Article pubs.acs.org/JPCA
Role of Hydrogen Bonding on the Reactivity of Thiyl Radicals: A Mass Spectrometric and Computational Study Using the Distonic Radical Ion Approach Published as part of The Journal of Physical Chemistry virtual special issue “Mark S. Gordon Festschrift”. Sandra Osburn,†,‡ Bun Chan,*,‡,∥ Victor Ryzhov,⊥ Leo Radom,*,‡,§ and Richard A. J. O’Hair*,†,‡ †
School of Chemistry and Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, 30 Flemington Rd, Parkville, Victoria 3010, Australia ‡ ARC Centre of Excellence for Free Radical Chemistry and Biotechnology, University of Sydney, Sydney, NSW 2006, Australia § School of Chemistry, University of Sydney, Sydney, NSW 2006, Australia ∥ Graduate School of Engineering, Nagasaki University, Bunkyo 1-14, Nagasaki 852-8521, Japan ⊥ Department of Chemistry and Biochemistry and Center for Biochemical and Biophysical studies, Northern Illinois University, Dekalb, Illinois 60115, United States S Supporting Information *
ABSTRACT: Experimental and computational quantum chemistry investigations of the gas-phase ion−molecule reactions between the distonic ions +H3N(CH2)nS• (n = 2− 4) and the reagents dimethyl disulfide, allyl bromide, and allyl iodide demonstrate that intramolecular hydrogen bonding can modulate the reactivity of thiyl radicals. Thus, the 3ammonium-1-propanethiyl radical (n = 3) exhibits the lowest reactivity of these distonic ions toward all substrates. Theoretical calculations on this distonic ion highlight that its most stable conformation involves a six-membered ring configuration, and that it has the strongest intramolecular hydrogen bond. In addition, the calculations indicate that the barrier heights for radical abstraction by this hydrogen-bond-stabilized 3-ammonium-1-propanethiyl radical are the highest among the systems examined, consistent with the experimental observations.
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the structure and reactivity of thiyl distonic ions16−19 derived from cysteine, its derivatives, and peptides,20−28 we discovered that the thiyl radical of cysteine, 1a (Scheme 2), is more reactive with respect to atom abstraction reactions than homocysteine, 1b. We speculated that this may be due to differences in the strength of intramolecular hydrogen bonding.29 In the present study, we use a combination of multistage mass-spectrometry-based experiments in an ion trap30 and quantum chemistry calculations31 to examine more closely how intramolecular hydrogen bonding32−34 influences the fundamental gas-phase reactivity of charge-tagged thiyl radicals toward the reagents dimethyl disulfide, allyl bromide, and allyl iodide. Thus, the reactivity of the following series of ammonium thiyl radicals H3N+(CH2)nS• was examined (Scheme 2): 1-ammonium-1-methanethiyl, 2a (n = 1); 2-
INTRODUCTION Nature exploits thiyl radicals of cysteine residues within ribonucleotide reductases to transform RNA to DNA via a key step involving intermolecular hydrogen-atom transfer (HAT) (Scheme 1).1,2 Although the key roles of the various residues in facilitating this transformation are now reasonably well understood3 and theoretical models have been developed,4 remarkably little is known as to how the surrounding protein architecture modulates the reactivity of the thiyl radical, particularly that involving intramolecular or intermolecular hydrogen bonding.5,6 On the contrary, hydrogen bonding can have a profound effect on the rates and modes of reactivity of other classes of radicals in the condensed7,8 and gas9,10 phases. The formation and gas-phase reactivity of amino acid and peptide radical cations has been the subject of considerable research over the past decade,11−14 and there is growing evidence that intramolecular hydrogen bonding at radical sites can influence their unimolecular and bimolecular chemistry. For example, intramolecular hydrogen bonding of the side chains of serine and threonine constrains free radical reaction dynamics at these residues.15 As part of a series of studies on © XXXX American Chemical Society
Received: August 24, 2016 Revised: September 28, 2016
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DOI: 10.1021/acs.jpca.6b08544 J. Phys. Chem. A XXXX, XXX, XXX−XXX
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The Journal of Physical Chemistry A Scheme 1. Simplified Pathway for HAT in RNA Reductasesa
a The sulfur radical at cysteine residue 290 in the R1 subunit of ribonucleotide reductase (complex A) abstracts a hydrogen atom from the 3′ position of a nucleoside diphosphate to form complex B, which is the first step in forming a 2′-deoxyribonucleotide, C.
spectrometer30 at a flow rate of 5.0 μL min−1. In the positive ion mode, the S-nitrosoammonium ions, H3N+(CH2)nSNO were formed and the source conditions were tuned to optimize their signal. Typical ESI conditions used were: spray voltage, 3.0−5.0 kV, capillary temperature, 250−270 °C, nitrogen sheath pressure, 15−20 (arbitrary units), and capillary voltage/ tube lens offset, were tuned to maximize the desired peak. The injection time was set using the AGC (automatic gain control) function. All ions mass-selected for collision-induced dissociation (CID) and ion−molecule reactions consisted of the most abundant isotopes (12C, 1H, 14N, 16O, and 32S), and mass selection was achieved using a 1−2 Th window. The H3N+(CH2)nSNO ions were mass-selected and subjected to CID in a series of MS2 experiments, which led to the homolysis of the S−NO bond to generate the ammonium thiyl radicals H3N+(CH2)nS• (eq 1):
Scheme 2. Structures of Distonic Ammonium Thiyl Radicals with Various Intramolecular Hydrogen-Bonding Environmentsa
a
Previously studied29 cysteine radical cation, 1a, and homocysteine radical cation, 1b, and model ammonium thiyl distonic radical cations H3N+(CH2)nS• studied here: 1-ammonium-1-methanethiyl, 2a (n = 1); 2-ammonium-1-ethanethiyl, 2b (n = 2); 3-ammonium-1-propanethiyl, 2c (n = 3); and 4-ammonium-1-butanethiyl 2d (n = 4).
