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Critical Review
Graphene in the Aquatic Environment: Adsorption, Dispersion, Toxicity and Transformation Jian Zhao, Zhenyu Wang, Jason C. White, and Baoshan Xing Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/es5022679 • Publication Date (Web): 14 Aug 2014 Downloaded from http://pubs.acs.org on August 21, 2014
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Graphene in the Aquatic Environment: Adsorption, Dispersion,
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Toxicity and Transformation
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Jian Zhao,†, ‡ Zhenyu Wang,†,‡ Jason C. White,§ and Baoshan Xing*,‡
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†
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Education, Ocean University of China, Qingdao 266100, China
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‡
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USA
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§
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College of Environmental Science and Engineering, Key Laboratory of Ministry of
Stockbridge School of Agriculture, University of Massachusetts, Amherst, MA 01003,
Department of Analytical Chemistry, The Connecticut Agricultural Experiment Station,
New Haven, CT 06504, USA
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*Corresponding author
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Tel.: +1 413 545 5212
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E-mail address:
[email protected] (Prof. Baoshan Xing)
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Abstract:
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Graphene-family nanomaterials (GFNs) including pristine graphene, reduced graphene
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oxide (rGO) and graphene oxide (GO) offer great application potential, leading to the
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possibility of their release into aquatic environments. Upon exposure, graphene/rGO and
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GO exhibit different adsorption properties towards environmental adsorbates, and the
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molecular interactions at the GFN-water interface are discussed. After solute adsorption,
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the dispersion/aggregation behaviors of GFNs can be altered by solution chemistry, as
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well as by the presence of colloidal particles and biocolloids. GO has different dispersion
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performance from pristine graphene and rGO, which is further demonstrated from surface
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properties. Upon exposure in aquatic environments, GFNs have adverse impacts on
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aquatic organisms (e.g., bacteria, algae, plants, invertebrates and fish). The mechanisms
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of GFNs toxicity at the cellular level are reviewed and the remaining unclear points on
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toxic mechanisms such as membrane damage are presented. Moreover, we highlight the
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transformation routes of GO to rGO. The degradation of GFNs upon exposure to UV
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irradiation and/or biota is also reviewed. In view of the unanswered questions, future
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research should include comprehensive characterization of GFNs, new approaches for
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explaining GFNs aggregation, environmental behaviors of metastable GO, and the
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relationship between dispersion of GFNs and the related adsorption properties.
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1. Introduction
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Graphene, due to its exceptional mechanical, electronic, optical and catalytic
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properties,1,2,3 has attracted great attention in the scientific community. Ideal graphene
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(Figure 1A) is a single layer of sp2-hybridized carbon atoms joined by covalent bonds.4,5
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Because of the difficulty in isolating single layers of graphene, “few-layer” graphene
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(2~5 layers), multilayer graphene (2~10 layers) and graphite nanoplates (2D graphite
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material with a thickness and/or lateral dimension less than 100 nm) are all considered as
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graphene-family nanomaterials (GFNs).6 Another type of GFNs is graphene derivatives,
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such as graphene oxide (GO) (Figure 1B). GO is an intermediate product during synthesis
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of reduced graphene oxide (rGO, Figure 1C) and prepared by oxidative exfoliation of
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graphite.7 The synthesis and chemistry of rGO and GO were comprehensively reviewed
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by Loh et al.8 and Dreyer et al.,9 respectively.
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Currently, GFNs are in commercial production.10 With projected rapid increases in
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production and application,11 GFNs will likely be released into the environment at
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significant levels. For example, GO-polymer nanocomposites could release GO particles
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during their life cycle because of photodegradation upon UV exposure.12 Notably,
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considerable GFN release could occur during environmental applications such as
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adsorbents for wastewater and drinking water treatment,13,14,15 materials for solid-phase
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extraction,16 membranes for desalination,17 catalysts for aqueous organic pollutant
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oxidation and degradation,18 and coating materials for filtration.19 In addition, GFNs
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could be introduced to the environment during the waste disposal of GFN-containing
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products. The released GFNs may have significant adverse environmental impacts.
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Consequently, significant research attention has recently been focused on the
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environmental behavior of GFNs.12,20,21
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However, the existing literature on environmental behavior of GFNs remains limited.
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In aquatic environments, GFNs would first interact with system components such as
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inorganic ions and natural organic matter (NOM), both of which are able to modify the
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surface of GFNs. After adsorption, dispersion-aggregation behaviors could also be altered.
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In addition, toxicity to aquatic organisms may be an important concern after
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environmental GFN release. Upon interaction with environmental media and biota, GFNs
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have been shown to transform and degrade.21 This thorough review will focus mainly on
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these four aspects of GFN fate: adsorption, dispersion, toxicity and transformation. Also,
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this review will identify key knowledge gaps and provide valuable insight into the
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transport, fate, and risk posed from GFNs, as well as their potential use for select
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environmental applications.
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2. Adsorption properties of GFNs in aquatic environments
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Adsorption on GFNs is a critical physiochemical process at the GFN-water interface
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due to large surface area and surface-active properties of the sorbents. This process can (1)
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affect the mobility and fate of both organic matter (e.g., humic acid, amino acids, proteins)
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and xenobiotic pollutants (e.g., heavy metals, hydrophobic organic compounds); (2) alter
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the surface characteristics of GFNs through coating and modification; and (3) be of
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importance for potential adsorbent applications in water treatment technologies.
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Adsorption of organic and inorganic compounds on GFNs has been investigated. In
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reviewing the current literature (Table S1), molecular interactions and adsorption
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capacity on the GFN surface will be addressed with regard to the structural properties of
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both GFNs and adsorbates, as well as important environmental factors.
