Photoredox Reactions and the Catalytic Cycle for Carbon DioxideFixation and Methanogenesis on Metal OxidesIlya A. Shkrob,*,† Timothy W. Marin,†,‡ Haiying He,§ and Peter Zapol†,§

†Chemical Sciences and Engineering Division, Argonne National Laboratory, 9700 South Cass Avenue, Argonne, Illinois 60439,United States‡Chemistry Department, Benedictine University, 5700 College Road, Lisle, Illinois 60532, United States§Materials Science Division, Argonne National Laboratory, 9700 South Cass Avenue, Argonne, Illinois 60439, United States

*S Supporting Information

ABSTRACT: Photoirradiated metal oxide semiconductors are known toreduce carbon dioxide to methane. This multistep reaction is commonlyrepresented as a sequence of proton-coupled two-electron reactions lead-ing from carbon dioxide to formate to formaldehyde to methanol and tomethane. We suggest that the actual reaction mechanism is more complex,as it involves two-carbon molecules and radicals in addition to these one-carbon species. The ″stepping stone″ of this mechanism for carbon dioxidefixation could be glyoxal, which is the product of recombination of twoformyl radicals, or glycolaldehyde, which is its reduced form. We demon-strate the main steps of this reduction chain and suggest a catalytic cycleintegrating these steps and the radical chemistry. In addition to methane,this cycle generates complex organic molecules, such as glycolaldehyde,acetaldehyde, and methylformate, which were observed in product analyses. This cycle can be regarded as one of the simplestrealizations of multistep, photosynthetic fixation of atmospheric carbon in prebiotic nature.

1. INTRODUCTIONThe present study continues the theme addressed in some otherrecent publications from our laboratory,1−5 viz., the mechanismfor catalytic reduction of CO2 on photo- and electroactivesemiconducting metal oxides.6−11 Methane, which attracts themost attention due to its use as a fuel, is one of the products ofthis multistep reduction: other known volatile products includeone-carbon (formate, formaldehyde, and methanol), two-carbon(methylformate and acetaldehyde), and three-carbon (acetone)molecules.6,11,12 In the following, hydrated TiO2 (anatase) servesas the model for all such oxide materials, as this material isparticularly amenable to spectroscopic study.In refs 1−3, we argued that the first steps of this reduction

involve (i) one-electron reduction of chemisorbed CO2 toCO2

−•, which is doubly bound to Ti4+−O−Ti4+ centers at thesurface through the two oxygens, (ii) a proton-coupled electrontransfer to this Ti4+−OCO−•−Ti4+ center resulting in theformation of the doubly bound formate anion, Ti4+−OC(H)-O−−Ti4+, and (iii) one-electron reduction of formic acid via Oatom transfer to the resulting Ti3+ center resulting in theformation of the formyl radical, HC•O (here the bullet standsfor the unpaired electron). Using eCB

−• as the general notationfor the conduction band (CB) or tail-band electron that istrapped by surface Ti4+ ions involved in the Ti−O bonds withthe adsorbate (or the electron-accepting adsorbate itself), thesereactions can be, respectively, written as

+ →−• −•e CO COCB 2 2 (1)

+ + →−• + −• −e H CO HCOCB 2 2 (2)

+ + → +−• + + − •e Ti HCO H Ti O H HC OCB4

24

(3)

The focus of the present study is to suggest how the 8-electronreduction of CO2 proceeds past reaction 3. As discussed else-where,2,5 it is not presently clear whether this reduction occursas a sequence of one-electron reactions similar to reactions 1 to3 or if it involves two-electron reactions that require concertedtransfer of two electrons to a reactant on the TiO2 surface. Thesimplest reaction scheme is a sequence of four consecutive two-electron proton-coupled reactions3,6

⎯ →⎯⎯⎯⎯⎯ ⎯ →⎯⎯⎯⎯⎯⎯ ⎯ →⎯⎯⎯⎯⎯

⎯ →⎯⎯⎯⎯⎯⎯

+

+

+−

+

+

+

+−

+

+

−

+

−

+

−

+

−

CO HCO H H CO CH OH

CH

22H

2e2

2HH O

2e2

2H

2e3

2HH O

2e4

2

2 (4)

While this way of visualizing the reaction is lucid and useful, itaffords limited insight into the actual reaction mechanism.Furthermore, it tacitly assumes that two- and three-carbon prod-ucts play no significant role in methanogenesis, which is not

Received: January 4, 2012Revised: February 16, 2012Published: March 6, 2012

Article

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self-evident, given that such molecules are more easily reducedthan one-carbon molecules. Can the latter molecules serve asthe precursors of methane, e.g., as the progenitors of the methylradical,2 as was recently suggested in ref 5?In a companion publication,1 we used electron paramagnetic

resonance (EPR) spectroscopy to study the photoreactions ofHCO2

− and HCO2H on hydrated TiO2. The CO2−• and

OC•OH (that is, protonated CO2−•) radicals arising from one-

electron oxidation of their parent molecules by valence bandholes (hVB

+•)

+ → ++• − + −•h HCO H COVB 2 2 (5)

and the formyl radical generated in reaction 3 were observed atlow temperature. No methyl radicals were observed. Trifunacand co-workers13,14 and subsequently Shkrob et al.15 used EPRspectroscopy to study the photoreactions of methanol andmethoxide on hydrated TiO2. No methyl radicals were observedunder the normal illumination conditions. However, Trifunacand co-workers13 observed methyl radicals below 10 K whenmethoxide-dressed TiO2 was irradiated using high-fluence248 nm laser pulses (>100 mJ/pulse). These conditions wereso extreme that direct photoexcitation of methanol cannot be ex-cluded. On the other hand, methyl radicals can be readily gen-erated on TiO2 by photooxidation of acetate,15 and such radicalscan be observed below 150 K; at higher temperature, the methylradicals migrate and abstract H from the acetate, yielding carbo-xymethyl radicals. Thus, the failure of EPR spectroscopy toobserve methyl radicals in methanol and formate solutions ofaqueous TiO2 cannot be due to the unusually facile secondaryradical chemistry (depleting the methyl radicals). In Sections 2.1and 2.2, we revisit these EPR observations and demonstrate thatmethanol and formaldehyde do not yield radicals via one-electronreduction. This is not too surprising given that these moleculeshave no electron affinity and do not react even with the hydratedelectron, which is a much stronger reducing agent than theelectron on TiO2.The key assumption of reaction scheme 4 is envisioning the four

proton-coupled two-electron (or two consecutive one-electron)transfers as H adatom reactions similar to those occurring on metalcatalysts. Mechanistically, this picture is unlikely to lead to methane:in the aqueous bulk, the H atoms abstract hydrogen from formate,formaldehyde, and methanol, yielding the corresponding CO2

