Noncovalent Interaction with Graphene Oxide: The Crucial Role of

Article pubs.acs.org/JPCC

Noncovalent Interaction with Graphene Oxide: The Crucial Role of Oxidative Debris Vitor R. Coluci,*,† Diego Stéfani T. Martinez,‡ Jaqueline G. Honório,† Andréia F. de Faria,‡ Daniel A. Morales,† Munir S. Skaf,§ Oswaldo L. Alves,‡ and Gisela A. Umbuzeiro† †

School of Technology, University of Campinas−UNICAMP, Limeira, SP 13484-332, Brazil Solid State Chemistry Laboratory, Institute of Chemistry, University of Campinas−UNICAMP, Campinas, SP 13081-970, Brazil § Institute of Chemistry, University of Campinas−UNICAMP, Campinas, SP 13084-862, Brazil ‡

ABSTRACT: Graphene oxide (GO) is a very promising material because it is easy to process, water-soluble, and chemically versatile due to the presence of oxygenated groups on its surface. GO has been used in different areas such as electronics, biosensing, and environmental remediation. To design efficient materials, especially for biosensing and for remediating pollutants, the knowledge of surface noncovalent interaction and functionalization is crucial. Recently, it has been suggested revisions on the structural models of GO because the presence of highly oxidized polyaromatic carboxylated fragments (oxidative debris) on the GO surfaces. These debris are produced during acid treatments commonly employed in GO synthesis and purification. Here we applied chemical analysis, bioassays, and atomistic simulations to study the influence of oxidative debris on the noncovalent interaction of GO sheets with an important organic pollutant (e.g., 1nitropyrene). GO samples without oxidative debris were found to be 75% more effective to adsorb 1-nitropyrene than samples with debris. Our results suggest that small (∼1 nm) oxidative debris are responsible for preventing adsorption sites on GO surfaces from being reached by potentially adsorbate molecules.

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INTRODUCTION Graphene oxide (GO) has been used in many applications such as nonvolatile memory,1 nanomechanical devices,2 electron field emission,3 supercapacitors,4 sensors,5,6 enzyme immobilization,7 drug delivery,8 and environmental decontamination.9−12 Besides applications, environmental, health and safety aspects of GO have been also investigated.13 GO is a functionalized graphene with oxygenated groups (e.g., −COOH, −CO, and −OH) on its structure with a C/O ratio of roughly 2:1.14,15 Alcohols and epoxides are mostly present on GO surfaces, whereas carboxylic acids lie at surface edges (Lerf−Klinowski model.14) These groups make GO a hydrophilic material that forms stable aqueous suspensions and are also important for the GO reactivity, dispersibility, and functionalization.16 Recently, Rourke et al.15 and Thomas et al.17 have shown that preparation of GO sheets by exfoliating graphite oxide with different oxidant protocols produces complex mixtures of highly oxidized polyaromatic carboxylated fragments (oxidative debris, OD) that are strongly bound to GO surface by noncovalent interactions. On the basis of those results, the actual GO structure would be composed of oxygenated functionalized graphene-like sheets with noncovalently attached OD. Representing up to a third of the whole material mass (graphene-like sheet plus debris), these debris act as surfactant, help stabilizing aqueous GO suspensions, and change the chemical environment for covalent and noncovalent interactions on GO. Faria et al.18 have shown © 2014 American Chemical Society