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2.1. Interactions at the GFN-water interface. For environmental adsorbates such as
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organic molecules, inorganic ions, macromolecules and mineral particles (Table S1), five
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molecular interactions are summarized: π bonding interaction, hydrophobic effect;
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electrostatic interaction (Coulomb force), hydrogen bonding and Lewis acid-base
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interaction. The four types of π bonding interaction are π–π, n–π, cation–π and anion–π
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bonding. π–π bonding occurs between C=C double bonds or benzene rings of adsorbed
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organic molecules and benzene rings on GFN surface via π–π coupling. π–π interaction is
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suggested as one of most important mechanisms contributing to GFN interaction with
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aromatic compounds (e.g., PAHs, biphenyl, phenol),22,23 macromolecules (e.g., humic
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acid, DNA, protein),24,25,26 and graphitic particles (e.g., carbon nanotubes (CNTs)).27 n–π
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interactions occur between GFN electron-depleted sites and n-electron donors of organic
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compounds which contain oxygen (e.g., 1-naphthol) or nitrogen (e.g., 1-naphthylamine)
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with lone electron pairs.28 Cation–π bonds form between the GFN π–electrons and easily
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protonated amino groups (e.g., tetracycline)29 or metal ions (e.g., Pb (II)).30 Conversely,
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the GFN surface could act as an electron acceptor for anion (e.g., F–, Cl–, Br–) adsorption;
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the anion–π bonding was unexpectedly strong using a computational method based on the
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density functional theory.31 Hydrophobic effects will occur with hydrophobic organic
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compounds (HOCs) on graphene and rGO, both of which have water hydrophobic
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external surfaces. The strength of binding is directly related to the hydrophobicity of the
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organic chemical. The hexadecane–water distribution coefficient (KHW) is a preferred
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parameter over the octanol-water distribution coefficient (KOW) to correlate adsorption on
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GFNs because octanol contains an –OH group that may possibly interact with organic
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chemicals.32 For GO, the hydrophobic interaction is generally weak due to oxygen-
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containing functional groups (e.g., epoxy and hydroxyl groups) on the edge but still
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occurs because of the hydrophobic basal plane.26 Electrostatic interaction depends on the
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charge nature of both GFNs and adsorbates. GO sheets are strongly negatively charged,
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with a zero point of charge (ZPC) lower than pH 2.0.33,34 Thus, the GO surface charge is
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negative in aquatic environments (pH 5-9), showing electrostatic attraction towards both
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organic and inorganic cations.35,36,37 A weaker attraction would exist on rGO surfaces due
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to the residual oxygen functional groups after the reduction process.38 Hydrogen bonding
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has been used to explain the interaction of GO functional groups with the adsorbed
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organic compounds,39 humic acid24 and mineral particles24 that contain oxygen-functional
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groups. In aquatic environments, this interaction could be weakened by water molecules
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that form hydrogen bonds with GO. Lewis acid-base interactions, including ligand
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exchange, metal ion exchange and complexation, play an important role in contributing to
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sorption on GFNs, especially for GO.40 Metal ion exchange and complexation are
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primary mechanisms for the adsorption of metal ions (e.g., Cu (II), Pb (II)) on GO.37,41,42
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The specific interactions for each type of adsorbate are shown in Table S2. The potential
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interactions that have not been reported in the literature but are possible based on
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theoretical analysis are also listed in Table S2. For example, although there are no current
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reports on the formation of covalent bonds, this interaction may occur between GO and
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organic compounds containing functional groups such as –OH, –COOH and –NH2 as the
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formation of covalent bonds have been reported on organic compounds (e.g., L-
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phenylalanine) and CNTs.43
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The strength of GFN interactions with adsorbates has been studied by both density
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functional theory (DFT) calculations and by batch experiments. DFT calculation has been
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applied to simulate the binding energy and adsorption configuration of both inorganic
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(Li+, Cl-)31,44,45 and organic adsorbates (benzene and naphthalene)46 on the graphene
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surface. Batch experiments with the aid of isotherm modeling could also be used to
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evaluate interaction strength. Among the models (Table S3), the Polanyi theory based
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Dubinin-Ashtakhov (DA) model has parameters E and b, which describe the strength of
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interaction forces.47 For most adsorbates, multiple interactions operate simultaneously at
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the GFN-water interface (Table S2). The individual interactions can be identified by the
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properties of both GFN and adsorbates. For example, π−π bond can be estimated by
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π−electron polarizability (π*). A detailed explanation of specific interactions has been
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summarized previously by our group.32,47 Currently, the contribution of individual
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interactions is hypothesized in most studies. How one can accurately calculate/quantify
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the contribution of a specific interaction is challenging. It is worth mentioning that Xia et
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al. reported a biological surface adsorption index (BSAI) approach based on the
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experimental obtained adsorption coefficients (K) and adsorbate properties such as excess
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molar refraction, effective dipolarity and polarizability, hydrogen-bond acidity and
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basicity, and McGowan characteristic volume.48 The BSAI model can predict the K value
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of a specific organic adsorbate on CNTs and quantify the contribution of a specific
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interaction without experimental adsorption data. For GFNs, a similar model may be
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established after more adsorption data (at least twenty compounds) become available in
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the near future.
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2.2. Adsorption capacity. For single-layer graphene, both sides of the graphitic
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surface provide adsorption sites. However, few-layer and multilayer graphene sheets
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comprised of stacked graphene layers have a much greater likelihood of entering aquatic
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environments due to the complicated and difficult process of isolating single-layer
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graphene.4 Single layers in multilayer graphene are stacked as in graphite,49 and the
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interlayer space will not be occupied by environmental adsorbates such as organic
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molecules because of the low adsorption capacity of graphite.40,50 Therefore, only the
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exterior surfaces of multilayer graphene are available for adsorption. GFNs adsorption
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capacity has mainly been obtained from isotherm modeling. Among the commonly used
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isotherm models (Table S3), Langmuir and Polanyi theory-based DA models have a
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maximum adsorption capacity parameter (Q0). The Langmuir model has been widely
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used for inorganic and organic molecule adsorption fitting, whereas the DA model is
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currently only applicable for an organic compound whose water solubility is available at
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a specific pH and temperature. Figure 2 presents the relationship between the Brunauer-
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Emmer-Teller (BET) surface area of GFNs and Langmuir-fitted adsorption capacity
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(mmol/g) for adsorbates. There is a positive correlation for the adsorption of metal ions
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and organic molecules on GO and rGO, respectively, showing that surface area is the
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primary factor determining the magnitude of adsorption onto GFNs. The low R2 values of
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the correlation can be explained as follows: (1) BET surface area cannot completely
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reflect the actual surface area because of GFNs agglomeration and aggregation in
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aqueous solution;51 (2) other parameters such as micropore volume could also contribute
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the high-energy adsorption sites,52 but limited work has characterized this phenomena; (3)
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oxygen content, number of functional groups, and structural defects which highly depend
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on the oxidation/reduction procedures could also affect the adsorption capacities of both
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GO and rGO;9,53 and (4) the occupied adsorption space by individual molecules depends
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on molecular size and interface conformation that differ among the reported compounds.
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These differences could be overcome by using molecular dynamics (MD) simulation that
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has been employed on peptide (arginine, glutamine, and asparagine) adsorption,54
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surfactants (sodium cholate),55 fatty acids and cellulose.56 The last two factors most
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certainly are responsible for the poor correlation between surface area of GO and the
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adsorption capacity for organic molecules (Figure 2, Table S4). There are very few data
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on adsorption of metal ions by rGO, probably because the functional groups on rGO are
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not abundant enough for ion complexation and as such, has not been considered as an
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attractive material for metal ion adsorption. In addition, adsorption capacity is one of the
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main factors driving the increasing application of GFNs in various technologies. The
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approaches on the enhancement of adsorption capacity are further summarized in the
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Supporting Information.
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2.3. Implications of adsorption on GFNs. In aquatic environments, two or more
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different types of adsorbates are often co-existing. These adsorbates are likely to be co-
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adsorbed on GFN sheets. Inorganic ions are able to produce a screening or shading effect
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on the GFNs surface charge, thereby promoting the adsorption of negatively charged
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organic molecules (e.g., Bisphenol A at pH 6.0)38 and the suppression of positively
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charged organic molecules (e.g., tetracycline at pH 3.6).29 In addition, the increase in
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ionic strength (I.S.) could also cause an increased “salting-out” effect by decreasing the
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solubility of organic molecules, thus altering their adsorption onto GFNs. In comparison
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with ionized organic molecules, the influence of I.S. on the non-ionized molecules is
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minimal.57 Metal ions will preferentially adsorb onto GO rather than rGO because of the
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abundant surface functional groups.13,36,58 Unexpectedly, a screening effect and
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competitive adsorption from I.S. have minor influences on metal ion adsorption.13,59
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Instead, solution pH was shown to be a dominant factor in metal adsorption onto GO.13,42
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NOM is widely present in natural aquatic environments, and its effect on adsorption is
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more complex. NOM molecules have been reported to adsorb on GO via hydrogen bonds,
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Lewis acid-base and π-π interactions;24 the maximum adsorption of humic acid by
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graphite oxide could be as high as 190 mg/g.60 Although there are no reports on the
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interaction of NOM with rGO, strong adsorption is expected via hydrophobic and π-π
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interactions. During co-adsorption with other adsorbates such as organic molecules and
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metal ions, NOM could (1) bind/solubilize organic molecules and metal ions; (2) compete
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with organic molecules and metal ions; and (3) indirectly adsorb organic molecules and
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metal ions on GFN surface. The integrated effect of NOM on organic molecule
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adsorption was reported as suppression by Apul et al.22 This suppression was less obvious
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for biphenyl, with a flexible molecular structure, than for phenanthrene, with a planar and
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rigid molecular structure.22 Furthermore, adsorption suppression by NOM was lower on
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GFNs (both graphene and GO) than CNTs and activated carbon, both of which had
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higher micropore volumes. For metal ions, Zhao et al. reported a reduction of adsorption
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at pH < 8.0 and an insignificant effect at pH > 8.0 for Co(II) on GO in the presence of
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humic acid, while adsorption reduction was observed for Cd(II) across the whole pH
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range (2-10).13 The reduction of adsorption was attributed to stronger complexation
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activity of GO in comparison with bound humic acid on the GO surface. The effect of
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NOM on metal ion adsorption by rGO has not been evaluated. Considering the low
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complexation activity of rGO in the absence of humic acid, adsorption enhancement is
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expected. This hypothesis could be supported by the data of Lin et al.,61 where Pb(II)
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sorption on CNTs was greatly enhanced by the oxygen-containing functional groups and
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negative charges on CNT surfaces coated with humic acid.
