Photochemical and Photophysical Properties of Sequentially

Nov 14, 2012 - (1C60*) and triplet (3C60*) excited states, affect the intersystem crossing (ISC) process ..... allowed for an important route of 1O2 s...
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Photochemical and Photophysical Properties of Sequentially Functionalized Fullerenes in the Aqueous Phase Samuel D. Snow,† Jaesang Lee,‡ and Jae-Hong Kim*,† †

Civil and Environmental Engineering, Georgia Institute of Technology, Atlanta, Georgia 30332, United States Center for Water Resource Cycle, Korea Institute of Science and Technology, Seoul 136-791, Korea

‡

S Supporting Information *

ABSTRACT: The vast range of C60 derivatives makes it difficult to assess the potential environmental impact of this class of materials, while past environmental studies mostly focused only on pristine C60. Central to derivatized C60’s potential to negatively impact (micro)biological receptors upon unintended release is its unique property of mediating the transfer of light energy to ambient oxygen, producing 1O2. To initiate the process of establishing a thorough understanding of the photoinduced adverse biological effects of functionalized fullerenes and their aqueous dispersions, the photochemical properties relevant to 1O2 production were evaluated using three selected series of mono-, bis-, and tris-adducted fullerene materials. Differential 1O2 production of derivatives in toluene were explained by spectral variations under visible and UVA light conditions. Of the nine functionalities studied only aggregates of two positively charged derivatives showed significant photoactivity under experimental conditions. Laser flash photolysis revealed a triplet excited state in the photoactive aggregates with a sufficiently long lifetime to be quenched by 3O2. Dynamic light scattering, transmission electron microscopy, and electron diffraction patterns revealed aggregates with sizes typical of aqueous C60 colloids that varied in crystallinity based on functionality. Results raised questions about our current understanding of the photoactivity of fullerene aggregates.

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INTRODUCTION

Many studies have examined the biological and environmental implications of C60 aggregates through various preparation methods.11,13,15−21 There has been some debate about the legitimacy of toxicology data from studies using THF as an intermediate solvent in aggregate preparation,20 but most studies have found C60 suspensions to be relatively benign, despite the propensity of C 60 to be an effective 1 O 2 sensitizer.22−25 The same cannot be said, however, for aggregates of fullerene derivatives. Despite the dearth of studies on aggregates of functionalized fullerene, a few have shown that the new materials can be photoactive and biocidal.15−17,19,21 Fullerene derivatives are now rapidly entering the industrial sector: in November of 2010, the U.S. EPA granted approval to commercially produce fullerenes and PCBM (Phenyl-C61Butyric acid Methyl ester).26 Now that a depth of knowledge has been built for pristine C60 and the properties of its aggregates, it is imperative to scrutinize fullerene derivatives that will be used in many emerging applications and will inevitably be released into the environment.

With great potential for many photophysical and photochemical applications, carbon fullerenes - C60 being the most abundant - have drawn much attention across many fields since their discovery and the ensuing rapid advances in mass production.1−7 The hydrophobic nature of the all-carbon molecule lends itself to further applications in surface coating and lubricant technologies8 yet poses a challenge for biological and aqueous phase applications,4,9 as C60 molecules form clustered aggregates in water.10,11 It is well established that these aggregates lose much of their photoactivity and capacity to photosensitize singlet oxygen (1O2), the property of interest for many applications and of concern for environmental implications.11,12 Decreased surface area for O2 interaction and internal excitation quenching processes caused by C60-C60 interactions (e.g., triplet−triplet annihilation) in crystalline aggregates have been conjectured as the explanation of the loss of photoactivity in aggregates.12−14 It has been shown, however, that water-soluble, functionalized fullerenes can form smaller, noncrystalline aggregates that can produce significant amounts of reactive oxygen species in the aqueous phase,15−20 although it is not clear what the minimum extent or what chemistry of functionalization is necessary for C60 to form photoactive suspensions in water. © XXXX American Chemical Society

