Environ. Sci. Technol. 2005, 39, 1359-1365
Fullerol-Sensitized Production of Reactive Oxygen Species in Aqueous Solution K. D. PICKERING AND M. R. WIESNER* Department of Civil and Environmental Engineering, Rice University, 6100 Main Street, Houston, Texas 77005-1892
The relative production rate of reactive oxygen in aqueous solution sensitized by fullerol (a polyhydroxylated, watersoluble form of the fullerene C60) was measured and compared to known reactive oxygen sensitizers using an oxygen consumption method. The solutions were irradiated by polychromatic visible and ultraviolet light. Reactive oxygen species were generated under both visible and ultraviolet light sources. The greatest rates of oxygen consumption were observed at acidic pH. We show for the first time evidence of both singlet oxygen and superoxide production by fullerol under both UV and polychromatic light sources.
Introduction Fullerene-based nanomaterials are emerging in a variety of potential applications, including energy production (1), semiconductors (2), and medical treatments (3) Buckminsterfullerene (C60), a hydrophobic molecule made up of 60 carbon molecules arranged in a characteristic soccer ball shape, is the backbone of the fullerene-based nanomaterials family. The symmetry and conjugated π-bond system of C60 (4) result in a number of unique properties, including high reactivity to nucleophiles, (5), electron affinity (6, 7), and photsensitization (8). Because of its extremely low solubility in water (9), monomeric C60 is unlikely to have a significant effect in aqueous systems. However, C60 can be modified in a variety of ways to make it water-soluble. C60 may be functionalized by the addition of hydrophilic functional groups (10), which increase the water solubility of the derivatized compound. In addition, C60 may form highly stable colloidal aggregates (n-C60) through the rapid mixing with water of fullerene solutions in a variety of organic solvents (11-13) or through long-duration stirring or sonification of C60 in water (14, 15). Aggregation and solubilization lead to fullerene colloids of varying size, depending upon the conditions of formation. The impacts of these derivatized compounds in aqueous systems are largely unknown. However one recent study (16) concluded that n-C60 produced oxidative damage in the brains of largemouth bass. A later study (17) found relatively high toxicity of n-C60 in experiments with human tissue cultures, while fullerols exhibited negligible toxicity. They speculated that toxicity was due to oxidative damage to cell membranes from superoxide anion radicals produced by n-C60. A variety of reactive oxygen species (ROS) may result from the exposure of a photosensitizer to light. Initial species may include singlet oxygen and superoxide. Subsequent reactions of these reactive species lead to the formation of secondary * Corresponding author telephone: (713)348-5129; fax: (713)3485203; e-mail:
[email protected]. 10.1021/es048940x CCC: $30.25 Published on Web 01/21/2005
2005 American Chemical Society
ROS, such as hydroxyl radicals, hydrogen peroxide, or perhydroxyl radicals. Singlet oxygen (1O2), a highly reactive, electrophilic, and nonradical molecule (18), can be generated in both the laboratory and the environment through photosensitization. 1 O2 is a selective oxidant, reacting principally with compounds containing electron-rich double bonds; compounds containing easily oxidized functional groups such as sulfides, anilines, and phenols; or compounds prone to Diels-Alder reactions. Arbogast et al. (8) first reported singlet oxygen production by fullerene in 1991. Later research demonstrated that fullerene in a benzene-methanol solution produced singlet oxygen at a rate 4.8 times greater than rose bengal when excited by 514.4 nm laser light (19). Flash photolysis studies of fullerol, a polyhydroxylated fullerene compound, and other water-soluble fullerene compounds revealed decreased rate constants for singlet oxygen generation with increasing derivatization; however, the production of singlet oxygen was observed with all derivatized fullerenes (20). Superoxide (O2•-), a radical anion formed from a oneelectron reduction of oxygen, is another reactive oxygen species generated through photosensitization. Superoxide dismutates rapidly in water to hydrogen peroxide. Although previous researchers have studied the photophysical properties of water-soluble fullerenes using techniques such as laser flash photolysis or pulse radiolysis (2124), this work is the first to consider the photosensitizing properties of fullerol under polychromatic, steady-state irradiation. Other research has shown that the production of oxidative species is up to 2 orders of magnitude greater using laser flash photolysis when compared to the use of steady-state irradiations of more environmental application (25) The aim of this work is to characterize the ability of fullerol to generate ROS. The implication of this capability is 2-fold. First, efficient production of ROS by fullerol may enable development of processes for oxidation of organic materials or disinfection. Second, as nanomaterial production increases due to development and commercialization of new applications, there is a need to understand the effect of ROS generation by fullerene nanoparticles on human health and natural environmental systems (26).