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Desorption hysteresis on GFNs is an important phenomenon impacting the mobility
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and fate of adsorbates in aquatic environments. Desorption hysteresis may be artificial,
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and could be caused by experimental artifacts such as change of adsorption temperature,
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unachieved equilibrium, inadequate solid-liquid separation or degradation of the
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adsorbate.47 True hysteresis for carbon nanomaterials such as CNTs and C60 is explained
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by deformation-rearrangement of aggregates62 and impurities (e.g., disorderly amorphous
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carbon).63 The formation of covalent bonds between the functional groups on carbon
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nanomaterials and organic molecules is another possible reason for desorption hysteresis,
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although this has not been directly shown. For GFNs, the hysteresis phenomenon of
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organic molecules has been observed in nearly all current desorption studies.50,64,65 Zhang
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et al. attributed this hysteresis on GO to entrapment of tetrabromobisphenol A molecules
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within the highly condensed matrices.64 In our recent study, we observed two states of
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graphene sheets in aqueous solution which were responsible for the hysteresis of
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phenanthrene.65 One state was the curling and folding of graphene sheets and the other
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was surrounding the edge of a sheet that was enclosed by other sheets. Both states could
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form closed interstitial spaces and entrap phenanthrene molecules after rearrangement of
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graphene sheets in water. In addition, the sheet-sheet aggregation of GFNs could be
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induced by adsorbate molecules, and these molecules inside this sandwich-like structure
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may not be able to diffuse out through the gallery space. Although no report on this
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hypothesis has been published, it may be another reason for the observed hysteresis. Due
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to desorption hysteresis, pollutants in aquatic environments would be locked or
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sequestered within GFNs aggregates, thus decreasing contaminant bioavailability and
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environmental risk, assuming there is not particle ingestion by biota. However, the risk
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could be enhanced if the graphene-pollutant complexes are transported to different
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aquatic environments such as estuaries, or are accumulated by animals or human beings.
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GFN sheets are able to adsorb both organic molecules (e.g., amino acids, proteins) and
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inorganic ions (K+, NO3-, Co2+, and Cu2+) (Table S1). An important study by Creighton et
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al. showed a significant depletion of micronutrients such as folic acid, pyridoxine HCl
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and niacinamide upon graphene exposure,66 indicating an indirect “starvation” toxicity
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mechanism in human hepatoma cells. Similar nutrient depletion is expected to occur in
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toxicological studies with aquatic organisms, although no findings have been reported. In
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addition, GFNs with high adsorption capacity might cause artifacts during in-vitro
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toxicology assays, including preventing molecular probes from interacting with their
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targets, quenching fluorescent probes in fluorescent tests, and/or reducing/oxidizing
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probes.66,67,68 Great care needs to be taken to avoid these adsorption-related artifacts and
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false positive results during risk assessment assays.69
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3. Dispersion/aggregation behaviors of GFNs in aquatic environments
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Graphene and rGO sheets with a hydrophobic graphitic lattice tend to undergo layer-
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to-layer aggregation in water due to hydrophobic forces, whereas GO sheets with
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carboxyl, hydroxyl, and epoxy groups on the surface are able to form relatively stable
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suspensions.33 Upon release into aquatic environments, GFNs are likely to interact with
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inorganic ions, surface active molecules, NOM, colloidal particles, as well as biocolloids.
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Their dispersion/aggregation behaviors can be very complex. Moreover, the transport and
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fate of GFNs is governed by their suspension stability and this may well be altered upon
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interactions with natural system constituents.
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3.1. Dispersion/aggregation of GO. The stability of GO sheets in water is affected by
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the solution chemistry. The possible dispersion/aggregation processes are illustrated in
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Figure 3A. Electrostatic repulsion is a major driving force preventing the GO sheets from
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aggregating.70 Therefore, suspension stability of GO is pH-tunable owing to different
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ionization degrees of the functional groups on the surface. Negatively charged colloids
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with zeta potentials more than –30 mV are considered to be electrostatically stable,34
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while ASTM defines colloids more negative than –40 mV as having “good stability”.71
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Hence, GO sheets are generally stable in neutral solutions where the zeta potentials of
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GOs were reported to be –40 mV,34 –45 mV,72 and –50 mV.73 As shown in Process I of
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Figure 3A, at higher pHs, greater amounts of functional groups on the surface are ionized,
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and the dispersion becomes more electrostatically stable. At lower pHs, the functional
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groups are protonated, and individual GO sheets form layer-to-layer aggregates as
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observed from MD simulations.74 Recently, the colloidal stability of GO under
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environmentally relevant pH range was studied by Lanphere et al. (pH 5-9)75 and
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Chowdhury et al. (pH 4-10);33 findings suggest a minor influence of pH on the dispersion
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of GO in most aquatic environments.
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Due to ionized functional groups on GO surfaces, an electrical double layer (EDL) is
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formed in aquatic solutions. The presence of electrolytes is able to compress the EDL and
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screen the surface charge of GO, thus resulting in irreversible homoaggregation76
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(Process II in Figure 3A). This is supported by the results of Yoon et al.,73 in which the
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net charge on GO nanoplatelets was significantly decreased with increasing salinity
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(NaCl) at a specific pH. Lanphere et al. also reported a great decrease of net
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electrophoretic mobility and an increase of hydrodynamic diameter when the I.S. of KCl
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−
1.5
M.75 Moreover, divalent or polyvalent cations may bridge the
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was higher than 10
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functional groups on two individual GO sheets via complexation77 as illustrated in
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Process II (Figure 3A), thus inducing stronger aggregation. In addition, GO aggregation
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in electrolytes likely follows Derjaguin-Landau-Verwey-Overbeek (DLVO) theory. The
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critical coagulation concentrations (CCC) of GO were reported to be 44 and 0.9 mM for
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NaCl and CaCl2, respectively.33 However, in another report, GO nanoplatelets were stable
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and homogeneous over salinity (NaCl) concentrations up to 5 wt% (i.e., I.S. at 0.85 M),73
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indicating that this type of GFNs may still have a good stability in seawater (~3.5 wt%).