that debris-free GO samples induce more efficiently the formation of covalently functionalized silver nanoparticles than GO samples with OD. Additionally, Li et al.19 have demonstrated that OD significantly affect GO electrochemical behaviors. Similar to GO, the carbon nanotube surface chemistry is also influenced by these carbonaceous byproducts.20−22 Because OD change the chemical environment for covalent chemical bonds on GO surfaces, we can expect similar effect for noncovalent chemical interactions. However, studies addressing this question are still lacking. Whereas covalent interactions are important for changing electronic and reactivity GO properties, noncovalent ones are relevant for adsorption, when the capture and release of the adsorbate (a pollutant, for instance) are both necessary. Here we studied the effect of oxidative debris on the noncovalent interaction of molecules with GO surfaces. We applied a fast, low-cost bioassay, commonly used in toxicological studies, to probe the adsorption capacity of GO samples. From the bioassay results and insights from molecular dynamics simulations, we concluded that small (∼1 nm) OD indeed play an important role on noncovalent interactions, preventing adsorbates from reaching favorable adsorption sites on GO surfaces. Received: September 23, 2013 Revised: January 10, 2014 Published: January 10, 2014 2187

dx.doi.org/10.1021/jp409501g | J. Phys. Chem. C 2014, 118, 2187−2193

The Journal of Physical Chemistry C

Article

Figure 1. Schematic illustration showing the sample preparation steps and the biological assay (Ames test) used to probe the adsorption capacity of GO samples.

Table 1. Ames Test Results for TA98 Strain without Metabolic Activationa average number of revertants per plate ± standard deviation (MR) 1-NP + raw-GO

1-NP + df-GO

dose of 1-NP (ng/plate)

1-NP

10 μg/plate

50 μg/plate

100 μg/plate

10 μg/plate

50 μg/plate

0 10 30 100 300 1000

20 ± 5 33 ± 1(1,6) 42 ± 2(2,1) 144 ± 1(7,2) 398 ± 77(19,9) 893 ± 77(44,6)

20 ± 0 25 ± 3(1,3) 51 ± 2(2,6) 81 ± 2(4,1) 286 ± 82(14,3) 724 ± 4(36,2)

23 ± 7 27 ± 1(1,2) 44 ± 4(1,9) 52 ± 10(2,3) 180 ± 13(7,8) 875 ± 93(38,0)

23 ± 4 24 ± 2(1,1) 31 ± 1(1,4) 48 ± 3(2,1) 138 ± 35(6,1) 641 ± 37(28,5)

28 ± 9 6 ± 2(0,6) 29 ± 5(1,0) 35 ± 5(1,0) 81 ± 8(2,9) 480 ± 196(17,1)

21 ± 2 20 ± 4(1,0) 28 ± 8(1,3) 28 ± 9(1,3) 31 ± 1(1,5) 152 ± 6(7,2)

100 μg/plate 18 23 25 25 24 56

± ± ± ± ± ±

2 2(1,3) 4(1,4) 2(1,4) 4(1,3) 12(3,2)

a

Average number of revertants per plate and the mutagenic ratio (MR = induced and spontaneous revertants/spontaneous revertants) are presented for different amounts of 1-NP and GO. MR values greater than 2 indicate mutagenic activity.

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EXPERIMENTAL SECTION We prepared the GO samples according to Figure 1. Commercially available (Cheap Tubes, Ballteboro, USA) single-layered GO sheets (raw-GO and as-purchased GO) were produced by exfoliating graphite with a mixture of potassium permanganate and concentrated sulfuric acid (modified Hummers method23). We also prepared debris-free GO (df-GO) samples from rawGO, the same samples prepared and characterized by Faria et al.18 First, 0.5 mg mL−1 of raw-GO was sonicated for 30 min in an ultrasound bath (Cole-Parmer 8891, 40 kHz) and then, after a 90 min reflux in a 0.1 mol L−1 NaOH solution, produced a suspension comprising a light-brown supernatant and a black pelletized sediment. Second, we filtered this suspension to separate the black pellets from the supernatant. Finally, the reprotonated (1.0 mol L−1 HCl solution), dialyzed, lyophilized black sediment was used as df-GO. The effect of OD on the noncovalent interaction of molecules with GO was indirectly measured by the capacity of GO sheets to adsorb aromatic molecules. The mutagenicity tests were carried out with the Salmonella typhimurium mutagenicity assay (also known as Ames test24), which is a short-term test, very simple and easy to perform. It is based on the property of different mutants of Salmonella typhimurium to revert from its inability to grow without the supplementation of histidine, to its independence of this aminoacid. Substances that are able to penetrate the bacteria and cause genetic mutations can be detected using this assay. Some substances show strong responses in this assay such as the nitro polycyclic aromatic hydrocarbons. The Ames test is very sensitive to 1-nitropyrene (1-NP), a well-known organic pollutant that is produced from