Experimental Section Chemicals. Furfuryl alcohol, humic acid, and superoxide dismutase (bovine ethyrocytes) were obtained from SigmaAldrich (St. Louis, MO). Fullerol (C60(OH)24) was purchased from MER (Tucson, AZ). Rose bengal and methylene blue were purchased from Acros Organics (Fairlawn, NJ). Sodium hydroxide, potassium hydrogen phthalate, potassium dihydrogen phosphate, and sodium tetraborate were purchased from Fisher Scientific (Fairlawn, NJ). pH was buffered at values of 5, 7, and 10 using 50 mM potassium hydrogen phthalate, 50 mM potassium dihydrogen phosphate, and 12.5 mM sodium tetraborate, respectively (27). Instrumentation. Oxygen consumption was measured using a polarographic oxygen sensor (ThermoOrion meter 830A, probe 083019A). pH was measured electrochemically (ThermoOrion meter EA940, probe 9104BN). Irradiation. The ultraviolet light experiments were carried out using two 15W fluorescent ultraviolet bulbs (Philips TLD 15W/08). These bulbs have an output spectrum ranging from 310 to 400 nm, with a peak at 365 nm. The visible light experiments were conducted using four 40W fluorescent fullspectrum bulbs (Philips F40C50). The output spectrum is designed to mimic full-spectrum daylight (28). The spectral distribution of both light sources is presented in Figure 1. VOL. 39, NO. 5, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 1. Spectral distribution of (a) ultraviolet lamp (Philips TLD 15W/08) and (b) visible light (Philips F40C50). Spectral distribution was measured using a Li-Cor 1800 spectroradiometer. Total irradiance of the UV lamps was 24.1 W/m2, while the visible light irradiance was 150.5 W/m2. Measurement of Oxygen Consumption. Oxygen consumption by an acceptor compound can be used to confirm the photochemical production of reactive oxygen species (29). An effective acceptor has a greater rate of reaction (kr) than the natural rate of decay of the ROS (kd). Several compounds for which kr . kd have been used as 1O2 acceptors, including histidine, tryptophan (30-32), and 2,5-dimethylfuran (DMF) (33, 34). However, the compound most frequently used as a singlet oxygen acceptor is furfuryl alcohol (FFA) (30, 35-40), with a second-order rate constant of 1.2 × 108 M s-1 (36). Although DMF is more sensitive than FFA, with a reaction rate constant 5 times faster than FFA, FFA and DMF produce comparable results for concentrations of singlet oxygen present in natural waters (36, 41). In addition, the reaction of FFA with singlet oxygen is independent of pH over the range of 5-12 (42). A concentration of 100 mM furfuryl alcohol was selected for measurement of relative quantum yield, similar to 1360
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concentrations used in previous studies (30, 36, 39, 43) At this concentration, a large excess of 1O2 acceptor ensures ∆[Ο2] ) ∆[Ο2]max and ensures that all the singlet oxygen generated was trapped by the substrate. This enables a comparison of various sensitizers and determination of a relative quantum yield. Confirmation of a reaction can also be obtained using a known quencher, or scavenger, for a specific reaction. A quencher molecule interferes in a reaction but does not react with the compound of interest. A variety of compounds are capable of quenching 1O2 reactions, including azide ions, tocopherol, and β-carotene (44). The quenching reaction by the azide ion (N3-) is shown in eq 1 (43), with a rate constant of 2 × 109 M s-1 (45): 1