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The different GO dispersion performances could be explained by the material size and
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oxidation degree. GO sheets with smaller size and lower C/O ratio will exhibit better
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dispersion due to lower van der Waals attraction and higher electrostatic repulsion.72,73
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The interaction of GO sheets with macromolecules such as humic acids and proteins is
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shown as Process III (a,b) in Figure 3A. After adsorption on GO via π-π stacking,
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hydrogen-bonding, and Lewis acid-base interactions as described earlier, humic acid is
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able to improve the stability of GO sheets.33 Electrostatic and steric repulsions are
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responsible for the stability of colloidal particles.76 Because the coating of humic acid did
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not significantly influence GO surface charge, steric repulsion would be the major
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determinant in dispersing GO. It should be noted that this dispersion enhancement by the
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macromolecules could also be influenced by solution pH. Another possible process
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during GO-NOM interaction is bridging. Bridging has been observed between negatively
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charged TiO2 nanoparticles (NPs) and fulvic acid.78 Our previous study also found that
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hydrodynamic diameter of CuO NPs was increased in the presence of fulvic acid.79 For
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GO, bridging caused flocculation with humic acid, subsequently settling out from
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water.24 The destabilization of GO due to bridging may also occur in the presence of
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protein, which was supported by the observed GO aggregation by fetal bovine serum in
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the culture medium.76 In addition, Zinchenko et al. reported that NPs (e.g., C60(OH)n and
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CNTs) could be removed from water by entrapment within long-chain DNA-chitosan
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complexes, indicating that GO sheets may be also assembled/wrapped by long-chain
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natural macromolecules such as alginic acid and DNA.80
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Aquatic environments contain a great number of natural particles,81 and as such,
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heteroaggregation is an important process for GO sheets (Process (IV) in Figure 3A).
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Heteroaggregation of GO with two mineral clays, hematite and kaolin, was investigated
327
recently.24 For positively charged hematite, an electrostatical patching effect governed
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aggregation with GO, and resulted in a flat configuration. For negatively charged kaolin,
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the heteroaggregation with GO was through Lewis acid-base and hydrogen-bonding
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interactions after charge repulsions were overcome. There have been no reports on the
331
interaction of GO with other types of minerals such as montmorillonite and goethite.
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Interestingly, GO has been considered as an amphiphilic material with hydrophilic
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domains on the edges and hydrophobic domains on the basal plane. The GO sheets can
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disperse insoluble materials such as graphite, multi-wall CNT (MWCNT) and single-wall
335
CNT (SWCNT) to form stable suspensions through strong supramolecular π-π
336
stacking;27,72,82 the obtained suspensions were stable over two years.82 In aquatic
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environments, GO sheets are likely to interact with other solid particles which have π-
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conjugated structure (e.g., black carbon). However, GO is unlikely to disperse these
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materials in aquatic environments unless GO concentration is extremely high (25-1000
340
mg/L).72,82
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Importantly, dispersion/aggregation behaviors of GO sheets in aquatic environments
342
are governed by the synergistic effects of individual environmental factors as shown in
343
Figure 3. There is only one report focusing on natural water and natural systems
344
directly.33 In this study, a short-term (1 hour) investigation showed that aggregation of
345
GO was negligible in almost all types of water (surface water, ground water and
346
wastewater included) except for a wastewater from North Oconee and a synthetic
347
groundwater. After long-term (28 days) testing, GO sheets remained stable only in a
348
natural surface water sample from Calls Creek and several synthetic wastewaters. The
349
aggregation of GO suspension in these waters was mainly induced by I.S. and ionic
350
species (e.g., Ca2+, Mg2+) while NOM (e.g., HA) partially suppressed this destabilizing
351
effect.
352
3.2. Dispersion/aggregation of graphene and rGO. Different from GO, graphene and
353
rGO sheets are unlikely to be stable in water due to their hydrophobicity. Li and
354
coworkers developed an approach to produce aqueous rGO suspension through
355
electrostatic repulsion by increasing solution pH (pH 10) and minimizing electrolyte
356
concentration.34 However, with the addition of electrolytes (NaCl), the suspension
357
became destabilized and immediately coagulated (Process V in Figure 3B). Therefore,
358
rGO sheets in natural waters would most likely settle out as large agglomerates. Another
359
approach to enhance the stabilization is noncovalent modification through dispersant
360
amendment. Environmental dispersants such as surfactants (Process VI (c,d)) and
361
macromolecules (Process VII) could prevent rGO aggregation by disrupting the inter-
362
sheet van der Waals attractions.83
363
There are numerous studies that investigated the dispersion of graphene during
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surfactant exfoliation of graphite.84-88 Surfactants adsorbed on graphene sheets can be in
365
the form of random encapsulation, micelles or hemimicelles.89 Guardia and coworkers
366
found that nonionic surfactants (especially for Tween 80 and P-123) were more effective
367
than ionic counterparts at stabilizing graphene sheets.85 They further concluded that steric
368
repulsion (contributed by nonionic surfactants) is more efficient than electrostatic
369
repulsion (contributed by ionic surfactants). However, Lin et al. explored the aggregation
370
kinetics of graphene stabilized by the ionic surfactant sodium cholate through MD
371
simulation and theoretical modeling.55 Their results revealed that steric hindrance was
372
more important than electrostatic interactions at graphene dispersion. These conflicting
373
reports on ionic surfactants suggest that the stabilization mechanism is complex and may
374
also relate to other parameters, including maximum adsorption capacity, surfactant chain
375
length and critical micelle concentration (CMC). Other surface-active molecules such as
376
pyrene derivatives,90 amino acids91 and polyphenol92 are also able to disperse graphene
377
sheets. For all dispersants, a well-dispersed graphene suspensions still requires sonication
378
to provide the activation energy to weaken layer-to-layer van der Waals interactions
379
between the layered sheets. However, long-term sonication appears to reduce flake size
380
and produce defects and oxygen-containing functional groups.93
381
Compared to surfactants, very few dispersion studies focusing on macromolecules are
382
available. Recently, DNA molecules (oligodeoxynucleotides) were used to disperse
383
graphene sheets through MD simulations.83 DNA prevented graphene aggregation
384
through disruption of interlayer van der Waals interactions, with the dispersion being
385
dependent on DNA size and molarity. It is reported that CNT aggregation could be
386
reduced by macromolecules such as humic acid, bovine serum albumin (BSA) and
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alginate.94 Similarly, tannic acid also exhibited good dispersion performance towards
388
CNTs through steric repulsion.95 The structural similarity of graphene/rGO with CNTs
389
suggests that stable graphene/rGO dispersion by the above mentioned macromolecules is
390
likely. Additional potential dispersants in aquatic environments include fulvic acid, lipids,
391
and aromatic macromolecules.
392
4. Toxicity of GFNs to aquatic organisms
393
The risk of GFNs to aquatic environments has received increasing attention, with these
394
materials now considered to be potential environmental pollutants of emerging concern.
395
Here, we address the following questions: (1) Which organisms in aquatic environments
396
are the most sensitive to GFNs? (2) How toxic is GFN in comparison to other carbon
397
materials (e.g., CNTs, black carbon)? (3) What are the main mechanisms responsible for
398
GFN-induced toxicity at the cellular level? (4) How would environmental factors
399
influence the toxicity? The recently published studies on GFNs toxicity to aquatic
400
organisms are presented in Table S5.
401
4.1. Toxicity to different organisms. The antimicrobial activity of GFNs have
402
attracted significant scientific interest as summarized in Table S6. Minimum inhibition
403
concentrations (MICs) of rGO against four types of bacteria were much lower than the
404
antibiotic kanamycin, with MIC values being 1-8 and 64-128 µg/mL, respectively.96
405
After exposure to GO and rGO (40 mg/L) for 2 h, gram-negative E. coli had viability
406
reductions of 69.3% and 47.4%, respectively.97 For another gram-negative bacterium, P.
