Elsevier

Water Research

Volume 165, 15 November 2019, 114987
Water Research

Widely distributed nanocolloids in water regulate the fate and risk of graphene oxide

https://doi.org/10.1016/j.watres.2019.114987Get rights and content

Highlights

  • Binding mechanisms of Nc onto GO at the molecular level in aqueous phase.

  • Biolayer interferometry was used to quantitatively analyze the binding affinity.

  • Nc reduced the aggregation and sedimentation of GO in water.

  • Co-exposure of GO and Nc led to antagonistic effects on zebrafish.

Abstract

The environmental behaviors and risks associated with graphene oxide (GO, a popular 2D nanomaterial) have attracted considerable attention. GO released to aquatic systems will most likely interact with ubiquitous nanocolloids (Nc) in surface water. However, the effects of Nc on the fate and risk of GO remain largely unknown in water. Herein, the binding of Nc onto GO was investigated via electron microscopy, electron paramagnetic resonance, 2D correlation spectroscopy and biolayer interferometry. The results revealed that electron charge transfers, hydrophilic effects and π-π stacking contributed to a strong affinity (KD = 5.6 nM) and high adsorption capacity (159.8 mg/g) of Nc onto the GO surface. Moreover, GO nanosheets transformed to a scroll morphology or multiple GO particles bridging by Nc, which remarkably reduced the aggregation and sedimentation rates after binding with Nc. Interestingly, co-exposure with Nc greatly alleviated the toxicity (e.g., tail malformation, yolk sac edema and oxidative stress) of GO to zebrafish embryos. Morphological and structural alterations of GO after binding to Nc contributed to the mechanisms for the antagonistic effects on the zebrafish embryos toxicity. The present work provides insights into the environmental fate and risk of GO by ubiquitous Nc in natural water.

Introduction

Natural colloids with a size range from approximately 1 to 1000 nm are important environmental components and widely present in aqueous environments (Stolpe et al., 2013; Zhou et al., 2016). Compared to large-scale colloids (100–1000 nm), nanocolloids (Nc, approximately 1–100 nm) have a large specific surface area and high dispersity, which may play an important role in the fate and bioavailability of pollutants in the aquatic environment (Santschi, 2018; Xu et al., 2018), although the related information remains obscure. Graphene oxide (GO), a two-dimensional carbon-based nanomaterial, presents unique structural and physical properties that highlight its applicability in various areas, such as energy storage (Georgakilas et al., 2016), biomedicine (Lee et al., 2016) and environmental protection (Joshi et al., 2014). Since GO released to aquatic systems will most likely interact with Nc, a deep understanding of the basic interactions between GO and Nc may help to better clarify the potential risks of GO and provide guidance on the safe design of GO.

Given the complex compositions of Nc, analyzing the interaction analysis between nanomaterials and Nc remains challenging. Two-dimensional correlation spectroscopy (2DCOS) that is capable of resolving overlapped peaks could probe the interaction mechanisms of complex compounds (Phong and Hur, 2018; Yan et al., 2013). Herein, a 2DCOS analysis that integrates synchronous fluorescence and Fourier transform infrared spectroscope (FTIR) was performed to provide an in-depth understanding of the binding characteristic mechanisms of Nc onto GO at the molecular level. The affinity interactions between Nc and GO are fundamental to understanding the effects of Nc on the environmental behaviors of GO. Biolayer interferometry (BLI) is a real-time and label-free optical technique that using fiber-optic biosensors to accurately quantify and measure the affinity between molecules, such as protein−protein, protein−nucleic acids, and protein−small molecules (Gao et al., 2017; Hjuler et al., 2017). In recent years, BLI has successfully used to investigate the interactions between GO and molecules, such as proteins, single-stranded DNA (ssDNA) and humic acid (HA) (Zhou et al., 2019). Herein, BLI was used to directly and accurately detect the binding affinity between GO and Nc.

The colloidal behaviors of GO with dissolved organic matter (DOM) or environmentally relevant cations (e.g., Ca2+ and Na+) have been extensively studied (Chowdhury et al., 2015; Yang et al., 2016). For example, Chowdhury et al. observed that DOM improved GO dispersion and divalent cations enhanced GO aggregation (Chowdhury et al., 2013). The roles of three common geogenic minerals (montmorillonite, kaolinite, and goethite) with different surface charge properties and geometric dimensions in the GO−mineral heteroaggregation and the environmental fate of GO were also investigated (Zhao et al., 2015). In contrast, Nc were extracted from the natural environment and contained inorganic mineral colloids (e.g., Fe and Mn oxides and aluminosilicates), aromatic refractory organic matter binding heavy metals, and rigid biopolymers (Buffle et al., 1998; Ouyang et al., 2018). However, effects of Nc on the aggregation, adsorption and morphological transformation of engineered nanoparticles (ENPs) remain largely unknown. GO with shape edges exhibited high colloidal stability, which led to adverse effects and sufficient direct contact on Escherichia coli, Chlorella pyrenoidosa or zebrafish (Akhavan and Ghaderi, 2010; Souza et al., 2017; Zhao et al., 2018). Compared to studies on the adverse effects of pristine GO, investigations into the environmental risks of the GO binding with Nc are much more meaningful. In the present work, the main objectives were to explore the effects of Nc on the morphology, aggregation, uptake and ecotoxicity of GO after binding. Zebrafish as a model was used as the tested organism. The findings will provide new insights into the fate and risks of ENPs under the influence of Nc at environmental concentrations.