−•,HC•O, and •CH2OH radicalsthat is, the same radicals that areproduced by photooxidation of these molecules on TiO2. Such Hatom reactions would close the catalytic cycle and direct the re-duction toward H2 rather than CH4. This undesirable propensitymakes one-carbon molecules in reaction scheme 4 unlikely pro-genitors of methane: it is much easier to remove a hydrogen atomthan to add a hydrogen atom to these molecules. While this maynot necessarily be correct regarding what occurs on the surface(which may reduce the barriers for H atom addition as opposed toH atom abstraction), an obstacle still presents itself: one-electronreduction of one-carbon molecules in reaction scheme 4 is ener-getically prohibitive.Therefore, it seems likely that the reduction is assisted by re-

actions joining two carbon atoms that yield molecules for whichthe reaction barriers for further reduction are significantlylowered. It is well-known16 that recombination of the formylradicals generated in reaction 3 produces glyoxal (ethanedial)

→•2HC O C H O2 2 2 (6)

Due to its π-conjugation, glyoxal has significant gas-phase adi-abatic electron affinity (EA, estimated as 0.62 or 0.9 eV)17 ascompared to monoaldehydes (e.g., acetaldehyde and formaldehydehave EA of a few millielectronvolts).18 While the electron affinity ofmonoaldehydes becomes slightly positive in solution, glyoxal is stilla much more efficient electron acceptor than these mono-aldehydes. Electrochemical reduction of glyoxal to trans-ethane-1,2-semidione, C2H2O2

−•,19 is facile, and so glyoxal can serve as a″stepping stone″ to further reduction past reaction 3. In contrast,the CO2

−• anions generated in reaction 1 cannot serve as such“stepping stones”: as shown in Section 2.5 below, the recom-bination of these radicals yields products which are difficult to re-duce on TiO2. In ref 1, we found that photolysis of oxalate andoxalic acid on TiO2 yielded only oxidation products via a Kolbereaction15

+ → ++• − −•h C O CO COVB 2 42

2 2 (7)

The involvement of glyoxal would solve another puzzle: in photo-excitation of TiO2 (in the absence of a sacrificial hole-scavengingreagent removing the trapped holes from the surface),11 for everyelectron, eCB

−•, there is a valence band hole, hVB+•, that is trapped

at the surface as the Ti4+−O• oxygen hole center or a boundhydroxyl radical.20 The reactions of these holes reverse scheme 4.In methanogenesis, such reactions are, in fact, necessary, as other-wise the photogenerated holes recombine with electrons on TiO2,inhibiting further reduction of the adsorbate: the products of CO2reduction double as sacrificial hole scavengers. While such oxi-dation is clearly necessary, it is not clear how reduction can prevailover oxidation, as the latter tends to be more facile.This general consideration indicates that in the overall re-

action scheme there must be a step involving a molecule whichis more readily reduced than oxidized, and it is this step thatallows the process to proceed to completion. If the oxidationreintroduces radicals whose reactions replenish this all-important “stepping stone” molecule, the reduction can takeadvantage of this stepping stone and carry past reactions 1 to 3.We suggest that glyoxal and glycolaldehyde serve as these stepp-ing stone molecules, and in Section 3.1, we suggest a catalyticcycle based on this assumption.Before we discuss this cycle in Section 3, much groundwork

needs be laid, and this program is implemented in Section 2. InSections 2.1 and 2.2, we demonstrate that methanol andformaldehyde can only be oxidized on TiO2; no radicals fromtheir one-electron reduction are generated. Then, we turn totwo-carbon molecules and in Section 2.3 demonstrate that bothglyoxal and glycolaldehyde can be reduced on TiO2, withglycolaldehyde yielding the vinoxyl radical, the precursor ofacetaldehyde. In Section 2.4, we show that acetaldehyde yieldsmethyl radicals on TiO2; these methyl radicals can serve as theprogenitors of methane. In Section 2.5, we demonstrate thatneither glyoxylate nor glycolate (which are two other candidatetwo-carbon molecules) can serve as stepping stones in thereduction chain. The reaction scheme is further examined andelaborated upon in Section 3.1. In Section 3.2, we demonstratethat radicals generated on the TiO2 surface generally escape tothe bulk or weakly interact with the oxide surface; the oc-currence of such desorption is an important concern for thesuggested reaction scheme, as the bound radicals tend tooxidize. Finally, in Section 4, we discuss some implications ofour mechanistic study.We have omitted the experimental and computational sec-

tion, as the methods we used are identical to ref 1, and we

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direct the reader to that study for more detail. To conservespace, some tables and figures have been placed in theSupporting Information. Such figures have designator ″S″(e.g., Figure 1S).

2. RESULTS2.1. Photoreactions of Methanol. Since the EPR study of

Trifunac and co-workers,13,14 it has been widely accepted thatphotooxidation of methanol and other hydroxylated compounds(ROH) involves the alkyloxyl (Ti4+O−R) centers serving as holetraps; this trapping is followed by or concerted with depro-tonation of the resulting O 2p hole centers, e.g.

+ →+• + − + •h Ti O CH Ti O CHVB4

34

3 (8a)

→ ++ • + − • +Ti O CH Ti O C H H43

42 (8b)

(Here it is implied that the released proton is attached to theTiO2 surface, as the Ti2

4+OH+ or Ti4+OH2 centers, or watermolecules, as hydronium ions). The key prediction of this mech-anism is that the resulting radicals are bound to the oxide sur-face.15 However, as shown in Section 3.2, density functionaltheory (DFT) calculations (both ours and from other groups)21

and observations of the so-called ″current doubling″ on TiO222,23

suggest that such bound radicals may not be stable on TiO2,decaying through back electron transfer to the metal oxide

→ + ++ − • −• +Ti O C H e Ti H CO42 CB

42 (9a)

If reaction 9a occurs, this implies that the reverse reaction (thereduction of formaldehyde)

+ + →−• + + − •e Ti H CO Ti O C HCB4

24

2 (9b)

is energetically unfavorable. Thus, it is difficult to reconcile theformation of bound oxymethyl radicals and the reduction of theformaldehyde to methanol via one-electron reactions (to sub-stantiate reaction scheme 4). However, to our knowledge, it hasnever been demonstrated that such bound radicals are indeedstable on TiO2.Figure 1a shows the EPR spectrum obtained from the frozen

aqueous solution of anatase nanoparticles containing methanoland irradiated by 355 nm laser light at 77 K under acidic (trace(i)) and basic (trace (ii)) conditions. For comparison, wesuperimposed the EPR spectrum of the hydroxymethyl(•CH2OH) radical generated in 3 MeV β-radiolysis of frozenmethanol at 77 K (trace (iii)). It is seen that traces (ii) and (iii)are almost identical, which strongly suggests that the radicalobserved on TiO2 is, actually, the