Received: August 9, 2012 Revised: November 12, 2012 Accepted: November 14, 2012

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Functionalization is known to affect C60’s photochemistry in several ways: additions of functional groups can alter the singlet (1C60*) and triplet (3C60*) excited states, affect the intersystem crossing (ISC) process, and impact the lifetime of 3C60*.27−29 Yet the mechanisms of how derivatization affects the formation of aggregates and their resulting photochemistries remain largely unknown. Additionally, changes to C60’s photochemistry as a molecule, observed in the organic phase, may not directly translate to changes in the photochemistry of aggregates of derivatized C60. For instance, C60-C60 interactions in C60 aggregates result in the disappearance, shifting, and broadening of many UV/vis absorption features characteristic of monodispersed C60.30 It is not known how these changes in photochemistry affect the photoactivity of aqueous aggregates. Further study is expedient and necessary to understand and predict the possible environmental consequences of derivatized fullerenes entering the environment and forming aqueous stable colloidal clusters. This study intends to examine key derivatives that will provide insights on the relationships between photophysical and photochemical properties of fullerene derivatives and their chemical structures. Three series of functionalized fullerenes, each with mono-, bis-, and tris-functionality, were selected such that specific structural features could be compared (i.e., the presence or absence of quaternary ammonium groups) and for their prevalence in current research and applications.

Laser Desorption-Ionization coupled with Mass Spectrometry (MALDI-MS) as seen in Figure S1 of the Supporting Information (SI). Clear peaks at expected molecular weights confirmed the parent molecules. Additionally, UV/vis characterization matched well with known spectra in the literature.19,29,31,32 Aqueous Phase Dispersion. Aqueous aggregates of the fullerene materials were prepared via sonication. Briefly, 9 mg of C60 or derivatives was added to 10 mL of toluene and sonicated in a bath sonicator (Fisher Scientific FS30) for 6 h in a sealed jar at ca. 60 °C. Ultrapure water (90 mL) was then added, and the mixture was sonicated for 24 h. B derivatives were added directly to water, due to their insolubility in toluene. Finally, the mixtures were unsealed and sonicated for an additional 24 h, allowing the toluene to evaporate. Aggregate solutions were then filtered with 0.45 μm Whatman nitrocellulose filters. Filtered solutions were then concentrated using a rotary evaporator (Rotavapor R-200, Buchi corp.) and stored in the dark. Final aggregate concentrations were measured using a Total Organic Carbon (TOC) analyzer (TOC-V ws, Shimadzu corp.) and ranged from 10 to 230 μM. Aggregate Characterization. Aqueous fullerene aggregates were measured for size and zeta potential using Dynamic Light Scattering (DLS) and Phase Analysis Light Scattering (PALS) techniques, respectively. Aggregate suspensions were measured in triplicate using a Zetasizer Nano ZS90 (Malvern Instruments, Worcestershire, OK) with a low end detection limit of ca. 5 nm. The fullerene aggregates were assigned a refractive index of 2.2.2 Transmission Electron Microscope (TEM) imaging coupled with Energy-Dispersive Spectroscopy (EDS) and electron diffraction patterns were used to confirm aggregate size, composition, and crystallinity. A Philips 120 TEM was used at the MVA Scientific Consultants Inc. TEM grids were prepared on carbon-coated copper grids with square mesh. Photochemical Experiments. Photochemical activities of the fullerene materials were measured in both organic and aqueous (as aggregates) phases. Experiments were performed using a 50 mL cylindrical quartz reactor with a magnetic stirrer. Two experimental light conditions were used: Black Light Blue (BLB) lamps with wavelengths from 350 to 400 nm and Fluorescent Lamps (FL) with a UV cutoff filter for wavelengths >400 nm. Irradiation intensities for BLB and FL conditions were probed with a potassium ferrioxalate actinometric method33 and found to be 4.70 × 10−6 Einstein·L−1s−1 (Φ = 1.26) and 4.31 × 10 −7 Einstein·L −1 s −1 (Φ = 1.11), respectively.34 For aqueous phase experiments, the reaction solution contained 40 mL total of 5 μM of fullerene aggregates, 10 mM phosphate buffer at pH 7.1, and 0.85 mM furfuyl alcohol (FFA) as a 1O2 probe with a reaction rate of k (FFA + 1 O2) 1.2 × 108 M−1s−1.35 Organic phase reactions consisted of 5 μM of fullerenes (fully dispersed) in toluene for C60, A and C with 0.85 mM FFA. Due to B’s insolubility in toluene and differential 1O2 lifetimes in solvents, FFA experiments were not performed for B in the organic phase. A positive control for 1O2 production was conducted with the well-known 1O2 sensitizer, Rose Bengal (Figure S2). Negative controls were conducted under dark conditions and with L-histidine, a well-known 1O2 quencher. Laser Flash Photolysis. Nanosecond transient absorption spectra of triplet states of C60 derivatives were measured using laser flash photolysis (LFP). The LFP experiments were carried out under air-equilibrated conditions. The third harmonic