incomplete combustion of fossil fuels and different types of natural biomass,25−27 and it was successfully applied to study the interactions of 1-NP and multiwalled carbon nanotubes.28 The sensitivity of the assay can be expressed by the minimum dose per plate that can provide a positive response, defined by the double of the background revertants of the Salmonella mutants. The results of the test can also be expressed as the number of revertants (induced by the mutations) per unit of mass of the tested compound, known as the potency of the compound in this specific assay. For 1-NP, 30 ng/plate (∼10 nmol L−1) is sufficient to provide a positive response in the TA98 strain, which was used in the test (Table 1). Therefore, we choose 1-NP as the probe molecule (adsorbate) to determine the GO adsorption capacity, in a way that only nonadsorbed 1-NP molecules will be free to cause mutations on Salmonella DNA (Figure 1). The Ames test was performed according ISO 16240:2005. 1NP (99% Sigma-Aldrich St. Louis MO) was dissolved in dimethylsulfoxide for testing (Sigma-Aldrich, St. Louis, MO). We employed the most sensitive condition for the detection of 1-NP mutagenicity using TA98 strain without metabolic activation. Stock solution dispersions of raw-GO and df-GO at 100 μg/mL sterile ultrapure water were sonicated at room temperature for 90 min. We incubated different concentrations of raw-GO/df-GO with 1-NP for 2 h before adding the bacteria culture. The plates were incubated at 37 °C for 66 h, and the numbers of induced/spontaneous colonies were manually counted under a stereomicroscope. We used sterile ultrapure water and dimethylsulfoxide as negative control and 0.5 μg/ plate of 4-nitroquinoline 1-oxide as positive control. We performed duplicate plates with 10, 50, and 100 μg/plate GO doses, and 10, 30, 100, 300, and 1000 ng/plate 1-NP doses. 2188



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Table 2. Ames Test Results for TA98 Strain without Metabolic Activationa raw-GO

df-GO

dose (μg/plate)

plate 1

plate 2

average

MR

plate 1

plate 2

average

MR

0 10 25 50 100

13 18 20 17 13

15 15 17 24 16

14 17 19 21 15

1,2 1,3 1,5 1,1

13 16 23 16 21

15 20 17 21 19

14 18 20 19 20

1,3 1,4 1,3 1,4

a

Average number of revertants per plate and the mutagenic ratio (MR = induced and spontaneous revertants/spontaneous revertants) for raw-GO and df-GO samples.

Like 1-NP molecules, GO sheets could also, in principle, enter into the Salmonella cells and cause mutations. However, different studies using Ames test have shown negative responses to carbonaceous nanomaterials, and the inability of Salmonella to absorb nanomaterials has been suggested.29 We tested GO both with and without OD using Ames test, and the samples were not able to revert TA98 under the tested conditions (Table 2). Therefore, we can safely assume that GO does not enter the Salmonella cell, similarly to the case of carbon nanotubes,28 and that only 1-NP molecules are responsible to cause mutations. Thus, we used the inverse potency of 1-NP as a measure proportional to the amount of 1NP adsorbed on GO surfaces.

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Figure 2. TEM images of (a) raw-GO and (b) df-GO samples. Insert: Photographs of GO suspensions (stock solution at 0.5 mg/mL) in deionized water.