•CH2OH radical rather thanthe Ti4+O−C•H2 radical or its protonated variant, Ti4+O(H)-C•H2. In alkaline solution, the EPR spectrum is different, as theradical exhibits smaller hyperfine coupling constants (hfcc) onthe two protons, which is consistent with the known propertiesof the •CH2O

−Alk+ radical (Table 1S). Thus, the progenitor ofthe latter EPR spectrum could be either the postulatedTi4+O−C•H2 (that is, Ti

4+−O−C•H2) radical or the physisorbed•CH2O

−Alk+ radical, whereas the radical observed in acidic solu-tion (actually, for pH < 8) is consistent with the •CH2OH radical.As the two radicals have rather different hfcc’s on their 13C nuclei(see Tables 1 and 1S and EPR simulations in Figure 1S), inFigure 1b we examined the EPR spectra obtained for 13CD3ODand 13CH3OH in these acidic and alkaline solutions (in D2O andH2O, respectively). These EPR spectra qualitatively correspond tosimulations shown in Figure 1S, suggesting that the isotropic hfccon 13C for the radical observed in acidic solutions is greater than

the hfcc for the radical observed in alkaline solutions. Figure 2 ex-hibits our simulations of the EPR spectra obtained for the TiO2/13CD3OD/D2O solutions, and Table 1 gives the optimized hfccparameters. It is seen that the hfcc for the radical observed inacidic solution is very close to the one observed for free •CH2OHradicals, whereas in alkaline solutions, this constant is lower thanfor the •CH2O

− radical in aqueous solutions.These results suggest that the photooxidation results in re-

lease of the radical from the surface

+ → ++ • + •Ti O CH H O Ti OH CH OH43 2

42 2 (10)

rather than reaction 8b. Trifunac and co-workers13 suggestedthat the bound alkoxyl groups can be reduced to alkyl radicalsvia the heteroatom transfer reaction1

+ + → +−• + − + + − •e Ti O R H Ti O H RCB4 4

(11)

(in this case, for R = Me). We did not observe the methylradical using 300 and 355 nm photoexcitation under acidic orbasic conditions, at any concentration of methanol nor anysample temperature for all of the TiO2 matrices that we used.Our results suggest that reaction 11 does not occur. Figure 2Sshows the analogous experiment for several ethanol isoto-pomers. These EPR spectra are fully accounted for by thecontributions from the CH3C

•HOH and •CH2CH2OH radicals

Figure 1. (a) First-derivative EPR spectra obtained in aqueoussolutions of TiO2 nanoparticles containing 5 wt % methanol-h3 with(ii) or without (i) 0.5 M KOH (see the legend in the plot). Thesesamples were irradiated by 355 nm laser light at 77 K, and the EPRspectra were obtained at 50 K, using a microwave power of 2 mW anda modulation amplitude of 2 G (100 kHz modulation). The resonancelines of the surface and lattice Ti3+ centers are not shown. Trace (iii) isthe EPR spectrum of the hydroxymethyl radical, •CH2OH, in neatmethanol-h3 irradiated by 3 MeV electrons at 77 K. Panel (b): Likepanel (a), for the three isotopomers of methanol, as indicated in theplot. The solid lines are the EPR spectra from pH 1.9 solutions, andthe dashed lines are from the solutions containing 0.5 M KOH.

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generated in the oxidation of the ethanol by TiO2; again, thereis no indication that the ethyl radical is generated in this photo-reaction.We conclude that methanol does not undergo one-electron

reduction on TiO2; instead it is oxidized to a f ree hydroxymethylradical. The last step of scheme 4 cannot be a sequence of twoone-electron reactions, and the prevalent photoreaction ofmethanol is oxidation. Disproportionation of the releasedhydroxymethyl radical with other radicals in the system (seesection 3.1) or reaction 9a yields formaldehyde, reversing thethird step in scheme 4.2.2. Photoreactions of Formaldehyde. Formaldehyde is

chemically unstable in aqueous solutions, undergoing base-catalyzed aldol condensation to glycolaldehyde involving its

acetal form (formose reactions),24 which can be schematicallywritten as

→2H CO HOCH CHO2 2 (12a)

The same product, glycolaldehyde, can occur through recom-bination of the formyl and hydroxymethyl radicals

+ →• •HC O CH OH HOCH CHO2 2 (12b)

While reaction 12a is interesting from a mechanistic standpoint, asit provides a molecular path to two-carbon molecules (Section 3.1),it complicates spectroscopic studies, as the aqueous formaldehydeis stabilized by methanol (“formalin”), which is photoreactive onTiO2 (Section 2.1). To avoid this complication, we generatedformaldehyde via high-temperature acidic hydrolysis of its linearpolymer (para-formaldehyde) and/or trimeric ortho-formaldehyde(Figure 3), rapidly added TiO2 to the mixture, adjusted the pH,and flash froze these solutions by immersion of the sample tubeinto liquid nitrogen.Figure 3a exhibits the EPR spectra from hydrolyzed para-

formaldehyde under weakly acidic (pH 1.9), strongly acidic, and

strongly basic conditions. In all of these systems, no organic radicalsother than HC•O were observed. The identity of the latter radicalis confirmed by 13C substitution (Figure 4 and Table 1S). Whilethere are resonance lines at the center, the same lines are observedwithout formaldehyde, so these EPR signals are from trapped-hole

Table 1. Optimized g- and hfcc Tensor Parameters for13C Nuclei for Hydroxymethyl (Low pH) and Oxymethyl(High pH) Radicals on Aqueous TiO2 Nanoparticles (50 K)Compared to Experimental Data in the Literature andGas-Phase DFT Calculations (B3LYP/6-31+G(d,p))

13C 13C

radical δg⊥ δg|| B||, G aiso, G•CD2OD

a 27 36 44.4 42.4•CD2O

−b 32 26 39.7 32.9•CH2OH 33c 47.4d

45.3e

•CH2O− 37c 37.7d

•CH2OHf 46.5g 59.2g

48.0h 37.5h

•CH2O−Li+f 41.4h 31.8h

•CH2O−f 20.6i 14.2i

aFor hydroxymethyl radicals. bFor oxymethyl radicals. cIsotropicδgiso = (δg|| + 2δg⊥)/3. We assumed coaxial (axially symmetrical) g andA tensors (B⊥ − B||/2). The hfcc's are given in Gauss (1 G = 10−4 T);δg = (g − 2) × 104. dFrom ref 39. eFrom ref 40. fB3LYP/6-31G(d,p)calculation for gas-phase radicals. gNonplanar (optimized geometry)radical; HCOH dihedral angle is 25°. hCs symmetry planar radical.

iC2vsymmetry (optimized geometry).