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EXPERIMENTAL SECTION Materials. Deionized/distilled water (resistivity >18.2 MΩ) from a Millipore ultrapure system (Millipore Co.) was used in preparation of all solutions and reagents. All chemicals used were analytical, reagent-grade, and used as received. All fullerene materials were used as received, with no further purification. Fullerene derivatives seen in Figure 1 are

Figure 1. Fullerene derivatives, A) methylpyrrolidine, n = 1, 2, or 3; B) quaternary pyrrolidine, n = 1, 2, or 3; and C) phenyl-C6(n)-butyric acid methyl ester, n = 1, 2, or 3 .

abbreviated using the following nomenclature scheme: derivatives A1, A2, and A3 are mono-, bis-, and trisfullereropyrrolidines, respectively;31 under the same convention, B refers to the fulleropyrrolidinium ions19 and C refers to phenyl-C61-butyric acid methyl ester (PCBM).3 Sublimed C60 (99.9%) was obtained from MER Corp., Tuscon, AZ. C1 (99%) was obtained from SES Research, Houston, TX. C2 (99.5%) and C3 (>95%) were obtained from Aldrich, St. Louis, MO. A and B (>95%) were obtained from The Chemistry Research Solution LCC, Bristol PA. The purity of A, B, and C3 were guaranteed to be above 95% by the providers, with impurities consisting of the same derivative with more or less addends (e.g., B2 contains trace amounts of B1 and B3). Identity of the derivatives was confirmed using Matrix Assisted B

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Figure 2. Visible absorption spectra for C60, A and C derivatives in toluene.

Figure 3. FFA degradation by C60, A and C in toluene under (a) fluorescent lamps with cutoff filter (400−650 nm) and (b) black light blue lamps (350−400 nm).

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RESULTS AND DISCUSSION UV/vis Absorption in Organic Solvent. The visible absorption spectra for C60, A and C in toluene are plotted in Figure 2 to compare relative absorption across the visible regions. The full absorption spectra of A and C from UV to near IR can be found in Figure S3. Consistent with previous reports, monofunctionalized A1 and C1 exhibited red-shifted peaks resembling C60’s characteristic 410 nm peak.3,31 The broad absorption band of C60 centered around 540 nm, which has been shown to correspond to forbidden singlet−singlet transitions,36 was blue-shifted and enhanced with each addition to the cage. This transition has been reported to be enhanced by interaction of 3O2, implicating 1O2 sensitization.10,36 Accordingly, it would be expected that these derivatives could have faster 1O2 sensitization rates than C60 in the natural environment where broad-spectrum visible light dominates. Absorption in the visible range was enhanced with increasing functionalization due to extended conjugation of the pi electron system,37 such that A3 > A2 > A1 > C60 and C3 > C2 > C1 > C60. Visible absorption of A was enhanced over C, such that A1 > C1, A2 > C2, and A3 > C3. The difference between A and C, given the same number of addends, is somewhat unexpected given that the structure of the C addend contains more piconjugation (i.e., the phenyl ring on C’s addend) than A. This difference, however, may be explained by the diminishing effects of adding to a highly conjugated chromophore and the