kq ′
O2 + N3- 98 N3- + O2
(1)
A number of studies have reported 70% to nearly 100% quenching of singlet oxygen production by azide ions. Researchers have used a variety of sensitizers for 1O2
FIGURE 2. Oxygen consumption in fullerol/FFA solution under (a) visible light and (b) ultraviolet light. Fullerol 1 µM, FFA 100 mM. generation, including porphyrin compounds (43), L-aspartyl chlorin (39), calcein (30), chlorophyll (31), 3-hydroxyflavothione (46), and antibiotic quinolones (47). Azide concentrations ranged from 5 to 100 mM in these studies. For each irradiation experiment, four borosilicate glass vials with PTFE-lined caps were filled with a solution consisting of 100 mM furfuryl alcohol in aerated buffer and 1 µM fullerol or other sensitizer. Three vials were exposed to light, while a fourth vial was double-wrapped in aluminum foil and used as the control sample. The dark control was kept with the three vials exposed to light in order to ensure the only variable between the irradiated solutions, and the control solution was exposure to light. Oxygen consumption was calculated as the difference in dissolved oxygen con-
centration of the control vial and the average dissolved oxygen concentration of the three vials exposed to light.
Results and Discussion Fullerol-Sensitized Production of Reactive Oxygen Species. The consumption of oxygen in the presence of 1 µM fullerol and 100 mM furfuryl alcohol was measured over time at varying pH. Oxygen consumption followed first-order reaction kinetics, with the greatest rates of oxygen consumption observed at pH 5. Little difference was observed between oxygen consumption monitored at pH 7 and pH 10. This trend was observed with both visible (Figure 2a) and ultraviolet light (Figure 2b). These results agree with prior VOL. 39, NO. 5, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 1. First Order Rate Constants for the Reaction of Oxygen with Furfuryl Alcohola
SCHEME 1. Potential Reaction Photosensitized Production of ROS
Mechanisms
for
rate constant (min-1) pH
UV
6.46 × 10-5 4.07 × 10-6 4.39 × 10-6
1.16 × 9.09 × 10-5 6.47 × 10-5
5 7 10 a
visible 10-3
Rate constants are normalized by spectral irradiance.
TABLE 3. Decrease in Oxygen Consumption normalized by Irradiancea
TABLE 2. Reduction in Total Oxygen Consumption in the Presence of Quenchersa
decrease in oxygen consumption/irradiance unit [(mg of O2 consumed/L)/(W/m2)) UV
% decrease in oxygen consumption UV
visible
pH
100 mM azide
1 unit/min SOD
100 mM azide
1 unit/min SOD
5 7 10
75 22 15
65
71 13 14
93
a
visible
pH
100 mM azide
1 unit/min SOD
100 mM azide
1 unit/min SOD
5 7 10
4.15 × 10-3 1.75 × 10-4 8.63 × 10-5
3.66 × 10-3
3.18 × 10-4 1.56 × 10-5 1.56 × 10-5
3.93 × 10-4
a Values shown represent the difference in oxygen consumption in fullerol/FFA solutions and fullerol/FFA/quencher solutions.
Fullerol ) 1 µM, FFA ) 100 mM, SOD ) 1 unit/mL, NaN3 ) 100 mM.