Figure 2. Simulation of the EPR spectra for photoirradiated 13CD3ODon anatase from Figure 1b obtained under acidic and basic conditions,respectively (as indicated in the plot), using the parameters given inTable 1. The vertical lines indicate the resonance lines for the mag-netic field oriented along the principal axes of (coaxial) g and A(13C)tensors.

Figure 3. EPR spectra obtained for photoirradiated solutions of 5 wt %formaldehyde on aqueous anatase. The formaldehyde was obtained byhydrolysis of (a) para- and (b) ortho-formaldehyde (see the insets forchemical structures). Trace (i) corresponds to the ″normal″ pH of 1.9;traces (ii) and (iii) were obtained in the presence of 2 wt % of 1 M HCland KOH, respectively; and trace (iv) is the simulated EPR spectrum ofthe formyl radical (whose resonance lines are indicated by arrows). Theresonance line from the oxygen hole centers on TiO2 contributes tothese EPR spectra; there is no evidence for the hydroxymethyl radical orother radical products of formaldehyde reduction.

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centers, which are known to be pH sensitive.20 The sameobservation applies to the formaldehyde generated from ortho-

formaldehyde. There is no evidence for Ti4+O−C•H2 or•CH2OH

radicals, which are the anticipated radical products of formaldehydereduction, while the formyl radical is the product of oxidation

+ → ++• • +h H CO HC O HVB 2 (13)

The methyl radical was also not observed in this photosystem. Likemethanol (Section 2.1), formaldehyde is oxidized on photoexcitedTiO2; there is no evidence for one-electron reduction under the relevantexperimental conditions. Thus, the photoreactions of methanol andformaldehyde on TiO2 are biased toward oxidation rather thanreduction. The reduction of these one-carbon molecules, if itoccurs at all, likely proceeds via concerted two-electron reactions.2.3. Photoreactions of Glyoxal and Glycolaldehyde.

Given the negative results of Sections 2.1 and 2.2 and thegeneral considerations in the Introduction, we turned to thetwo-carbon products. The most appealing candidates are theglyoxal generated in reaction 6 and glycolaldehyde generatedvia reactions 12a or 12b. Since glycolaldehyde is the product oftwo-electron reduction of glyoxal, both of these molecules arestrong candidates for the elusive “stepping stone” (Section 1).Figure 5a exhibits the EPR spectra of glyoxal on photo-

illuminated TiO2 in weakly acidic solutions. In addition to aweak resonance line of the formyl radical, there is a doublet thatcan only originate from a >C•H radical. In an alkaline solution,this doublet collapses to a poorly resolved line (Figure 5b). Assuggested by our simulations in Figure 3S (the reported hfcc’sfor the corresponding radicals are given in Table 1S), theradical observed in acidic solutions is HOC•HCHO, and theradical observed in alkaline solutions is C2H2O

−•. Thus, themain photoreaction is one-electron reduction, with oxidation as aside reaction

+ + →−• + •e C H OH H HOC HCHOCB 2 2 (14)

+ → ++• • +h C H O OC CHO HVB 2 2 2 (15)

→ +• •OC CHO CO HC O (16)

This unusual property of the glyoxal makes it a candidate speciesfor overcoming the bottleneck mentioned in the Introduction, asthis molecule is more readily reduced than oxidized. Furthermore,oxidation reaction 16 regenerates a formyl radical, which canrecombine with another formyl radical (reaction 6) to re-introduce the glyoxal, completing the cycle.Turning to the reactions of glycolaldehyde, we first observe

that one-electron reduction of this molecule, written as

+ →−• • −e HOCH CHO HOCH C HOCB 2 2 (17a)

produces the same radical anion as the one produced by Habstraction from ethylene glycol (HOCH2CH2OH) in stronglyalkaline solutions.25,26 The well-known reaction of this radicalanion is a 1,2-shift coupled to elimination of hydroxide25,26

→ +• − • −HOCH C HO CH CHO OH2 2 (17b)

Thus, the overall photoreaction can be written as

+ + → +−• + •e HOCH CHO H CH CHO H OCB 2 2 2(17c)

yielding the vinoxyl radical, •CH2CHO. Due to the energy gainaccompanying dehydration, reaction 17c is facile even thoughthe electron affinity of glycolaldehyde is low. The oxidation ofglycolaldehyde can yield either the same HOC•HCHO radicalthat is generated by the reduction of glyoxal or HOCH2C

•O

Figure 4. Solid lines are the EPR spectra obtained in photoirradiatedsolutions of TiO2 nanoparticles containing 5 wt % of (i) 12CH2O or(ii) 13CH2O generated from para-formaldehyde. The arrows indicatethe resonance lines from the isotopomers of the formyl radical, and thedashed lines are simulated EPR spectra. There is no evidence for otherorganic radicals present in this system. Trace (iii) is the spectrum ofthe H13C•O radical obtained by photoreduction of (CH3)2N

13CHOon TiO2 (from ref 1). Figure 5. (a) EPR spectra for photoirradiated aqueous anatase nano-

particles containing 1 M (i) glyoxal and (ii) glycolaldehyde at pH 1.9.Traces (i) were obtained at 2 mW, 50 K (solid lines), and 0.2 mW,12 K (dashed line). The arrow indicates the low-field line from theformyl radical. In trace (ii), the dashed line is the EPR spectrum fromhydroxymethyl as observed in the TiO2/MeOH system, replottedfrom Figure 1a. (b) EPR spectra from glyoxal on TiO2 obtained underthe (i) acidic and (ii) basic conditions. These transformations corres-pond to the protonation equilibrium shown in the inset. See Figure 3Sin the Supporting Information for simulations of these EPR spectra.

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which is likely to decarbonylate to yield the hydroxymethylradical

Unfortunately, the EPR spectra of the vinoxyl and the hydro-xymethyl radicals (which are both methylene radicals) arealmost identical as both have negligible hfcc’s on their HO andHCO protons. Figure 5a shows the EPR spectrum obtained byphotoirradiation of glycolaldehyde on TiO2. This EPR spec-trum arises from a methylene radical, and the comparison ofthis EPR spectrum to the one replotted from Figure 1a em-phasizes the similarity of the hfcc’s for this radical and •CH2OHon TiO2. While it is impossible to tell with certainty whether theobserved radical is a variant of the hydroxymethyl radical formedin reaction 18b or the vinoxyl radical formed in reaction 17c,there are differences between the traces shown in Figures 5a thatsuggest the occurrence of reaction 17c. We conclude that ourEPR results do not contradict the occurrence of reaction 17c,and this reaction looks plausible from the known radical chem-istry. The important point is that the sequential reduction ofglyoxal via glycolaldehyde leads to the vinoxyl radical, which isthe precursor of acetaldehydeone of the known products ofCO2 reduction on TiO2.