generation (THG, 355 nm) of a Q-switched Nd:YAG laser (Continuum, Surelite II, pulse width of 4.5 ns, full width at halfmaximum, fwhm) was applied as the excitation light. A Xenon lamp (ILC Technology, PS 300-1) was focused on the experimental suspensions as the probe light to monitor the transient formation and subsequent decay. The temporal profiles were recorded using a monochromator (Dong-Woo Optron, Monora 500i) equipped with a photomultiplier (Zolix Instruments Co., CR 131) and a digital oscilloscope (Tektronix, TDS-784D). The transient absorption spectra were measured by an intensified charged-coupled device (CCD) with a gate time of 1.6 ns and a 10 ns time delay (Ando Technology, iStar). The subpicosecond transient absorption spectra of triplet states of functionalized C60 were obtained with a pump−probe transient absorption spectroscopy system (Ultrafast Systems, Helios). The pump light was generated using a regenerative Ti:sapphire laser amplifier system (Coherent, Libra-F, 1 kHz) with a diode-pumped Q-switched laser (Coherent, Evolution). The seed pulse was generated by a Ti:sapphire laser (Coherent, Vitesse). The pulse (355 nm) produced from an optical parametric amplifier (Coherent, TOPAS) was used as the excitation pulse. The pump pulse passes through a mechanical chopper synchronized to one-half of the laser repetition rate, resulting in a pair of the spectra with and without the pump, from which absorption change induced by the pump pulse was projected. C

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Figure 4. UV/vis spectra for A, B, and C as aqueous aggregates at 5 μM.

aggregates.10 Interestingly, aggregates of B had significantly lower absorption in the UVA-visible range, despite being structurally very similar to A. FFA degradation experiments were performed using all aqueous aggregate samples with UVA radiation, yet only B2 and B3 exhibited significant 1O2 production over the course of the photoillumination, as seen in Figure 5 (data not shown for

strain induced by the three-membered ring between the addend of C and the C60 cage compared with the five-membered ring in A.37,38 1 O2 Production in the Organic Phase. Probing 1O2 production, Figure 3 shows the FFA degradation curves for A and C in toluene under FL (a) and BLB (b) irradiation. Under visible light illumination, the derivatives showed enhanced 1O2 production over pure C60, which was consistent with the visible light absorption trends mentioned above, C3 > C2 > C1 > C60. The trend is reversed under UVA irradiation, where there is less difference in absorption between derivatives. This reversal in kinetics between light conditions provides some evidence for less efficient ISC with higher triplet excited state and lower singlet excited state energy levels. A closely matched C in these FFA degradation patterns with the exception of not having distinguishable differences in kinetics under visible irradiation, which can be attributed to more overlaps in their visible spectra (e.g., A2 ≥ A3 at 405 and 490 nm). Contrary to what is expected based on their visible absorption spectra, C exhibited enhanced 1O2 production over A with visible light. This apparent contradiction implicates other factors, possibly more important than ground state absorption, that affect 1O2 production (i.e., the type of bond a functional group forms with the C60 cage may affect the 3C60* lifetime). The apparent difference in reaction orders in the visible light cases can likely be attributed to the concentration of FFA used compared to the rate of 1O2 production, such that rapid production yields a second-order rate dependent on both [FFA] and [1O2] and slower production allows for a pseudo-first-order case when a steady state 1O2 concentration can be established.35 Aqueous Aggregate Photoactivity. Aqueous aggregates were formed at the nanoscale for all derivatives and were stable (unchanging in size) as prepared over several months, with the exception of B1 which continued to agglomerate into larger particles after preparation. UV/vis spectra taken at 5 μM are plotted in Figure 4. It is known that the UV/vis spectra of fullerenes change significantly upon aggregation, resulting in broadened and shifted peaks, depending on preparation methods and size of the aggregates.30 C60, along with the A and C series, exhibited enhanced absorption in the visible range, and notably, C60’s broad absorption peak centered about 500 nm is no longer lower than the corresponding peaks of the derivatives. The characteristic vibronic signal for C60 at 410 and 430 nm for A1 and C1 in toluene (Figure 2) disappears for the aggregates, due to fullerene-fullerene interactions within the