407
aeruginosa, 2 h median lethal concentrations (LC50) of both GO and rGO were within the
408
range of 75-100 µg/mL.98 Krishnamoorthy et al. reported that gram-negative bacteria (E.
409
coli and S. typhimuirum) were more susceptible to GFNs (rGO) than gram-positive
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bacteria (B. subtilis and E. faecalis).96 The authors attributed the higher susceptibility to
411
the thinner peptidoglycan layer of gram-negative species (7-8 nm) as compared to gram-
412
positive microbes (20-80 nm). However, the opposite result was observed by Akhavan
413
and Ghaderi,99 where increased resistance of E. coli was attributed to the gram negative
414
outer membrane that is lacking in gram-positive organisms such as S. aureus. Therefore,
415
the role of cell wall structure in minimizing GFN toxicity is unclear. In another study on
416
carbon materials, B. subtilis was resistant to both MWCNT and graphite. However, the
417
gram-positive S. epidermis had similar or lower resistance as compared to the gram-
418
negatives E. coli and P. aeruginosa.100 This indicates that antibacterial activity of GFNs
419
is bacterial species-dependent rather than gram-dependent. Moreover, these two studies
420
employed different test approaches (broth microdilution96 vs. agar dilution99), which is
421
likely another reason for the different results.
422
In-vivo antibacterial activity of graphene (graphite nanoplatelet) was reported by
423
employing a unique bacterium-nematode infection model.101 In this study, the host C.
424
elegans was first infected with the pathogenic P. aeruginosa which expressed the green
425
fluorescent protein (gfp). After infection, the bacteria could be observed in nematodes by
426
fluorescence microscopy. Interestingly, bacteria in nematode bodies cannot be detected
427
after graphene exposure, presumably due to complete inactivation of P. aeruginosa by
428
the GFN. Fourier transform infrared spectroscopy (FTIR) mapping showed that graphene
429
sheets were distributed along the nematode body, including embryos, without causing any
430
adverse effects on the animal. Similarly, insignificant toxicity of GO to C. elegans was
431
observed.102 For crustaceans, the only toxicological report was on A. amphitrite larvae,
432
with a 48 h LC50 of 560 µg/mL.103 The main overt symptoms of toxicity were swimming
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speed reduction and settlement inhibition upon GO exposure. However, there were no
434
further investigations to elucidate the mechanisms of toxicity. Zebrafish, a model fish
435
species, exhibited good resistance to GFNs (GO and multi-functional graphene) in spite
436
of complete GFN distribution from head to tail.104,105 Notably, NPs (e.g., CuO)
437
accumulated in fish muscle,106 potentially raising food safety concerns but no information
438
is available on this point. Additional research efforts are needed to focus on sub-acute and
439
chronic toxic effects of GFNs to fish and other biota after longer-term exposure.
440
Algae may be one of most vulnerable organisms to NPs in the aquatic food-chain).79,107
441
One study on algal toxicity reported EC50s (72 h) of 1.14 and 2.25 mg/L for monolayer
442
graphene and graphene nanopowder, respectively.108 To date, there are no reports on the
443
interaction of GFNs with other organisms such as ciliates, yeasts or aquatic plants (Table
444
S6). However, the toxicity of GFNs (GO) to a series of terrestrial plants (cabbage, tomato
445
and red spinach) has been reported.109 Observed visible symptoms of phytotoxicity
446
included necrotic lesions and membrane damage of leaf cells after GO (500 mg/L)
447
exposure for 20 days; notably, the damage was dose-dependent (500-2000 mg/L). Similar
448
membrane damage was recently reported from an in vitro study with Arabidopsis
449
thaliana T87 cells at a GO exposure concentration of 40 mg/L.110 The above results on
450
plants were conducted under hydroponic conditions, where GFN behavior approximates
451
aquatic environments. In comparison with terrestrial plants, aquatic plants have thinner
452
cuticles, larger air spaces inside the mesophyll layer and more stomata on the epidermal
453
surfaces.111 On the basis of these differences, aquatic plants may be more sensitive to NPs
454
such as GFNs as compared to terrestrial species. However, no comparative study has
455
been performed to verify this hypothesis.
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4.2. GO and rGO in comparison with other carbon materials. GFNs can be
457
compared to other carbon materials where sufficient toxicological data exists. GO and
458
rGO, with smaller size and thinner layers, have higher antibacterial activities than
459
graphite oxide and graphite.97 Thickness is likely a more important factor because smaller
460
lateral size did not contribute higher antibacterial activity in another study from this
461
group.112 The importance of thickness is further confirmed by an investigation with
462
crustaceans (A. amphitrite),103 in which nano-size black carbon had much lower toxicity
463
than single-layer graphene. Graphene, with sharp edges, can damage plasma membranes
464
and cause cell death.97,110 Moreover, the lower adverse effects of black carbon than GFNs
465
were also found in a cellular Arabidopsis thaliana investigation.110 Taken together, one
466
can conclude that graphene materials are more toxic than conventional carbon materials
467
such as black carbon and graphite. Conversely, fullerene and CNTs share a similar sp2
468
carbon structure with graphene, but differ in shape or conformation. Zebrafish (Danio
469
rerio) and nematodes (C. elegans) exhibited severe growth inhibition after exposure to
470
fullerols (25 mg/L)105 and MWCNTs (100 mg/L),101 respectively. However, graphene had
471
minor effects at the same concentrations. Therefore, it seems that the toxicity of graphene
472
to aquatic organisms may not be as great as carbon nanomaterials such as fullerenes and
473
CNTs. Further work needs to be done to reveal the dominant properties of GFNs that lead
474
to this lower toxicity than CNTs and fullerols.
475
It is interesting and necessary to explore the toxicity difference of graphene/rGO with
476
its derivatives such as GO and carboxylated graphene. To date, the comparative studies
477
have focused on bacteria and human cells (Table S5). rGO consistently shows more
478
pronounced adverse effects than GO in these studies, with the exception of the two
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studies on bacterium E. coli97 and human endothelial cells.113 In these two studies, the
480
authors attribute the stronger cytotoxicity of GO to its greater dispersibility, smaller
481
aggregate size and higher surface functionality; all of which increases direct contact with
482
cells and induces greater intracellular oxidative stress. However, this explanation fails in
483
several other studies in Table S5, where higher rGO toxicity was demonstrated.98,99 The
484
following explanations are proposed for the higher observed toxicity of rGO. (1) Thinner
485
monolayer sheets. The thickness of the rGO monolayer (~0.34 nm) is much smaller than
486
that of GO (~1 nm)114 due to the removal of oxygen-containing groups. Even after
487
aggregation, there would be sharp edges exposed on the surfaces because of various
488
lateral sizes, resulting in stronger and more negative interactions with cellular membranes
489
as evidenced by the efflux of cytoplasmic RNA.99 (2) Better electrical conductivity. After
490
reduction, the sp2 hybridized electron structure on the graphitized sheets is restored,
491
which can be visualized by the reduction of the ID/IG ratio from Raman spectra. The
492
electrical conductivity of rGO are therefore improved relative to GO. This improvement
493
could lead to the greater damage of cellular membranes through increasing oxidization of
494
intracellular glutathione and subsequent oxidative stress99 or by directly promoting
495
electron transfer between rGO edges and biological membranes.97 (3) Stronger
496
hydrophobicity. It is known that bacteria cells tend to associate with hydrophobic
497
surfaces as compared to hydrophilic materials.112 Thus, the hydrophobic rGO sheets
498
could more readily interact with bacteria and other cells. Subsequent nutrient absorption
499
and gas exchange across the membrane will then be hindered. The covering of GFN
500
sheets on the surface of cells/organisms was found in several studies on bacteria,97,98
501
yeast115 and plant roots.109
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4.3. Toxicity mechanisms at the cellular level. On the basis of the existing literature,
503
we propose several cytotoxic mechanisms for graphene (both GO and rGO) in Figure 4.