11

2.4. Photoreactions of Acetaldehyde. Figure 6 (trace(i)) exhibits the EPR spectrum observed in 355 nm photolysis of

acetaldehyde on TiO2 (we emphasize that none of the examinedmolecules absorbs the 355 nm photons; the laser light wasabsorbed by the oxide nanoparticles only). The quartet of re-sonance lines from the methyl radical is the predominant featureof this EPR spectrum with a broad, poorly resolved line over-lapping this quartet. The likely pathway to this methyl radicalinvolves oxidation of acetaldehyde, yielding the unstable acetylradical, which promptly decarbonylates27

+ → ++• • +h CH CHO CH C O HVB 3 3 (19a)

→ +• •CH C O CH CO3 3 (19b)

The broad EPR signal overlapping with the methyl radicalappears to be from the vinoxyl radical that is generated viathe alternative oxidation channel

+ → ++• • +h CH CHO CH CHO HVB 3 2 (19c)

There is no evidence for one-electron reduction (as is also thecase for formaldehyde) in this acidic solution. However therecould be photoreduction in alkaline solution (Figure 6), as theobserved EPR spectrum resembles the EPR spectrum expectedfor CH3C

•HO−, although the progenitor of this EPR spectrumcan be a variant of the vinoxyl radical (as shown in Figure 4S).Since the acetaldehyde may undergo aldol condensation undersuch alkaline conditions, we did not pursue the matter further.

2.5. Photoreactions of Glyoxylate and Glycolate. Wehave suggested glyoxal and glycolaldehyde as possible candi-dates for our sought-after stepping stone; however, as both theHC•O and CO2

−• radicals are present in the photosystem andthe CO2

−• radicals could be more abundant than the formylradical, the joining of the two carbons may actually involvereaction 20 rather than reaction 6

+ →• −• −HC O CO HC(O)CO2 2 (20)

Thus, it is prudent to examine the redox reactions of glyoxylate.Previous research suggested that carboxylic acids undergo aphoto-Kolbe reaction with elimination of CO2,

15 in this case

+ → ++• − •h HC(O)CO HC O COVB 2 2 (21a)

However, the hydroxyl radical oxidizes glyoxylate by H abstrac-tion rather than this reaction, so the second possibility is

+ → ++• − • − +h HC(O)CO C OCO HVB 2 2 (21b)

followed by decarboxylation of the unstable radical intermediate

→ +• − −•C OCO CO CO2 2 (21c)

In contrast, the reduction can either yield the HOC•HCO2−

radical (in analogy to reaction 14) or HCOC•O radical (inanalogy to reaction 3). The latter radical would also decarbo-xylate, yielding the formyl radical

Thus, the formyl radical can be the product of either reductionor oxidation, while the CO2

−• radical is the product of oxi-dation and the HOC•HCO2

− radical the product of reduction.Figure 7 shows EPR spectra obtained in photolysis of glyo-

xylic acid and glyoxylate on TiO2. Glyoxylate yields a weak EPRsignal from the HC•O radical (which was not observed at lowpH, thereby excluding reaction 22b) and a strong EPR signalfrom CO2

−• (which was significantly reduced at low pH; seeFigure 7). The latter can be isolated by subtraction of the EPRspectrum obtained at low pH from the EPR spectrum observedat higher pH (Figure 7). It is clear that both radicals are theproducts of photooxidation. In addition to these two radicals,there is also a very saturable EPR signal that can be isolated bysubtraction of the CO2

−• (or OC•OH) trace from the com-posite EPR spectrum (Figure 7). This yields a doublet corres-ponding to a >C•H radical, whose EPR spectrum resembles thespectrum of HOC•HCHO from glyoxal (Section 2.3 and alsoFigure 8). This is clearly the HOC•HCO2H radical; i.e., bothglyoxylate and glyoxylic acid are ef f iciently reduced on TiO2 byproton-coupled electron attachment.

Figure 6. EPR spectra from acetaldehyde on aqueous TiO2nanoparticles obtained under (i) acidic and (ii) basic conditions (0.5M H+ or OH−). The quartet of lines from the methyl radical (dashedline) is visible in trace (i), being superimposed on the broaderresonance lines of the •CH2CHO. In basic solutions, the α-hydroxyethyl radical or its deprotonated form (see the legend in theplot) may contribute to the observed EPR spectrum. See Figure 4S inthe Supporting Information for more simulations.

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Further reduction of the HOC•HCO2− radical yields glycolic

acid, HOCH2CO2−, which can also be generated in reaction 23

+ →• −• −CH OH CO HOCH CO2 2 2 2 (23)

Glycolate can be readily oxidized back to HOC•HCO2− or

•CH2OH radicals via

+ → +

→ +

+• − •

• − +

h HOCH CO CH OH CO (24a)

HOC HCO H (24b)

VB 2 2 2 2

2

Figures 8 and 5S show the EPR spectra obtained for glycolateat high (pH 1), medium (pH 6), and low (pH 10) acidity. Instrongly acidic solutions (Figure 8a), the prevalent EPR signalis the doublet from the HOC•HCO2H radical: reaction 24bprevails. In neutral solutions, both •CH2OH and HOC•HCO2

−

radicals are observed at 50 K shortly after the photolysis(Figure 8b); however, over time the •CH2OH radicaldisappears, and only the HOC•HCO2

− radical is observed(Figures 8b and 5S). This transformation is very rapid at 130 K(Figure 8b). Apparently, there is a reaction

+ → +• − • −CH OH HOCH CO CH OH HOC HCO2 2 2 3 2(25)

In alkaline solutions, both the •CH2O− and −OC•HCO2

−

radicals are initially observed (Figure 5S; the latter radical hasa more positive g-factor and smaller hfcc on the α-proton thanthe protonated form, see Figure 8b), but over time the •CH2O

−

radical disappears in a reaction analogous to reaction 25. Exceptfor these two radicals, no other species are observed. We pointout that a reaction analogous to reaction 3 with a generic acidRCO2H (including the glycolic acid)

+ + → +−• + + − •e Ti RCO H Ti O H RC OCB4

24

(26a)

yields the unstable RC•O radical, which promptly decarbon-ylates27

→ +• •RC O R CO (26b)

so this reduction reintroduces smaller fragment radicals throughwhich RCO2

− is generated in an R• + CO2−• recombination.