Figure 5. FFA degradation by the B series in the aqueous phase under BLB irradiation.

A and C, showing no degradation). Initial (30 min) rate constants for 1O2 production for B2 and B3, represented by their FFA degradation rates, were found to be 17.11 (R2 = 0.9921) and 17.40 (R2 = 0.9988) μM/min, respectively, which correspond to steady-state 1O2 concentration of 1.1 × 10−8 M for both. Control experiments under dark conditions and with specific radical quenchers confirmed that FFA degradation was ascribed to the photochemical production of 1O2. FFA degradation kinetics of B2 and B3 were not significantly different, as might be expected from their nearly identical UVA absorption spectra. The UV/vis absorption spectra, however, do not fully explain the dearth of 1O2 production in aggregates of other derivatives; in fact, the B series aggregates have lower absorption than A, C and C60 at wavelengths above 350 nm. The presence of a broad absorption band from 400 to 600 nm in C60 and the A and C derivatives likely indicates C60-C60 interactions.30 The lack of this band in the B series suggests a difference in aggregation state, possibly with less molecule− molecule interactions within the aggregate. It is known that C60 aggregates are not effective for photosensitized 1O2 production (compared to its molecularly dissolved counterpart), likely due D

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Figure 6. Absorption differences displaying triplet excited state populations probed with LFP for (a) B2 at 650 nm (with the singlet population probed at 510 nm) and (b) A1 at 700 nm.

Figure 7. Nanosecond laser spectroscopy for B2: (a) triplet state absorbance 500 ns after laser excitation and (b) triplet state absorption difference at 650 nm in the presence of O2.

the extent of other derivatives with the same number of addends. Previous studies showed that aggregated C60 has a triplet state that decays within picoseconds, compared with lifetimes of 50 to 150 μs when molecularly dispersed with surfactants or in benzene.14,39 Aggregate Characterization. In an effort to explain the anomalous production of 1O2 by B2 and B3, aggregates of each derivative were characterized and compared. DLS analysis, as reported in Table 1 and Figure S5, found the aggregates to be highly polydisperse and to vary in size and ζ-potential. Less stable aggregates (with low absolute ζ-potential values under ca. 30 mV) increased in size with decreasing ζ-potential, as expected from colloidal physics. ζ-potentials of the aggregates had an expected correlation to the number of addends for the B series. With increasing addends for B, the zeta potential becomes more positive, starting at a negative value for B1 (−16.9 mV). The negative ζ-potential of B1, indicates that one cationic charge does not stabilize C60 in water enough to counteract the hydroxylation, epoxidation, and subsequent hydration that are suggested to be responsible for the negative surface charge.40−43 It is important to note that the size of aggregates did not matter for 1O2 production in our study, as B2 and B3 degraded FFA at very similar rates, despite the significant difference in size. Additionally the A and C derivatives were not photoactive in the experimental time