SIMULATION METHODS Therefore, we can consider that df-GO still shows oxygenated groups covalently bonded to the sheets that allow the formation of stable suspensions in deionized water. Spectroscopy studies showed that raw-GO and df-GO present a mixture of oxygenated groups, specially, epoxy, hydroxyl, and carboxyl groups. However, after treating with NaOH, a decrease in the quantity of oxygen moieties in GO was observed due to the removal of OD. Thermogravimetric analyses (TGA) have also supported the removal of OD from raw-GO after the NaOH treatment. We observed by TGA that approximately 14% in weight of our raw-GO samples are attributed to OD, which is roughly half of that previously obtained by Rourke et al.15 This difference in the amount of OD generated is not unexpected. Although the amount of debris is apparently relatively insensitive to preparation,17 the different types of graphite source used might play a role, but this question was not addressed here. Further detailed physicochemical characterization (AFM, FT-IR, Raman, XPS, UV−vis, TGA, and suspension stability analysis) of raw-GO, df-GO, and OD samples have been already reported.18 Adding GO on 1-NP incubation solutions reduced the average number of revertants per plate for 93% of 1-NP/GO dose ratios used here (Table 1). The reduction is larger for dfGO samples than for raw-GO ones. Whereas raw-GO samples show an average reduction of 36%, df-GO show 63%. This indicates that df-GO are more efficient in capturing 1-NP molecules in water. We observed different adsorption behaviors for raw-GO and df-GO samples (Figure 3). For 1-NP/GO dose ratio smaller than 0.005 (dashed vertical line in Figure 3), dfGO exhibits almost no variation on the inverse potency, which indicates that all 1-NP (within the limit of sensitivity) are adsorbed by GO. Adsorption is reduced when the amount of 1NP is increased, as indicated by the decreasing inverse potency after the 1-NP/GO dose ratio of 0.005. In principle, GO sheets can also inhibit bacteria growth by means other than DNA mutations. Conflicting reports have

To investigate the effect of OD on the 1-NP adsorption, we carried out atomistic simulations based on classical molecular dynamics (MD). Our model system comprised a single GO sheet oriented along the xy plane, 10 1-NP molecules, and water in a simulation box (3.4 × 3.4 × 7.0 nm3) with periodic boundary conditions applied in all directions. To study the role of small OD, we considered different OD amounts: none, 2, 4, 6, and 8 OD molecules, initially placed near the GO surface and symmetrically distributed along the z-direction. The model for the small OD was the highly oxidized C28O19H12,15 which is approximately 1 nm sideways. The simulations were carried out at the Large-scale Atomic/Molecular Massively Parallel Simulator (Lammps)30,31 using the Verlet algorithm with a time step 0.5 fs to integrate the equations of motion in the NPT ensemble (300 K and 1 atm), lasting 8 ns in production runs. We used the ReaxFF force field32 with the parameters obtained from33,34 to describe the covalent and noncovalent interactions of the 1-NP/OD/GO system. Originally developed for hydrocarbons, the ReaxFF has also been used to describe the structural evolution of GO35,36 and the mechanical properties of GO composites in the presence of water37,38 and of organic molecules like DNA.39

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RESULTS AND DISCUSSION Raw-GO samples consist of GO single-layered sheets and OD.18 The size distribution of OD showed a typical mean size of 50 nm, as observed from atomic force microscopy images.18 However, smaller OD (∼1 nm) are also expected to be present on raw-GO sample as previously revealed by mass spectrometry analysis.15 Transmission electronic microscopy (TEM) images of dried GO samples on holey carbon grids show different morphologies (Figure 2). Raw-GO exhibits visible flat surfaces (Figure 2a), whereas df-GO appears crumpled (Figure 2b). Both samples showed good water dispersibility and stability (see inset photographs in Figure 2). 2189