We conclude that for glycolate there is no reaction analogous toreaction 17c, which makes further reduction possible, and thecycle just loops back, as shown in Figure 6S. Thus, oxalate,glyoxylate, and glycolate cannot serve as stepping stones forfurther reduction.

3. DISCUSSION3.1. Overall Reaction Mechanism. To summarize Section

2, for TiO2 (under [weakly] acidic conditions):

(i) neither methanol nor formaldehyde can be reduced viaone-electron reactions, but both of these molecules arereadily oxidized to the hydroxymethyl and formylradicals, respectively;

(ii) glyoxal, the product of HC•O + HC•O recombination, ismore readily reduced to the HOC•HCHO radical than itis oxidized to the formyl radical;

Figure 7. EPR spectra from (i) 0.35 M sodium glyoxylate and (ii) 0.7 Mglyoxylic acid on aqueous TiO2 nanoparticles. The difference traces(iii) obtained by subtraction of trace (ii) from trace (i) reveal thepresence of CO2

−• (a narrow singlet line at 3375 G). Trace (iv) is aGaussian fit to this EPR signal, and trace (v) is the difference of trace(ii) and trace (iv). This difference trace is compared to the EPRspectrum of the HOC•HCO2H radical from Figure 8a (trace (vi)).The distortions in the EPR spectra are due to the strong overlap withthe low-field wing of the Ti3+ signal.

Figure 8. EPR spectra observed from 0.5 M glycolate on TiO2 at pH 1(panel (a)) and pH 6 (panel (b)). In both cases, the EPR spectrumobserved at 50 K slowly changes over time due to the occurrence ofreaction 25. In panel (a), trace (i) shows the EPR spectrum obtainedshortly after photolysis, while the solid lines indicate EPR spectraobtained 90 min later, at pH 1 (ii) and pH 10 (iii), respectively. Thevertical marks indicate the centers. In panel (b), the EPR spectrumobtained shortly after the photolysis of a pH 6 solution (trace (i)) iscompared to the spectrum of the hydroxymethyl radical from Figure 1(trace (ii)). Forty minutes later, the latter contribution to the EPRspectrum (trace (iii)) is much reduced. Warming the sample to 130 Kcompletes the reaction so that only the HOC•HCO2

− radical isobserved (trace (iv)). Superimposed on trace (iv) is trace (v), which isthe difference of traces (i) and (ii), suggesting that trace (i) is aweighed sum of EPR signals from the HOC•HCO2H and •CH2OHradicals.

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(iii) glycolaldehyde, the product of HC•O + •CH2OH recom-bination and/or aldol condensation of formaldehyde andmethanol (and reduction of the glyoxal on TiO2), iseither oxidized back to the hydroxymethyl radical or re-duced to the vinoxyl radical;

(iv) acetaldehyde is oxidized to the methyl radical;(v) neither HC•O + CO2

−• nor CO2−• + CO2

−• yields pro-ducts that can be further reduced on the metal oxide(Figure 6S): oxalate can only be oxidized (Section 1), andglycoxylate, though it can be reduced to the HOC•HCO2

−

radical, has a reduced form, glycolate, that can only beoxidized back to •CH2OH and HOC•HCO2

− radicals; itcannot be further reduced to glycoaldehyde (Section 2.5).

Thus, the only two-carbon products generated in reactions offirst-generation radicals (CO2

−•, HC•O, and •CH2OH) thatcan carry the reduction chain further are glyoxal and glyco-laldehyde (as the latter is reduced to the acetaldehyde). Anotherpossibility is the reaction of two hydroxymethyl radicals, yieldingethylene glycol28

→•2 CH OH HOCH CH OH2 2 2 (27)

In ref 29 we demonstrated that on TiO2 ethylene glycol can bephotooxidized to the HOC•HCH2OH radical (reaction 28),which is known to dehydrate to the vinoxyl radical in proton-catalyzed reaction 29)25,26

+ → ++• • +h HOCH CH OH HOC HCH OH HVB 2 2 2(28)

→ +• •HOC HCH OH CH CHO H O2 2 2 (29)

Therefore, the vinoxyl radical can be generated through the re-duction of glycolaldehyde (reaction 17c) or oxidation of ethyleneglycol (reactions 28 and 29). No other reaction pathways appar-ently lead to the desired products.Thus, the methyl radical, the progenitor of methane, can be

generated in the following way (Figure 9):

(a) the CO2 is stepwise reduced to the formyl radical in re-actions 1 to 3;

(b) two formyl radicals recombine to yield glyoxal (reaction 6);(c) glyoxal is reduced to glycolaldehyde (reaction 14);(d) glycolaldehyde is reduced to acetaldehyde (reaction 17c);(e) acetaldehyde is oxidized to the methyl radical (reactions

19a and 19b);(f) the organic intermediates generated in these reactions

(including formate, methanol, and formaldehyde) serveas sacrificial hole scavengers;

(g) the hydroxymethyl radicals recombine, yielding ethyleneglycol, which is oxidized to the vinoxyl radical (reactions28 and 29).

We stress that we have not demonstrated steps (c) and (d);rather we observed that glyoxal can be reduced to theHOC•HCHO radical, and glycolaldehyde can be reduced tothe vinoxyl radical. To complete these transformations, onemore H atom needs to be attached to these radicals: we haveproved the elaborate scheme shown in Figure 9 only halfway,due to the limitations imposed by our method, that is, EPRspectroscopy, which is selective to paramagnetic species. Never-theless, these transformations can be readily completed giventhat these radicals are involved in H-abstraction reactionsinvolving H donors (such as methanol)

+ ′ → + ′• •R R H RH R (30)

and disproportionation involving suitable radicals, such ashydroxymethyl28 and formyl30 radicals, e.g.

+ → +• •R CH OH RH H CO2 2 (31a)

+ → +• •R HC O RH CO (31b)

There is also possible proton-coupled reduction at the oxidesurface

+ + →−• • +e R H RHCB (32)

Reaction 25 is a specific example of reaction 30 that wasdirectly observed in our EPR experiments at low temperature(see Section 2.5 and Figure 5S).Reactions 30 and 31 indicate that one-carbon molecules and

their radicals can serve as reservoirs of H atoms for reduction oftwo-carbon molecules whose oxidation, in turn, replenishes thestock of HC•O and •CH2OH radicals in the reaction mixture.Two important examples of the disproportionation are the self-termination reactions28,30

→ +•2HC O CO H CO2 (33)

→ +•2 CH OH H CO CH OH2 2 3 (34)

which convert one-carbon radicals to oxidizable one-carbonmolecules, allowing them to serve as H atom donors in reaction

Figure 9. ″Glyoxal cycle″. In this scheme, RH stand for the generic(molecular or radical) donor of H atoms in reactions 30 and 31.