to surface area limitations and self-quenching mechanisms, and it has been suggested that more soluble derivatives that either do not aggregate significantly or do not form crystalline aggregates are more capable of sensitizing 1O2 in the aqueous phase.12,14 The presence of photoactivity in B2 and B3 aggregates and the lack thereof in other derivatives was confirmed using LFP experiments. Figure 6 compares the population of the triplet excited states of B2 and A1, as examples of photoactive and nonphotoactive derivatives, respectively. After the initial excitation pulse, a clear triplet state can be seen being populated at 650 nm for B2, with a corresponding decay of the singlet excited state observed at 510 nm. In contrast, A1’s triplet state (probed at 700 nm due to a shifted triplet energy state) was rapidly quenched with a lifetime on the order of picoseconds. The singlet state of A1, probed at 550 nm, formed and decayed on the same time scale as the triplet state (Figure S4). Probing B2’s triplet state 500 ns after the excitation pulse, Figure 7(a) revealed that its lifetime in an oxygen purged environment was long-lived compared to triplet A1. When monitored in the presence of O2, however, B2’s triplet state was quenched within nanoseconds (Figure 7(b)). These results suggest that the lack of photoactivity in most of the derivatives can be attributed to a rapidly quenched triplet state and that B2 and B3 aggregates do not undergo self-quenching pathways to E

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Table 1. Aggregate Zeta Potentials and Sizesa sample

ζ-potential (mV)

d (nm)

w (nm)

PDI

C60 A1 A2 A3 B1 B2 B3 C1 C2 C3

−46.0 −43.0 −47.5 −48.3 −16.9 +13.1 +27.4 −52.3 −42.3 −34.9

122.5 117.0 127.7 114.1 260.5 711.1 145.9 112.3 107.7 99.7

47.01 62.90 32.48 35.09 34.65 49.57 36.66 29.19 31.42 26.35

0.155 0.192 0.229 0.133 0.325 0.513 0.213 0.173 0.189 0.238

fully explain the dearth of photoactivity in aggregates (diffraction patterns not shown). These data on the photoactivity and physical characteristics of the aggregates of fullerene derivatives put many prior assumptions about the relationships between aggregation and 1O2 production in question. Environmental Perspectives. The results of thorough characterizations of carefully chosen fullerene derivatives herein highlight several key gaps in the understanding of how aggregation affects fullerene photochemistry, particularly for functionalized fullerenes. There have been two common explanations for the lack of photoactivity of fullerene aggregates: reduced surface area44 of the particles and their crystalline nature promoting triplet−triplet annihilation,17,39,45 effectively reducing their photoactivity. In this study, however, neither theory has fully explained the observations made for the derivatives studied: large aggregates effectively produced 1O2, while smaller particles that were not crystalline produced no observable 1O2. The only observable difference between the photoactive and nonphotoactive derivatives was that B2 and B3, which both produced 1O2, had positively charged surfaces, unlike all other derivatives with negative zeta potentials. Although molecule−molecule interactions are still likely to be important, surface phenomena may also be critical to the photochemistry of aggregates. In particular, surface oxidation and consequent hydration structures may interfere with the sensitization process of negatively charged fullerene aggregates that may otherwise be effective sensitizers (e.g., the C series which were not crystalline).40−43 It is known that redox characteristics affect 1O2 production efficiency for sensitizers46 and that significant solvent-complex reorganization must be allowed for an important route of 1O2 sensitization.47 These characteristics have perhaps been overlooked by researchers wishing to establish a mechanistic understanding of fullerene aggregate photochemistry. While further investigation is critical,

a All values are calculated from three or more repetitions. ζ is the zeta potential, d is the Z-average diameter, w is the peak width, and PDI is the polydispersity index.

frame, despite being similar or smaller in size than any of B. These findings contrast the often hypothesized surface-area limitation explanation for fullerene aggregates not producing significant amounts of 1O2. TEM imaging confirmed the DLS size measurements, finding aggregates to be variable in size and shape, matching expected dimensions from DLS. Further, electron diffraction patterns were used to probe the crystallinity of the aggregates. Representative TEM images with corresponding diffraction patterns are shown in Figure 8. Based on past hypotheses on the photoactivity of fullerene aggregates, it is expected that photoactivity of aggregates is mitigated by their crystalline nature, due to self-quenching mechanisms (e.g., triplet−triplet annihilation).11−14,17 In line with the crystallinity hypotheses, C60, B1 and the A series were all found to have crystalline diffraction patterns, and B2 and B3, which were definitively photoactive, were not crystalline. None of the C derivatives, however, were crystalline, suggesting that crystallinity does not

