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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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Environmental Science & Technology

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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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1

ACS Paragon Plus Environment


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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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TOC art:

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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

292

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

300

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

311

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

313

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

315

charged TiO2 nanoparticles (NPs) and fulvic acid.78 Our previous study also found that

316

hydrodynamic diameter of CuO NPs was increased in the presence of fulvic acid.79 For

317

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

320

the culture medium.76 In addition, Zinchenko et al. reported that NPs (e.g., C60(OH)n and

321

CNTs) could be removed from water by entrapment within long-chain DNA-chitosan

322

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,

325

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

328

aggregation with GO, and resulted in a flat configuration. For negatively charged kaolin,

329

the heteroaggregation with GO was through Lewis acid-base and hydrogen-bonding

330

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

333

domains on the edges and hydrophobic domains on the basal plane. The GO sheets can

334

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

337

environments, GO sheets are likely to interact with other solid particles which have π-

338

conjugated structure (e.g., black carbon). However, GO is unlikely to disperse these

339

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

17



364

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

18


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387

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

19



410

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

20


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433

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.

21



456

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

22


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479

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

23



502

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

24


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525

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

25



548

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

26


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570

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

27



Page 28 of 61

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

28


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616

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,

29



639

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

30


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662

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

31



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

32


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707

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

33



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

34


Page 34 of 61

Page 35 of 61


754

*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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1214 1215

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1216

55



1217

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

56


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1228 1229

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

57



1238 1239

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).

58


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1248 1249

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

59



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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1262

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.

61


Adsorption, Dispersion, Toxicity and Transformation - American

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