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30. The photoreactions shown in Figures 9 and 6S constantlyreintroduce formyl and hydroxymethyl radicals, formaldehyde,and methanol, and it is this process that keeps the reductiongoing (via reactions 30 and 31). These one- and two-carbonmolecules also serve as sacrificial hole acceptors, restocking theformyl radicals for glyoxal formation via reaction 6.The scheme in Figure 9 has two possible “shortcuts” that do

not involve redox or radical chemistry. One is reaction 12a,yielding glycolaldehyde which is subsequently reduced inreaction 17c. The second possible shortcut is surface-catalyzedesterification

+ → +CH OH HCO H HCO CH H O3 2 2 3 2 (35)

Methylformate is one of the known products of CO2reduction.12 In ref 1 we showed that the photooxidation ofmethylformate on TiO2 yields H loss radicals

while the main photoreduction reaction is analogous toreaction 3

+ + → +−• + + − •e Ti HCO CH Ti O CH HC OCB4

2 34

3(37)

In addition to reaction 37, methylformate can also react onTiO2 by dissociative electron attachment typical of otheresters31

+ + → +−• + + − •e Ti HCO CH Ti O CHO CHCB4

2 34

3(38)

generating a methyl radical. While reaction 38 is a minor sidereaction, it does generate the methyl radical through a(exclusively) reduction pathway, whereas the acetaldehydepathway shown in Figure 9 requires a combination of thereduction and oxidation and, therefore, cannot occur inelectrolytic reduction of CO2 on TiO2.

32

Together, these reactions constitute a cycle for CO2 fixationthat we suggest to call the ″glyoxal cycle″ to emphasize theunique role of glyoxal in the reduction chain on metal oxides.3.2. Radicals on Metal Oxides. In the scheme in Figure 9,

we suggest that the main mechanism for conversion of radicalintermediates to molecules is via reactions 30 and 31 ratherthan reaction 32. Indeed, the very fact that organic radicals canbe observed on the oxide surface by EPR argues against theoccurrence of facile reactions 9a or 32 despite the fact that suchradicals typically have lower ionization potentials and higherelectron affinities than their parent molecules.In ref 1, we observed that CO2

−• (OC•OH) radicals gen-erated by the photooxidation of formate (formic acid) on TiO2exhibited hfcc parameters indicating weak interaction with theoxide surface. The hfcc parameters for the formyl radicalgenerated in reactions 3 and 5 were also indicative of weakmatrix perturbation. Using the hfcc constants on carbon-13 inradicals generated in the TiO2/MeOH system (Section 2.1), wecan determine whether these radicals are free (expelled to thebulk or weakly interacting with the oxide surface) or bound(strongly interacting with the oxide surface).To this end, we used a first-principles DFT method (see

section 2 in ref 1 for more computational detail) to calculateEPR properties of radicals either in the gas phase, in aqueoussolution, or on an anatase (101) surface (Table 2). For boundradicals, we consider Ti4+O(H)C•H2 and Ti4+O−C•H2 centers

(structures 1 and 2 in Figure 10) and also several structures of•CH2OH radicals strongly interacting with undercoordinated

Ti4+ atoms on the surface (Table 2S). The latter species can beimmediately rejected, as the DFT calculations yield hfcc’s in the1Hα that strongly disagree with experimental estimates. The twostructures shown in Figure 10 are also unsatisfactory. Structure2 yields an hfcc on 13C that is 48% smaller than in the radicalobserved in alkaline TiO2 solutions (Figure 1 and Section 2.1)and 60% smaller than the radical in weakly acidic TiO2

solutions. Likewise, structure 1 gives an estimate for the hfccon the 13C nucleus that is 55% greater than the experimentalvalue (in acidic solutions). As seen from Table 2, (free)hydrated hydroxymethyl and oxymethyl radicals provide amuch better match for the experimental estimates for aiso(

13C)than either of these bound structures, and we believe that theseDFT calculations and our results demonstrate that the radicalsgenerated in the photooxidation of methanol are released f rom thesurface even if the parent molecule is bound to the surface through

Table 2. Calculated Isotropic (aiso) and Anisotropic (Bνν)hfcc Parameters for 13C and 1Hα Nuclei in OptimizedGeometries for Hydroxy- Or Oxymethyl Radicals in the GasPhase, Aqueous Solution, and on an Anatase (101) Surfacea

Using the B3LYP/6-31+G(2df,p) Method

radical [Bxx, Byy, Bzz], G aiso, G•CH2OH gas phase 13C [−23.9,−23.2,47.1] 51.5

1Hα [−12.6,−0.1,12.6] −15.31Hα [−12.7,0.1,12.5] −12.2

•CH2OH in H2Ob,c 13C [−23.4,−22.8,46.3] 48.1

1Hα [−12.4,0.1,12.3] −14.81Hα [−12.5,0.2,12.3] −13.1

•CH2O− gas phase 13C [−10.9,−9.8,20.7] 10.9

2 1Hα [−7.0,2.0,5.0] −12.1•CH2O

− in H2Oc,d 13C [−16.1,−15.6,31.7] 34.2

2 1Hα [−8.9,0.8,8.4] −8.9Ti4+O(H)CH2

• structure 1a 13C [−25.7,−24.8,50.5] 65.61Hα [−13.4,0.1,13.3] −14.41Hα [−13.0,−0.4,13.4] −17.0

Ti4+O−CH2• structure 2a 13C [−9.5,−8.9,18.5] 17.1

1Hα [−4.2,−0.3,4.4] −8.61Hα [−5.0,0.0,5.0] −8.6

aSee Figure 10. bThe experimental estimates for proton hfcc’s on Hα

are −17.7 and −18.5 G (ref 40). cThe solvent was simulated using thepolarizable continuum model (ref 41). dThe experimental estimatesfor proton hfcc’s on Hα are −14.3 G (ref 39).

Figure 10. Optimized structures for bound hydroxy- (1) andoxymethyl (2) radicals on the anatase (101) surface. See Table 2 forcalculated EPR parameters.