504
The primary mechanism will likely be the synergy between direct contact and indirect
505
oxidative stress. After exposure, monolayer or a few-layer GFN (GO and rGO) sheets are
506
able to cut and penetrate cell membranes (also the cell wall, if present), and result in
507
direct physical membrane damage.99 Another type of physical damage by GFNs is
508
destructive extraction of lipid molecules via hydrophobic effects, which has been
509
observed for E. coli by both transmission electron microscopy and computer
510
simulation.116 In addition, the covering of cells by GFNs could result in indirect growth
511
inhibition by restricting ion/gas exchange on membranes as mentioned above.
512
Single graphene sheets tend to aggregate due to van der Waals forces. Small GFN
513
aggregates (~500 nm) could be internalized through endocytosis while larger aggregates
514
(up to 5 µm) via phagocytosis. As shown in Figure 4, GFN (GO) sheets enclosed by
515
vesicles could be deposited into vacuoles after uptake.110 The internalized cytoplasmic
516
GFNs can also induce oxidative stress.98,109 In addition to the possible production of
517
reactive oxygen species (ROS) by GFNs themselves,117 ROS are mainly produced by
518
interacting of GFNs with mitochondria, chloroplasts (for plant and alga cells),
519
peroxisomes and oxidases.110 As an example, graphene may interrupt electron transfer in
520
the mitochondria by causing the overproduction of ROS. Normally, the antioxidant
521
system of cells can balance ROS production. However, excessive ROS could result in
522
subsequent cell death through a number of pathways (e.g., organelle dysfunction). Begum
523
and Fugetsu observed the dysfunction of mitochondria in plant cells (A. thaliana) but it is
524
unclear if the damage was caused directly by physical contact or indirectly induced by
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oxidative stress.110 Oxidative stress may also result in lipid peroxidation96 and the loss of
526
cell integrity. Another important toxicity mechanism is DNA damage, including nucleic
527
acid fragmentation and destruction. DNA damage has been detected in human cells after
528
incubation with GFNs,118,119 whereas no DNA damage was observed in plant cells.110
529
Similar to mitochondrial dysfunction, DNA damage may also be caused by either
530
physical damage and/or oxidative stress. GFNs internalized by endocytosis are first
531
enclosed in endosomes, but then may be released into the cytoplasm120 (Figure 4).
532
Therefore, physical damage could result from the GFN sheets which enter the cells by
533
direct penetration or from endosomal release.
534
At the cellular level, intercellular GFNs may also be subject to biodegradation and
535
exclusion after uptake (Figure 4). After internalized by macrophages, GFNs may be
536
degraded in late endosomes and lysosomes that possess digestive environments. It has
537
been reported that both in-vivo and in-vitro macrophages can degrade carboxyl
538
functionalized graphene;121 a detailed degradation mechanism will be illustrated in the
539
next section. To date, there is no literature on biodegradation of GFNs in aquatic
540
organisms. Exclusion is a type of self-defense of cells; we have quantified the exclusion
541
of CuO NPs from human cells (A549).122 Intercellular GFNs may be excluded from
542
aquatic organisms, although further investigation is needed to document this process.
543
4.4. Influence of environmental factors. To date, there is little information regarding
544
toxicity of GFNs under different environmental conditions. Current research on other
545
NPs suggests that the GFN toxicity will depend on both inherent material properties and
546
water chemistry.123 Our previous study found that DOM coating mitigated CuO NPs
547
toxicity to bacteria (E. coli) due to the hindrance of direct contact between particles and
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bacteria.79 Interestingly, the opposite result was obtained with algae (M. aeruginosa),
549
suggesting the influence of DOM may be species-dependent. GFNs are able to adsorb
550
DOM (Table S1), and this surface coating is expected to alter material toxicity to aquatic
551
organisms. In addition, I.S., ion species and pH of the water are likely to influence the
552
GFN toxicity by altering its dispersion state.
553
Co-existence of GFNs with pollutants in aquatic environments could alter the transport,
554
accumulation and toxicity of both constituents. Zhang et al. reported enhanced cadmium
555
accumulation in fish by co-addition of TiO2 NPs; the higher accumulation factor of TiO2
556
directly led to enhanced uptake of the heavy metal.124 In contrast, the bioavailable
557
fraction of a pollutant (e.g., HOCs) can be reduced if accumulation factor of the NPs
558
carrier in the test organism is lower than the adsorbed pollutant.125 Therefore, for GFNs,
559
the toxicity could be synergistic for both GFNs and the adsorbed pollutant, depending
560
both on GFN sorption capacity and the accumulation factors for both constituents in the
561
test organism. Interestingly, a recent study revealed a stress-induced toxicity of GO to
562
nematodes (C. elegans)102 by impairment of the inherent antioxidant defense system
563
under additional oxidative or thermal stress through a multiple-path mechanism. This
564
indicates that possible cooperative toxicity of GFNs may occur under other
565
environmental stresses, including co-contaminants. In addition, GO could be transformed
566
to rGO under UV irradiation126 or in the presence of reducing chemicals such as sulfur-
567
containing compounds,127 resulting in changes in the pattern of GO toxicity in aquatic
568
environments. The transformation process is reviewed in detail in the next section.
569
5. Transformation and Biodegradation of GFNs in aqueous environments
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GFNs may be transformed and degraded under ambient conditions after release into
571
aqueous environments or after uptake by biota. Until now, direct evidence on
572
transformation and degradation of GFNs in natural environments has not been reported.
573
However, there are a number of investigations under laboratory conditions (Table S7),
574
which imply the possible transformation and degradation of GO in aqueous environments.
575
5.1. Transformation of GO to rGO in aquatic solution. GO is considered as a
576
metastable material which undergoes spontaneous reduction.128,129 This reduction reaction
577
could be accelerated in the presence of UV irradiation, inorganic and organic reductants,
578
and biota (Figure 5A). Under UV irradiation, GO sheets were reduced to rGO in the
579
presence of TiO2 as a photocatalyst.130,131 This deoxygenation process was nearly
580
completed in only 2 h. In the absence of a photocatalyst, the reduction of GO aqueous
581
solution was still achieved, but only after longer irradiation times (5 h).126 However, this
582
does suggest that GO could be reduced in natural environments under longer-term UV-
583
rich irradiation.
584
Zero-valent metals such as Al132 and Fe133 were observed to be efficient reductants for
585
the deoxygenation of GO sheets in acidic solution. The possible mechanism can be
586
expressed as: GO + a·H+ + b·n·M → rGO + b·Mn+ + c·H2O. In neutral solution, the
587
reduction was not obvious after 2-days of observation. This phenomenon was explained
588
by the formation of metal oxide film on the surface of zero-valent metal, thereby
589
protecting against further oxidation.132
590
Another group of inorganic reductants important in anoxic environments such as
591
eutrophic waters are sulfur-containing compounds.134 All evaluated compounds (NaHSO3,
592
Na2SO3, Na2S2O3, Na2S, SOCl2, and SO2) reduced GO, with NaHSO3 being the most
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593
effective.127 SOCl2, which could form HSO3- when reacting with water, also showed high
594
reducing activity towards GO as indicated by the C/O ratio of the resulting rGO. The
595
transformation of GO under nitrate-reducing conditions has not yet been reported.