Section snippets

Sampling, isolation and enrichment of Nc

The Haihe River with the mainstream length 105 km, an average width of approximately 100 m, and an average depth of 6.5 m, is the one of the seven largest basins in China (Liu et al., 2007). Because the river receives domestic, industrial, and agricultural pollutants from Tianjin City, Hebei Province and Beijing City, the Haihe River has been profoundly contaminated (Niu et al., 2018). According to our recent work, the concentrations of Nc ranged from 3.7 to 7.2 mg/L with similar morphologies,

Complicated Nc enriched from surface water

The morphology and size distribution of the Nc were examined via transmission electron microscopy (TEM) and atomic force microscopy (AFM) (Fig. S2a−2d). Most of the observed Nc presented irregular or flaky grain shapes, and the size and the thickness of the Nc were predominantly (>70%) smaller than 40 nm and 10 nm, respectively. The Nc with size ranges of 1–20 and 21–40 nm accounted for 42% and 50%, respectively (Fig. S2b). The mean size of the Nc was approximately 20 nm. Furthermore, the AFM

Conclusions

In the present study, the multiple analytical methods (e.g., BLI and 2DCOS) revealed that the Nc exhibited a high binding affinity onto GO via hydrophilic effects, electron charge transfers and π-π stacking interactions. Nc adsorption also promoted the dispersity of GO in water. After binding to Nc, the properties (e.g. morphology and structure) of GO changed. Morphology was a critical factor that affected graphene nanotoxicity (Hu et al., 2015). The pristine GO was transformed into a scroll

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (grant nos. 21722703, 21677080 and 31770550).

References (57)

  • J.P. Souza et al.

    Toxicological effects of graphene oxide on adult zebrafish (Danio rerio)

    Aquat. Toxicol.

    (2017)
  • B. Stolpe et al.

    Abundance, size distributions and trace-element binding of organic and iron-rich nanocolloids in Alaskan rivers, as revealed by field-flow fractionation and ICP-MS

    Geochem. Cosmochim. Acta

    (2013)
  • H. Xu et al.

    Characterization, origin and aggregation behavior of colloids in eutrophic shallow lake

    Water Res.

    (2018)
  • M. Yan et al.

    Study of iron and aluminum binding to Suwannee River fulvic acid using absorbance and fluorescence spectroscopy: comparison of data interpretation based on NICA-Donnan and Stockholm humic models

    Water Res.

    (2013)
  • S. Yang et al.

    Effects of humic acid on copper adsorption onto few-layer reduced graphene oxide and few-layer graphene oxide

    Carbon

    (2014)
  • Z. Yang et al.

    Flocculation performance and mechanism of graphene oxide for removal of various contaminants from water

    Water Res.

    (2013)
  • Z. Zhou et al.

    Colloidal size spectra, composition and estuarine mixing behavior of DOM in river and estuarine waters of the northern Gulf of Mexico

    Geochem. Cosmochim. Acta

    (2016)
  • O. Akhavan et al.

    Toxicity of graphene and graphene oxide nanowalls against bacteria

    ACS Nano

    (2010)
  • M.A. Ali et al.

    Lipid–lipid interactions in aminated reduced graphene oxide interface for biosensing application

    Langmuir

    (2014)
  • G. Barba-Spaeth et al.

    Structural basis of potent zika–dengue virus antibody cross-neutralization

    Nature

    (2016)
  • N.R. Brun et al.

    Nanoparticles induce dermal and intestinal innate immune system responses in zebrafish embryos

    Environ. Sci.: Nano

    (2018)
  • J. Buffle et al.

    A generalized description of aquatic colloidal interactions: the three-colloidal component approach

    Environ. Sci. Technol.

    (1998)
  • V.L. Castro et al.

    Nanoecotoxicity assessment of graphene oxide and its relationship with humic acid

    Environ. Toxicol. Chem.

    (2018)
  • Y. Chen et al.

    Mitigation in multiple effects of graphene oxide toxicity in zebrafish embryogenesis driven by humic acid

    Environ. Sci. Technol.

    (2015)
  • Y. Chong et al.

    Reduced cytotoxicity of graphene nanosheets mediated by blood-protein coating

    ACS Nano

    (2015)
  • I. Chowdhury et al.

    Colloidal properties and stability of graphene oxide nanomaterials in the aquatic environment

    Environ. Sci. Technol.

    (2013)
  • I. Chowdhury et al.

    Aggregation and stability of reduced graphene oxide: complex roles of divalent cations, pH, and natural organic matter

    Environ. Sci. Technol.

    (2015)
  • M.R.R. De Planque et al.

    Electrophysiological characterization of membrane disruption by nanoparticles

    ACS Nano

    (2011)
  • Cited by (22)

    View all citing articles on Scopus
    View full text