research (34), which determined that, in general, higher rates of oxidation of FFA are observed at lower pH. Normalized by irradiance, ultraviolet light resulted in greater rates of reaction than did irradiation by visible light for a given pH (Table 1). A higher reactivity of fullerol in UV light is likely due in part to its optical absorbance spectrum, which peaks at 215 nm (22). Optical absorption by fullerol is 2-3 times greater in the range of 300-400 nm than in visible wavelength ranges. Quenching of Reactive Oxygen Species. To confirm fullerol-sensitized production of singlet oxygen, the reaction was quenched with sodium azide, an efficient singlet oxygen scavenger (48). In fullerol-sensitized photooxidation, the oxygen consumption in the presence of azide varied according to pH at a N3- concentration of 100 mM, as shown in Table 2. Quenching was more complete at acidic pH, similar to results reported by Inbaraj (49). Incomplete quenching by N3implies a second reaction that contributes to the consumption of oxygen (50). The possibility of oxygen consumption due to a direct reaction of fullerol with singlet oxygen was eliminated by irradiation of fullerol in an oxygenated solution. Under these conditions, no consumption of oxygen was observed in the absence of FFA, confirming that fullerol did not act as a singlet oxygen acceptor. Although numerous researchers have used FFA as a specific 1O2 acceptor, further investigation was necessary to rule out participation by other reactive oxygen species. A second potential pathway for oxygen consumption could be the production of superoxide radicals that subsequently reacted with FFA. A similar fullerol compound, C60(OH)18, has been shown to form the radical anion of fullerol, (C60(OH)18•-) (23, 51). Formation of the radical anion can be a precursor for the formation of superoxide anion via a Type I photochemical reaction. Although FFA has generally been used as a specific singlet oxygen acceptor, a reaction of FFA with superoxide has been reported at FFA concentrations greater than 10 mM (52, 53). To determine if superoxide participates in the consumption of oxygen by FFA in the current study, superoxide dismutase (SOD) was added to the fullerol/FFA solution for a final concentration of 1 enzyme unit SOD/mL (54), at pH 5. SOD is an enzyme produced by a wide range of organisms that catalyzes superoxide conversion to peroxide according to eq 1362
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2, thereby accelerating the natural dismutation of superoxide and preventing its reaction with other substrates (50): SOD
2O2•- + 2H+ 98 H2O2 + O2
(2)
When SOD was added to the fullerol/FFA solution, oxygen consumption decreased by 93% during visible light irradiation and 65% under UV light irradiation. These results indicate that superoxide plays a large role in the consumption of oxygen by FFA. The proposed reactions for the photosensitized production of superoxide and singlet oxygen by fullerol are shown in Scheme 1. We note that the standard buffer used at pH 5 in these experiments was potassium hydrogen phthalate. The phthalate anion is an aromatic carbon molecule, which has been found to form hydrated electrons upon irradiation (25, 55, 56). It is likely that hydrated electrons produced by irradiation of the buffer ions in solution served as the electron source for generation of the fullerol radical anion and subsequent formation of superoxide. The absence of an aromatic compound to promote hydrated electrons at pH 7 and pH 10 would explain the reduced rate of oxygen consumption observed at these higher values of pH. Also, hydrated electrons are produced in greater concentrations under UV light than visible light (34, 57). Therefore, if the proposed reaction scheme holds, it is reasonable to assume that the proportion of ROS attributed to superoxide should be greater under irradiation with UV light than with visible light. In what at first appears to be a contradiction to this expectation, the greater quenching efficiency of SOD under visible light would seem to indicate that superoxide is the dominant species under visible light irradiation. However, this discrepancy is resolved when oxygen consumption, used as a measure of ROS generation, is normalized by the irradiance of the light source (Table 3). Oxygen consumption under UV light was an order of magnitude higher than that observed under visible light when normalized by irradiance. Thus, consistent with expectations based on hydrated electron production, the quantity of ROS quenched by SOD is calculated to be an order of magnitude greater for UV light after normalization. If fullerol-sensitized superoxide production is rapid, the rate of superoxide production may have exceeded the rate of quenching, and the quantity of enzyme present may have been limiting in the UV light experiments.