596
A number of organic antioxidants have been used for GO reduction in the synthesis of
597
GFNs. Polyphenols and vitamins (C and E) are two common types of natural antioxidants,
598
and both have been investigated for GO reduction. Wang et al. reported the efficient
599
reduction of GO in tea solution with the assistance of heating; the polyphenol
600
components were the main contributors to the observed transformation.135 Moreover, the
601
reducing ability of polyphenols was enhanced with iron amendment because of electron
602
donation into GO sheets and promotion of proton dissociation from polyphenols.136 For
603
vitamins, L-ascorbic acid (vitamin C) was found to yield highly reduced rGO.91,137
604
However, the reducing activity of vitamin E remains unexplored. In addition, amino acids
605
(glycine,
606
polysaccharides (natural cellulose),141 and protein (BSA, lysozyme)142,143 have been
607
shown to remove oxygen moieties on GO sheets upon reduction.
L-cysteine),138,139
saccharides
(glucose,
fructose
and
sucrose),140
608
The transformation from GO to rGO may also take place under direct interaction with
609
aquatic organisms. In aqueous solution, peeled wild carrot root was able to reduce GO;
610
the mechanism of reduction was attributed to the presence of endophytic microorganisms,
611
as evidenced by the control experiments treated with microbial inhibitors.144 Therefore,
612
this reduction most likely occurred after accumulation within the plant. In addition,
613
microorganisms could also independently reduce GO without the participation of plant
614
host. Salas et al. reported the bacterially mediated reduction of GO for the first time using
615
the environmental microbe Shewanella;145 this was verified by both Wang et al.146 and
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Jiao et al.147 More importantly, reduction by Escherichia coli, one of the most widely
617
present stains in aqueous environments, was recently observed.148 The mechanism of
618
bacterial transformation of GO involves reduction during bacterial respiration145 and
619
glycolysis.148 During these processes, electrons are generated and transferred from the
620
cell interior to GO, which acts as an external electron acceptor. Salas et al. found that
621
during respiration among the primary protein components, inner-membrane-anchored c-
622
type cytochrome (CymA) was found to be dispensable.145 This is inconsistent with the
623
findings of Jiao et al.,147 where CymA was as important as other proteins, including the
624
periplasmic (MtrA) and outer-membrane-anchored (MtrB) c-type cytochromes. There is
625
only one report on biotransformation of GO mediated by fungi.149 In this study, the epoxy
626
functionalities of GO were easily coupled with the amine groups of nicotinamide adenine
627
dinucleotide phosphate (NADPH) present in yeast, leading to the removal of oxygen
628
functionalities from the GO surface. The control group treated with yeast inhibitors was
629
conducted simultaneously, further confirming the reduction of GO sheets via yeast
630
activity. Last, poly(norepinephrine), a marine mussel-derived polymer, was shown to be
631
an effective agent for GO reduction.150
632
In order to achieve a reasonable reduction within a short time (1 min-3 days),
633
assistance by heating, sonication, specific solution pHs, and substrates (H2O2) is often
634
employed. In natural environments, reduction and transformation of GO could occur
635
spontaneously over time without amendment,128 but the reaction rates will likely be quite
636
slow. In addition to environmental media as discussed above, GO transformation is
637
expected to be promoted under other reducing conditions (e.g., sediments in a eutrophic
638
pond),134 or in the presence of other environmental reductants such as humic substances,
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flavonoids, ferulic acid, and carvacrol;151,152 however, no reports on these reducing
640
conditions have been published.
641
5.2. Degradation of GFNs in aqueous solution. Photodegradation of GO has been
642
observed in combination with TiO2 NPs in ethanol.153 In this study, GO sheets were
643
completely reduced to rGO after 2 h UV irradiation as indicated by the increasing
644
graphitized sp2 structure on graphene oxides, which is in agreement with the finding of
645
Williams et al.130 and Kim et al.131 It should be noted that the observed photodegradation
646
was only reported in ethanol; further research needs to be done on the photodegradation
647
of GFNs in aqueous solutions (indicated by the dotted arrow in Figure 5B).
648
We are aware of only two studies on biodegradation of GFNs in aqueous solution
649
(Figure 5B). Kotchey et al. reported the biodegradation of GO sheets to rGO via
650
enzymatic catalysis.21 The oxidative biodegradation by plant-derived horseradish
651
peroxidase (HRP) resulted in a number of defects and holes on the graphitic lattice of GO,
652
and the final product of oxidation was CO2, according to oxidation product analysis. The
653
active site for catalyzed biodegradation was the heme group of the HRP molecule;
654
molecular modeling suggests that the primary binding position on GO sheets was the
655
basal plane, as opposed to the rather the edge which lacks sufficient sites for stable GO-
656
HRP contacts. Furher biodegradation of rGOs was not observed in this study, which can
657
be explained as follows: (1) After binding, the distance between active heme group and
658
basal plane of rGO (11.5 Å) was longer than GO (8.7 Å), which led to unsuitable
659
interaction between Heme group and rGO sheets; (2) The functionalized groups (e.g.,
660
epoxide, hydroxyl, and carboxyl groups) on the basal plane of GFNs may act as the
661
originating point of oxidization and biodegradation by HRP, and the basal plane of rGO
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sheet lacks oxygen-containing groups (Figure 1). The lack of rGO degradation was
663
consistent with that of pristine CNTs, which are also not enzymatically degraded by
664
HRP.154,155,156 The CNT biodegradation studies did reveal that two human derived
665
enzymes, eosinophil peroxidase157 and neutrophil enzyme myeloperoxidase,158 degraded
666
carboxylated CNTs; however, the degradative capacity of these two enzymes has not
667
been verified for GFNs. Another important study revealed in-vivo biodegradation via
668
confocal Raman imaging of carboxylated graphene in tissue-bound macrophages after
669
uptake by mice.121 The structural disorder of graphene sheet was detected after 8 days,
670
and carboxylated graphene was degraded to amorphous carbon over 3 months. The in-
671
vitro study on macrophages reiterates the potential biodegradation of carboxylated
672
graphene. Interestingly, the degradation of carboxylated graphene began from the edges
673
in this study, rather than from basal plane as reported by Kotchey et al.21 This difference
674
on the primary action sites of graphene may result from the different biodegradation
675
systems (enzyme vs. macrophage); a topic that merits further investigation. In aquatic
676
environments, similar GFN biodegradation may also take place after accumulation by
677
select biota (e.g., fish) that possess cellular macrophages.
678
Thermal degradation has been shown to be effective for select polymer
679
nanocomposites.159 GO can be reduced by microwave irradiation for 1 min160 or heating
680
at 80-90 °C for 5 h in alkaline solution.161 However, the obtained rGO was resistant to
681
further degradation. Black carbon has a similar graphite-like structure as graphene;
682
residence times of black carbon in soil162 and marine waters163 were reported as 2000 and
683
2400-13900 years, respectively. If the size and surface area of these materials were not
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684
considered, the possible residence time of graphene and rGO may be expected to be
685
thousand years in the similar environments.
686
6. Challenges and Perspectives
687
We have reviewed four critical processes determining GFNs fate and disposition in
688
aquatic environments. GO preferentially adsorbs metal ions and positively charged
689
organic molecules, whereas graphene/rGO adsorb hydrophobic and aromatic molecules.
690
Because of their dissimilar surface properties, the materials exhibit distinct
691
dispersion/aggregation behaviors under environmentally relevant conditions. The toxicity
692
and transformation of GFNs has been summarized based on the currently available data.
693
However, research on the environmental behavior of GFNs is still at an early stage.