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its oxygen (reaction 10). Since the hydroxymethyl radical isreleased from the surface, further redox reactions involving thisradical are suppressed until it is readsorbed on the surface. Wesuggest that this release is a general occurrence of photoreactions onmetal oxides, as was previously suggested by Henderson.33

It is less clear, however, whether this release always occursduring photoreactions, as the bound radical may simply rapidlyreact further by oxidation (such as reaction 9a) or reduction(reaction 32) and in doing so may become invisible to EPRspectroscopy. Interestingly, the Ti4+−O−C•H2 radical shown inFigure 10 (structure 2) has low spin density on 13C chieflybecause of the partial electron (and spin) transfer to the tita-nium ion; i.e., it has Ti3+···OCH2 character. Thus, it ispossible that photooxidation can produce oxygen-boundradicals (reaction 8b) or free radicals (reaction 10), but thebound radical is unstable, decaying by reaction 9a, so that onlya released radical is observed by matrix isolation EPR.Given the propensity of the hydroxylated radicals to oxidize

back to aldehydes in reactions analogous to reaction 9a, weconsider it unlikely that (nonconcerted) two-electron reduction(involving reaction 32 as the second step) plays a significantrole in the catalytic cycle.

4. CONCLUDING REMARKSIn this study, we have asked whether the reduction of CO2 toCH4 on the surface of semiconducting, photoactive metal oxi-des involves one-carbon intermediates and concerted two-elec-tron reactions2,5,6,34,35 (scheme 4) or some other products thatcan be reduced by stepwise one-electron reactions.36 There ismore than one consideration favoring the second alternative, asexamination of the redox reactions of formate,1 formaldehyde,and methanol on TiO2 (Sections 2.1 and 2.2) showed no one-electron reduction of these adsorbates. This prompted us tosearch for complementary mechanisms, and we realized that theease of one-electron reduction considerably increases for two-carbon molecules as compared to the one-carbon molecules inreaction scheme 4. We recognized that glyoxal, which is theproduct of recombination of two formyl radicals (reaction 6),can serve as a strong electron acceptor, and we demonstratedthat its reduction on TiO2 is more facile than its oxidation(Section 2.3). The products of recombination of CO2

−• withCO2

−•, HC•O, and •CH2OH do not yield molecules that cancarry the reduction chain more than one step further withoutrecycling the products (Section 2.5 and Figure 6S). Thereduction of glycolaldehyde, which is the product of (i) glyoxalreduction, (ii) aldol condensation of formaldehyde, and (iii)recombination of HC•O and •CH2OH, is also facile, as the cor-responding radical anion is unstable to dehydration and yieldsthe vinoxyl radical. The latter can be reduced to acetaldehyde,which is photooxidized to the methyl radical, the precursor ofthe methane. Other pathways to the methyl radical could in-volve dissociative electron attachment to the methylformate thatis generated through esterification of formic acid by methanol.We suggest that one-carbon molecules play only an auxiliary rolein methanogenesis by serving as sacrificial hole scavengers andreplenishing the pool of formyl and hydroxymethyl radicalswhose reactions (i) lead to the formation of reducible two-carbon molecules and (ii) maintain the reduction chain throughH abstraction and disproportionation reactions with the two-carbon radicals.Thus, we suggest that methanogenesis occurs through two-

carbon molecules and involves mainly one-electron reactions incontradistinction to reaction scheme 4 that involves one-carbon

molecules and two-electron reactions. The photoredox, radical,and molecular reactions shown in Figures 9 and 6S comprisethe complex “glyoxal cycle.”While the critical steps of this cycle have been demonstrated

in this study, some of these steps remain tentative. In particular,we did not demonstrate how the radicals are reduced to mole-cules, though the radical reactions that we suggest as a means ofsuch reduction are well-known. More work to prove or dis-prove this reaction mechanism using other techniques isneeded. In addition to methanogenesis, the glyoxal cycle ac-counts for several known byproducts, such as methanol, for-mate, formaldehyde, acetaldehyde, and methylformate, forwhich (to our best knowledge) no specific reaction scheme hasbeen suggested heretofore. We predict that this cycle alsoproduces glyoxal and glycolaldehyde (and, possibly, glycoxylateand glycolate) as minor products (given their high reactivity).These products have not yet been observed, and the detectionof these products could corroborate the scheme shown inFigure 9.While this glyoxal cycle is primitive as compared to the

Calvin cycle through which biological nature fixes atmosphericcarbon as glyceraldehyde-3-phosphate37 (with relatively lowconversion efficiency, as the reaction intermediates are bothgenerated and consumed), this glyoxal cycle yields complexorganic molecules as byproducts of CO2 reduction, and itrequires only a hydrated metal oxide surface (abundant onmany planets) and UVA light as opposed to the sophisticatedenzymatic machinery of a living cell.Apart from the obvious significance for production of

fuels and carbon sequestration, the glyoxal cycle is one ofthe simplest realizations for abiogenic fixation of CO2 from theatmospheres of terrestrial planets that can operate over a widerange of conditions. Photoactive metal oxides (e.g., particulateiron(III) oxides that constitute most of the martian regolith)are ubiquitous on both Earth and Mars. Ages ago, the atmo-spheres of these planets were reducing and transparent to UVAradiation, and both planets had water.38 We argue that youngEarth and Mars (the latter, both early and modern) could havebeen a vast ″solar panel factory″ abiotically fixing atmosphericCO2 and converting it to CH4 and complex organic molecules.These molecules look remarkably similar to the common micro-bial metabolites. Some of these molecules (e.g., glycolaldehyde)can undergo further aldol condensation24 producing 3- and 4-atomic carbohydrates: the very building blocks of organic life. Inother words, the glyoxal cycle could have been nature’s first draftof the photosynthetic cycle that after many millions of years ofevolutionary tinkering became the Calvin cycle that gives us ourdaily bread.

■ ASSOCIATED CONTENT

*S Supporting InformationA file containing the list of reactions, Tables 1S and 2S, andFigures 1S to 6S with captions, including the experimental andsimulated EPR spectra. This material is available free of chargevia the Internet at http://pubs.acs.org.

■ AUTHOR INFORMATION

Corresponding Author*Tel.: (630) 252-9516. E-mail shkrob@anl.gov.

NotesThe authors declare no competing financial interest.

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■ ACKNOWLEDGMENTS

This work is supported by Grant No. NNH08A65I from theMars Fundamental Research Program of NASA (to I.A.S. andT.W.M.) and the Division of Chemical Sciences, Geosciences,and Biosciences, Office of Basic Energy Sciences of the U.S.Department of Energy under Contract No. DE-AC02-06CH11357, including the use of the Center for NanoscaleMaterials. I.A.S. thanks N. Dimitrijevic, T. Rajh, D. Catling, andD. Tiede for many useful discussions.

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The Journal of Physical Chemistry C Article

dx.doi.org/10.1021/jp300122v | J. Phys. Chem. C 2012, 116, 9450−94609460