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adsorption on the condition of high 1-NP doses (or equivalently low GO amounts), the effect is not expected to be important for low 1-NP doses, and therefore, competition among 1-NP is not likely responsible for the decreasing of adsorption on raw-GO. Because df-GO samples are produced from raw-GO ones, we considered the adsorption reduction to be associated to the excess in mass on raw-GO samples. However, by considering the largest 1-NP dose used here (1000 ng/plate) as the reference for the mutagenic ratio on the performed Ames tests, we observed a reduction in the mutagenic ratio of 36% and 93% for 1-NP/raw-GO and 1-NP/df-GO samples with 100 μg/ plate, respectively (Table 1). This reduction on the mutagenic ratio of the samples after OD removal cannot be explained considering solely the OD mass effect of raw-GO (∼14%). Therefore, we attribute the reduction of the adsorption on rawGO for dose ratios smaller than 0.005 to the presence of OD. Assuming that all GO surfaces are accessible for adsorption and that all OD (∼14% of the total GO mass with typical mean (large) size of 50 nm18) are adsorbed on GO, we estimated the coverage of OD and 1-NP (size ∼1 nm) on GO surfaces for different amounts of 1-NP as illustrated in Figure 4. For the

Figure 3. Adsorption behavior obtained from mutagenicity tests (Table 1) for raw-GO and df-GO samples for different 1-NP/GO dose ratios. Vertical dashed line indicates the value 0.005 of 1-NP/GO dose ratio. Full lines are only guides to the eye.

been published about bactericidal activity of GO, likely related to different methods, bacteria strains, and material characteristics and preparation. Some studies reported viability loss of gram-negative and -positive bacteria exposed to GO,40,41 whereas others find GO to exhibit no antibacterial or bacteriostatic properties.42,43 To verify whether our GO samples were cytotoxic when exposed to different doses in the Salmonella assay using the same protocol applied in this study, we carefully observed the background of the plates under a stereomicroscope. No toxicity or reduction in the number of revertants per plate was detected (Table 2), which rules out the effect of GO cytotoxicity on the GO adsorption capability. Therefore, we associated the reduction of the df-GO adsorption capacity to the reduction of the available surface area for the 1NP adsorption. Assuming that all GO surface is available for adsorption, we can estimate the available surface area for a 1NP molecule (S) as a function of the 1-NP mass (M), the specific surface area of GO (SA), and the ratio between the GO dose (D) and the 1-NP dose (d), i.e., S = (SA × M)D/d.28 For d/D = 0.005 (Figure 3) and SA = 800 m2/g,44 S = 67 nm2, which corresponds to a square of side approximately 8 nm. For d/D = 0.1, S is reduced to about 4 nm2. The actual values for the available surface area for 1-NP are probably smaller than the ones we estimated, mainly because some regions of the GO surface may be inaccessible for adsorption. One factor that can reduce the available surface area is the crumpled nature of the df-GO sheets (Figure 2b), which can hide adsorption sites that would be accessible if the GO sheets were totally flat. Therefore, we suggest that the decreasing of the adsorption capacity of df-GO occurs because the competition among 1-NP molecules for room on GO surfaces. For relatively large 1-NP doses (or equivalently to relatively small GO amounts), the probability of 1-NP molecules to reach a region occupied by another 1-NP is high. In this case, the incoming 1-NP is not adsorbed and becomes bioavailable to enter the bacteria and cause mutation on the Salmonella DNA, consequently increasing the number of revertants per plate. Similarly to df-GO samples, we also observed the competition effect for raw-GO for 1-NP/GO dose ratios larger than 0.005. However, the adsorption begins to decrease from the smallest dose ratio used here. Although the competition for space among 1-NP molecules may reduce the available area for

Figure 4. Schematic representation of the estimated coverage of large (40−60 nm) OD and 1-NP on a 400 × 400 nm2 GO surface for (a) 0.001, (b) 0.01, and (c) 0.1 1-NP/GO dose ratios. Filled squares represent OD, whereas dots represent 1-NP molecules (∼1 nm). The number of 1-NP molecules is 50 (a), 500 (b), and 5000 (c).