FIGURE 3. Comparison of oxygen consumption by furfuryl alcohol for various photosensitizers under irradiation with (a) UV light and (b) visible light. Oxygen consumption under visible light, sensitized by humic acid, was too low to measure. Production of Reactive Oxygen Species Compared to Other Photosensitizers. A relative quantum yield can be determined for a variety of sensitizers by comparing oxygen consumption, d[O2]/dt, over a range of sensitizer concentrations, [A], and observing when the change in oxygen concentration over fixed time increments increases to a maximum plateau value under constant irradiation (39). This plateau value of ∆[Ο2] ) ∆[Ο2]max is proportional to the quantum yield. In laboratory settings, a variety of dyes are frequently used for the photosensitized generation of 1O2. Rose bengal, a modified xanthene dye, is a standard for singlet oxygen generation (29, 37, 42, 58, 59). Other compounds used by laboratory researchers for 1O2 generation include methylene blue, eosin Y, and riboflavin (18, 29, 58). Naturally occurring organic matter such as humic and fulvic acids may also serve as photosensitizers (34, 35, 60). A comparison of oxygen consumption at pH 5 versus irradiation time is for several photosensitizers is shown in Figure 3 under conditions of both UV (panel a) and visible light (panel b) irradiation. An average molecular weight of 1.65 × 10-4 g/mol was assumed in calculating the approximate molar concentration of the humic acid used in these experiments (61). The relative quantum yield determined for each sensitizer is shown in Table 4. Rose bengal was assigned a relative quantum yield
TABLE 4. Relative Quantum Yield of Photosensitizers relative quantum yield sensitizer (1 µM)
UV light
visible light
rose bengal fullerol methylene blue aldrich humic acid buffered water
1.00 1.86 0.26 0.16 0.16
1.00 0.11 0.11 0.01
of 1.00, and all other sensitizers were normalized by the rose bengal results. Irradiation of fullerol by UV light resulted in oxygen consumption and a relative quantum yield greater than any of the other compounds evaluated in UV light. Furthermore, only rose bengal under visible light yielded greater oxygen consumption than fullerol exposed to either light source. We attribute the high relative quantum yield of fullerol to the concurrent production of single oxygen and superoxide. The presence of the phthalate anions likely increased the availability of hydrated electrons, which promoted superoxide production. The humic acid sensitized production of ROS was lowest of all the evaluated sensitizers due to the low VOL. 39, NO. 5, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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optical density of humic acid at 1 µM. No humic acid sensitized oxygen consumption was observed over the length of the experiment under visible light. In summary, fullerol produces a mixture of reactive oxygen species under both visible and ultraviolet irradiation. Evidence of both singlet oxygen and superoxide production was obtained through quenching experiments with sodium azide and superoxide dismutase. Although the photophysical capability of fullerol has been shown by other researchers to be reduced by the hydroxylation of the C60 when compared to pristine C60 fullerene, sufficient activity remains to have a measurable effect on aqueous systems. Indeed, when compared to other known sensitizers of reactive oxygen, including rose bengal, methylene blue, and humic acid, fullerol produced reactive oxygen species at a rate at least two times that of other sensitizers under UV light. This result, coupled with the observation that fullerol exhibited low toxicity to human cell cultures (17), suggests that fullerol toxicity will increase in the presence of light. The rate of reactive oxygen species generation sensitized by fullerol under UV light was an order of magnitude greater than that obtained under visible light when normalized by irradiance of the light source. These results indicate that fullerol in the environment may accelerate natural photodynamic processes. Moreover, there is the potential for harnessing the photosensitizing properties of fullerol for use in engineered systems. Singlet oxygen induced DNA cleavage might be used for oxidative destruction of bacteria (62, 63), while photosensitized production of ROS may lead to the indirect photolysis of organic contaminants (37, 64, 65). Superoxide, as well as hydrogen peroxide and hydroxyl radicals, are potent oxidizers in environmental systems. The formation of these ROS at relatively low concentrations of fullerol suggest the possibility of engineering fullerolsensitized systems for advanced oxidation processes to destroy organic compounds or possibly disinfection.
Acknowledgments The authors gratefully acknowledge the Crew and Thermal Systems Division at NASA Johnson Space Center for the use of the spectroradiometer. In addition, K.D.P. was supported by a NASA Johnson Space Center Graduate Fellowship. The insight from two anonymous reviewers is also appreciated.
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Received for review July 9, 2004. Revised manuscript received November 3, 2004. Accepted November 8, 2004. ES048940X
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