694
Considerable challenges limit the understanding the environmental fate, exposure and
695
risk of GFNs; four such challenges are identified as follows:
696
(1) Depending on synthesis routes,2,164 assisted processes165 and original graphite
697
materials;72 GFNs structural and surface properties can vary considerably. These
698
properties include lateral size, C/O ratio, and structural defects, all of which induce
699
different colloidal behaviors, adsorption capabilities and toxicities of graphene and
700
GO.22,66,72,112,165 Unfortunately, the existing literature often contains insufficient
701
information on synthesis conditions. Therefore, a more thorough and detailed description
702
on production procedures and material characterization are required.
703
(2) DLVO theory has been widely applied in colloidal stability studies. In traditional
704
DLVO theory, two colloid particles are assumed to be spherical, and the interactions are
705
dominated by summed van der Waals and EDL forces.81 The features of GFNs, including
706
chemical composition, shape and surface coating; challenge classical DLVO.55,166 For
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example, due to the two-dimensional nature, the inter-sheet attraction of GFNs could be
708
stronger than that of spherical particles because higher amounts of atoms on GFNs are in
709
close proximity to each other.81 In actual environments, bridging, steric and hydrophobic
710
forces are also present between individual GFN sheets, thus complicating the colloidal
711
system. In this case, expanded theoretical approaches are needed to accurately predict the
712
aggregation/dispersion behavior of GFNs. Hotze and coworkers have summarized
713
expanded DLVO models and the related single forces (e.g, van der Waals attraction,
714
bridging attraction) between colloidal particles,81 which will be helpful in overcoming
715
this challenge. Importantly, multiple forces co-exist in most GFN aggregation cases.
716
Therefore, new approaches should expand/modify existing DLVO theories to combine all
717
relevant forces in a specific model and distinguish their contributions for GFNs and other
718
NPs systems.
719
(3) Initially, GO was synthesized as a byproduct in the oxidative process during
720
graphene production using the oxidation/exfoliation approach.9,70 Currently, a number of
721
distinctive properties of GO that differ from graphene have been recognized, but are
722
poorly understood. It is known that GO can act as surfactant to lower interfacial energy at
723
air-water interface and can emulsify organic solvents at water-oil interfaces.27,70 However,
724
these surfactant sheets are probably unable to form micelles and do not exhibit salient
725
CMC features.74 Further, it is unknown whether GO sheets are able to solubilize/bind
726
organic pollutants similar to conventional chemical surfactants. GO sheets can also
727
spontaneously degrade to humic acid-like materials during long-time exposure (two
728
months) in water.128 Consequently, what surface activity and adsorption behavior will
729
result when the GO sheets begin to transform/degrade? What is the fate of GO in natural
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730
aquatic environments? GO behavior is not currently predictable due to lack of relevant
731
data; new approaches and analytical tools are needed to answer the above questions. For
732
example, a passive dosing technique65 is suitable to investigate the solubilization effect of
733
GO towards organic pollutants, especially when the dispersion of GO sheets is decreased
734
during the transformation/degradation period. Long-term (> 2 months) degradation
735
experiments could be conducted to explore the spontaneous degradation of GO by
736
controlling solution conditions such as sunlight irradiation, pHs and temperature.
737
(4) We reviewed the adsorption of environmental adsorbates such as organic molecules
738
and metal ions and their effects on GFN dispersion/aggregation. However, the direct
739
relationship between adsorption and dispersion is poorly understood. In the presence of
740
organic molecules or metal ions, dispersion/aggregation of GFNs could be altered as
741
reviewed above, but the influence of dispersion alteration on GFNs toxicity is poorly
742
understood. Furthermore, despite high adsorption capacity of GFNs, the risk and toxicity
743
of co-existent GFNs and other contaminants are unknown. A complete understanding of
744
the interactions among adsorption, dispersion and toxicity warrant further research in the
745
future.
746 747
ASSOCIATED CONTENT
748
Supporting Information.
749
Seven tables. This material is available free of charge via the Internet at
750
http://pubs.acs.org.
751 752
AUTHOR INFORMATION
753
Corresponding Author
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*E-mail:
[email protected] (Prof. Xing)
755
Notes
756
The authors declare no competing financial interest.
757 758 759
ACKNOWLEDGMENTS This research was in part supported by NSFC (41325013, 41328003, 41120134004),
760
USDA-AFRI (2011-67006-30181), and USDA-AFRI Hatch program (MAS 00978).
761 762
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Figures and Tables
1218
A
1219
B
1220
C
O
OH OH
O
1221
O
O
1222
Figure 1. Structural models of single-layer graphene (A), graphene oxide (B) and
1223
reduced graphene oxide (C). Functional groups such as hydroxyl, carboxyl and epoxy
1224
groups can be introduced on graphene oxide (B) after the oxidative exfoliation process.
1225
For reduced graphene oxide (C), hydroxyl and carboxyl groups could still remain on the
1226
edge of the graphitic sheets due to incomplete reduction.
1227
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2 Adsorption capacity (mmol/g)
inorganic ions on GO organic molecules on rGO 1.5
organic molecules on GO R² = 0.9359
1
0.5 R² = 0.8702 0 0
200
400 600 BET surface area (m2/g)
800
1000
1230 1231
Figure 2. Relationship between BET surface area of GFNs and Langmuir-fitted
1232
adsorption capacities for organic and metal adsorbates: Adsorption of inorganic ions and
1233
organic molecules on GO and rGO, respectively; Adsorption of organic molecules on GO.
1234
The detailed adsorption data and other information are presented in Table S4. For
1235
inorganic ions on rGO, no published data (both surface area of rGO and adsorption
1236
capacity) were found in the current literature.
1237
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Figure 3. Dispersion/aggregation behaviors of GO (A) and rGO (B) in aquatic
1240
environments. For GO, the suspension can be stable at the whole pH range of aquatic
1241
environments (pH 5-9) (I). Compression of EDL and the screening effect are responsible
1242
for the aggregation of GO at high ionic strength, and the bridging would occur when
1243
divalent or polyvalent cations are present (II). Macromolecules and colloidal particle (e.g.,
1244
clays) can also influence the stability of GO suspension (III and IV). For rGO, the sheets
1245
could only disperse at high pH and low ionic strength (V). Surfactants (both nonionic and
1246
ionic) and macromolecules, however, can disperse rGO via different mechanisms (VI and
1247
VII).
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Figure 4. Proposed interactions of GFNs with aquatic organisms at the cellular level.
1250
Direct penetration and endocytosis are two pathways for GFNs internalization by cells.
1251
The direct penetration is able to cause physical membrane damage via extracting and
1252
cutting effects. Covering on the external surface of cells could lead to indirect toxicity
1253
because of blocking ion/gas exchange. The internalized GFNs can cause oxidative stress,
1254
mitochondrial dysfunction and DNA damage.
1255
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A
1256
B
1257
1258 1259
Figure 5. Transformation and degradation of GFNs. (A) Transformation from GO to rGO
1260
with the assistance of (1) UV irradiation, (2) inorganic reductants (e.g., zero-valent
1261
metals, and sulfur-containing compounds), (3) organic compounds (e.g., polyphenols, 60
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vitamins, and proteins) and (4) organisms (e.g., bacteria, fungi and plants). (B)
1263
Photodegradation of GO under UV irradiation, and biodegradation by enzyme (e.g.,
1264
horseradish peroxidase) and macrophage. In panel B, it should be noted that the
1265
photodegradation from rGO to degraded rGO (indicated by the dotted arrow) was only
1266
reported in ethanol, no report in aquatic solution was found.
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