Figure 8. TEM and associated electron diffraction images for C60, A3, B3, and C3. Well-defined diffraction rings around the electron beam in C60 and A3 indicate an ordered, crystalline structure. F

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(5) Mroz, P.; Pawlak, A.; Satti, M.; Lee, H.; Wharton, T.; Gali, H.; Sarna, T.; Hamblin, M. R. Functionalized fullerenes mediate photodynamic killing of cancer cells: type I versus type II photochemical mechanism. Free Radical Biol. Med. 2007, 43 (5), 711−9. (6) Isaacson, C. W.; Kleber, M.; Field, J. A. Quantitative analysis of fullerene nanomaterials in environmental systems: a critical review. Environ. Sci. Technol. 2009, 43 (17), 6463−74. (7) Xiao, L.; Takada, H.; Maeda, K.; Haramoto, M.; Miwa, N. Antioxidant effects of water-soluble fullerene derivatives against ultraviolet ray or peroxylipid through their action of scavenging the reactive oxygen species in human skin keratinocytes. Biomed. Pharmacother. 2005, 59 (7), 351−8. (8) Tsukruk, V. V.; Everson, M. P.; Lander, L. M.; Brittain, W. J. Nanotribological properties of composite molecular films: C60 anchored to a self-assembled. Langmuir 1996, 12 (16), 3905−3911. (9) Nakamura, E.; Isobe, H. Functionalized fullerenes in water. The first 10 years of their chemistry, biology, and nanoscience. Acc. Chem. Res. 2003, 36 (11), 807−15. (10) Bensasson, R. V.; Bienvenue, E.; Dellinger, M.; Leach, S.; Seta, P. C60 in model biological-systems - a visible-UV absorption study of solvent-dependent parameters and solute aggregation. J. Phys. Chem. 1994, 98 (13), 3492−3500. (11) Fortner, J. D.; Lyon, D. Y.; Sayes, C. M.; Boyd, A. M.; Falkner, J. C.; Hotze, E. M.; Alemany, L. B.; Tao, Y. J.; Guo, W.; Ausman, K. D.; Colvin, V. L.; Hughes, J. B. C60 in water: nanocrystal formation and microbial response. Environ. Sci. Technol. 2005, 39 (11), 4307−4316. (12) Lee, J.; Fortner, J. D.; Hughes, J. B.; Kim, J. H. Photochemical production of reactive oxygen species by C60 in the aqueous phase during UV irradiation. Environ. Sci. Technol. 2007, 41 (7), 2529−2535. (13) Hotze, E. M.; Badireddy, A. R.; Chellam, S.; Wiesner, M. R. Mechanisms of bacteriophage inactivation via singlet oxygen generation in UV illuminated fullerol suspensions. Environ. Sci. Technol. 2009, 43 (17), 6639−45. (14) Lee, J.; Yamakoshi, Y.; Hughes, J. B.; Kim, J. H. Mechanism of C60 photoreactivity in water: fate of triplet state and radical anion and production of reactive oxygen species. Environ. Sci. Technol. 2008, 42 (9), 3459−3464. (15) Cho, M.; Snow, S. D.; Hughes, J. B.; Kim, J. H. Escherichia coli inactivation by UVC-irradiated C60: kinetics and mechanisms. Environ. Sci. Technol. 2011, 45 (22), 9627−33. (16) Huang, L.; Terakawa, M.; Zhiyentayev, T.; Huang, Y. Y.; Sawayama, Y.; Jahnke, A.; Tegos, G. P.; Wharton, T.; Hamblin, M. R. Innovative cationic fullerenes as broad-spectrum light-activated antimicrobials. Nanomedicine: nanotechnology, biology, and medicine 2010, 6 (3), 442−52. (17) Lee, J.; Mackeyev, Y.; Cho, M.; Li, D.; Kim, J. H.; Wilson, L. J.; Alvarez, P. J. J. Photochemical and antimicrobial properties of novel C60 derivatives in aqueous systems. Environ. Sci. Technol. 2009, 43 (17), 6604−6610. (18) Lee, J.; Cho, M.; Fortner, J. D.; Hughes, J. B.; Kim, J. H. Transformation of aggregate C60 in the aqueous phase by UV irradiation. Environ. Sci. Technol. 2009, 43 (13), 4878−4883. (19) Tegos, G. P.; Demidova, T. N.; Arcila-Lopez, D.; Lee, H.; Wharton, T.; Gali, H.; Hamblin, M. R. Cationic fullerenes are effective and selective antimicrobial photosensitizers. Chem. Biol. 2005, 12 (10), 1127−35. (20) Sayes, C. M.; Fortner, J. D.; Guo, W.; Lyon, D.; Boyd, A. M.; Ausman, K. D.; Tao, Y. J.; Sitharaman, B.; Wilson, L. J.; Hughes, J. B.; West, J. L.; Colvin, V. L. The differential cytotoxicity of water-soluble fullerenes. Nano Lett. 2004, 4 (10), 1881−1887. (21) Cho, M.; Fortner, J. D.; Hughes, J. B.; Kim, J. H. Escherichia coli inactivation by water-soluble, ozonated C60 derivative: kinetics and mechanisms. Environ. Sci. Technol. 2009, 43 (19), 7410−7415. (22) Kovochich, M.; Espinasse, B.; Auffan, M.; Hotze, E. M.; Wessel, L.; Xia, T.; Nel, A. E.; Wiesner, M. R. Comparative toxicity of C60 aggregates toward mammalian cells: role of tetrahydrofuran (THF) decomposition. Environ. Sci. Technol. 2009, 43 (16), 6378−6384.