dose ratio of 0.001 (Figure 4a), 1-NP molecules have plenty of available space to adsorb on GO surface, even on top of OD, which presents similar chemical surface characteristics to GO. Space can become limited for a dose ratio of 0.1 (Figure 4c). However, even for this high dose ratio, we do not expect 1-NP adsorption to diminish in the presence of a large OD because of the chemical surface similarity. Therefore, large OD alone would not be responsible for limiting 1-NP adsorption, and we attribute the limitation on adsorption to small OD (∼1 nm) also presented in raw-GO samples. These small OD have dimensions comparable to that of a 1-NP molecule, and a large 60 × 60 nm2 OD is equivalent, in terms of size, to ∼3600 OD measuring 1 × 1 nm2. This number is comparable to the number of 1-NP in the case of 0.1 1-NP/GO dose ratio (Figure 4c). Our MD results show that, for the same simulation time, 1NP can reach the surface on the debris-free system and stay in close vicinity to the surface for at least 4 ns (Figure 5a), whereas the presence of OD seems to prevent 1-NP molecules from reaching adsorbing GO surface sites (Figure 5b). This behavior can also be seen through the atomic density profiles (Figure 6) where a more spread 1-NP distribution close to GO is observed when the OD are present, indicating that 1-NP does not adsorb as effectively as in the debris-free GO surface. 1-NP molecules can reach the GO surface individually (Figure 5a) or as a group (Figure 7a). Even when OD is present but there is free space for adsorption, a group of 1-NP molecules can reach the surface and adsorb on it (Figure 7a). 2190



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Figure 7. Snapshots of MD simulations showing (a) the adsorption of 1-NP molecules (indicated by arrows) and (b) the blocking effect on a group of 1-NP molecules (dashed rectangle) caused by the presence of an OD on the GO surface. Figure 5. Snapshots of MD simulations of GO system (a) without and (b) with debris. Hydrogen and oxygen atoms in GO, debris, and 1-NP are not shown for clarity. Water molecules are represented as red dots and nitrogen atoms as blue spheres. In panel a, the dashed circle indicates a group of five 1-NP molecules and arrows indicate 1-NP molecules adsorbed on GO surface. The locations of some OD are indicated by dashed squares in panel b.

The separation of individual molecules from the group toward the surface indicates a stronger interaction between 1-NP and GO than between 1-NP molecules themselves. In cases where OD are present (Figure 7b), even a single OD may interfere negatively on the adsorption mechanism of the 1-NP group for a relatively long time (∼2 ns) as it approaches the GO surface.

Figure 6. Time evolution of the atomic density profile of the simulation box along z-direction for the system without (left) and with (right) debris. Carbon and nitrogen atom distributions are depicted in red and blue, respectively. The number of nitrogen atoms are multiplied by 50 for clarity. 2191



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CONCLUSIONS We have shown that oxidative debris adsorbed on graphene oxide surfaces play an important role on the noncovalent interaction with aromatic compounds such as 1-nitropyrene. We suggest that mainly oxidative debris of sizes comparable to 1-NP molecules (∼1 nm) are responsible for obstructing adsorption sites on the GO surface. By removing these oxidative byproducts from graphene oxide surfaces, we were able to increase its adsorption capacity, obtaining graphene oxide samples that are 75% more effective to adsorb 1nitropyrene than samples with debris. Our results indicate that oxidative debris should be taken into account in processes involving noncovalent functionalization of graphene oxide nanosheets.

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AUTHOR INFORMATION

Corresponding Author

*(V.R.C.) E-mail: [email protected]. Phone: +55 (19) 2113 3401. Fax: +55 (19) 2113 3364. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by CIGENANOTOX, INOMAT, CNPq, CAPES, and FAPESP (grants 2010/50646-6 and 2013/ 13640-8). The authors thank Dr. Amauri J. Paula for TEM analyses.

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