zhen Xia and P. Das for discussions. This work was partially supported by the National Natural Science Foundation of China (grant nos 11290164, 11204269, 11172158 and 11105088), the National Basic Research Program of China (2012CB932400, 2013CB933800 and 2012CB932600) and the First-class Discipline of Universities in Shanghai. The authors acknowledge the IBM Blue Gene supercomputer and Shanghai Supercomputer Center for computational resources. R.Z. acknowledges support from the IBM Blue Gene Science Program.

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Authors and Affiliations

  1. Institute of Systems Biology, Shanghai University, Shanghai, 200444, China

    Yusong Tu & Zengrong Liu

  2. Division of Interfacial Water and Division of Physical Biology, Shanghai Institute of Applied Physics, Key Laboratory of Interfacial Physics and Technology, Chinese Academy of Sciences, PO Box 800-204, Shanghai, 201800, China

    Yusong Tu, Min Lv, Meng Zhang, Qing Huang, Chunhai Fan & Haiping Fang

  3. Department of Engineering Mechanics and Soft Matter Research Center, Zhejiang University, Hangzhou, 310027, China

    Peng Xiu & Ruhong Zhou

  4. IBM Thomas J. Watson Research Center, Yorktown Heights, New York, 10598, USA

    Tien Huynh, Matteo Castelli & Ruhong Zhou

  5. Department of Chemistry, Columbia University, New York, 10027, USA

    Ruhong Zhou

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Contributions

R.H.Z., Q.H., H.P.F. and Y.S.T. conceived and designed the experiments and simulations. Y.S.T., P.X., T.H. and M.Z. performed the simulations. M.L. performed the experiments. Y.S.T., P.X., H.P.F., R.H.Z., Q.H., C.H.F. and Z.R.L. analysed the data. Y.S.T., R.H.Z., H.P.F., P.X., M.C., Q.H. and C.H.F. co-wrote the paper. All authors discussed the results and commented on the manuscript.

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Correspondence to Qing Huang or Ruhong Zhou.

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Tu, Y., Lv, M., Xiu, P. et al. Destructive extraction of phospholipids from Escherichia coli membranes by graphene nanosheets. Nature Nanotech 8, 594–601 (2013). https://doi.org/10.1038/nnano.2013.125

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