the molecules studied serve as a representative model for several classes of fullerenes that may find commercial applications and be released into the environment. For the cases of slightly functionalized fullerenes (as in our study), environmental concerns based on the photosensitization capacity of fullerene aggregates appear to be dependent on the properties of the type of functional group attached, more than the number of addends. Finally, as many applications are on the horizon for functionalized derivatives, this work provides some insight on the photophysical effects of functionalizing fullerenes with mono-, bis-, and tris-functionality. Functionalization with up to three groups can be used to tune the photochemical properties for various applications. Indeed, the 1O2 sensitization rates of B2 (17.11 μM/min) and B3 (17.40 μM/min) represent much more efficient 1O2 production than previously reported aminofullerenes that exhibited similar rates (from 8.18 to 19.06 μM/min) at ten times the concentration (50 μM was used for the aminofullerenes while 5 μM was used here).17 According to calculations of CT for 1O2 exposure to MS2 bacteriophage viruses, B2 and B3 are expected to exhibit extremely fast viral inactivation compared with aminofullerenes, representing both an interesting possibility for disinfection applications and a potential phototoxicological concern.48

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ASSOCIATED CONTENT

S Supporting Information *

Additional figures showing MALDI-MS analysis, extended UV/ vis spectra in toluene, organic phase FFA control data, aqueous FFA degradation experiments for A and C derivatives and aggregate size distributions. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Phone: (404) 894-2216. Fax: (404) 385-7087. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the National Science Foundation (Grant #: CBET-0932872) and by the Green City Technology Flagship Program funded by the Korea Institute of Science and Technology (KIST-2012-2E23333). The authors extend much gratitude to Dr. Jim Millette at the MVA Scientific Consultants, Inc. and KyoungEun Park at the Georgia Institute of Technology for their assistance with TEM imaging. The authors would also like to thank Dr. Daewon Cho for his assistance during laser flash photolysis, which was performed at Next Generation Solar Cell Research Center, Konkuk University.

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REFERENCES

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