H3N+(CH 2)n SNO → H3N+(CH 2)n S• + •NO
(1)
These charged thiyl radicals were further mass-selected and allowed to undergo ion−molecule reactions in a series of MS3 experiments. The neutral reagents (dimethyl disulfide, allyl bromide, or allyl iodide) were introduced into the mass spectrometer via the helium bath gas line. The ion−moleculereaction conditions were activation energy 0%, Q of 0.25, and the reaction time between 10 and 10000 ms prior to ejection from the ion trap for detection. Theoretical rates for the reaction were calculated with the program COLRATE36 using the average dipole orientation (ADO) theory of Su and Bowers.37 Quantum Chemistry Calculations. Standard density functional theory (DFT) calculations were carried out with Gaussian 09.31 Geometries were optimized at the B3-LYP/ def2-SVP level. Improved single-point energies were obtained at the B98/def2-TZVP level. This was found to show good agreement with the high-level G4(MP2)-6X procedure38 in our preliminary assessment study for a prototypical set of systems representative of those examined in the present study. Zeropoint vibrational energies and thermal corrections for enthalpies and entropies at 298 K were obtained using unscaled B3-LYP harmonic vibrational frequencies. Unless otherwise noted, energies in the text refer to free energies at 298 K. All calculated structures are available in the Supporting Information.
ammonium-1-ethanethiyl, 2b (n = 2); 3-ammonium-1-propanethiyl, 2c (n = 3); and 4-ammonium-1-butanethiyl 2d (n = 4).
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EXPERIMENTAL AND THEORETICAL METHODS Experimental Section. Reagents. The following reagents were used as received: 2-amino-1-ethanethiol (Fluka, > 97%); 3-amino-1-propanethiol (Aldrich, 95%); 4-amino-1-butanethiol (Otava, 95%); tert-butyl nitrite (Aldrich, 90%); dimethyl disulfide (Sigma, 98%); allyl bromide (Aldrich, 99%); allyl iodide (Aldrich, 98%). Mass Spectrometry. Multistage mass spectrometry (MSn) experiments were conducted on a Thermo Scientific (Bremen, Germany) LTQ FT hybrid mass spectrometer consisting of a linear ion trap (LTQ) coupled to a Fourier-transform ion cyclotron resonance (FT-ICR) mass spectrometer, which has been modified to allow the study of ion−molecule reactions.30 Under ion−molecule reaction conditions, collisions with the helium bath gas quasi-thermalizes the ions to room temperature.35 Generation and Ion−Molecule Reactions (IMR) of Ammonium Thiyl Radicals 2a−2d. Each of the amine thiols (2-amino-1-ethanethiol; 3-amino-1-propanethiol, and 4-amino1-butanethiol) were separately nitrosylated in 1:1 methanol− water solution with tert-butyl nitrite as described previously.20−28 The resultant reaction solutions containing the Snitrosoamines were diluted to a 0.5 mM 1:1 methanol−water solution and directly infused into the electrospray ionization (ESI) source of a modified hybrid LTQ FT-ICR mass
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RESULTS AND DISCUSSION Experimental Examination of Radical Abstraction Reactions from Dimethyl Disulfide, Allyl Bromide, and B
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Table 1. Rates and Branching Ratios for Ion−Molecule Reaction Products of Ammonium Thiyl Radicals 2b−2d Reacting with Dimethyldisulfide, Allyl Bromide and Allyl Iodide ion +
neutral •
H3N (CH2)2S , H3N+(CH2)3S•, H3N+(CH2)4S•, H3N+(CH2)2S•, H3N+(CH2)3S•, H3N+(CH2)4S•, H3N+(CH2)2S•,
a
2b 2c 2d 2b 2c 2d 2b
CH3SSCH3 CH3SSCH3 CH3SSCH3 CH2CHCH2Br CH2CHCH2Br CH2CHCH2Br CH2CHCH2I
H3N+(CH2)3S•, 2c
CH2CHCH2I
H3N+(CH2)4S•, 2d
CH2CHCH2I
rate, kexpta
reaction efficiencyb
100% 100% 100% 20%
8.70 5.55 6.05 9.68 5.67 7.22 16.0
56 35 40 67 44 59 112
18%
12.1
92
21%
13.1
105
product(s) and branching ratios +
H3N (CH2)2SSCH3, 100% H3N+(CH2)3SSCH3, 100% H3N+(CH2)4SSCH3, 100% H3N+(CH2)2SCH2CHCH2, H3N+(CH2)3SCH2CHCH2, H3N+(CH2)4SCH2CHCH2, H3N+(CH2)2SCH2CHCH2, H3N+(CH2)2SI, 80% H3N+(CH2)3SCH2CHCH2, H3N+(CH2)3SI, 82% H3N+(CH2)4SCH2CHCH2, H3N+(CH2)4SI, 79%
×10−10 molecules cm3 s−1. bReaction efficiency = (kexpt/kADO) × 100.
Allyl Iodide by Distonic Ions H3N+(CH2)nS• 2b, 2c, and 2d. 2-Ammonium-1-ethanethiyl, 2b (n = 2), 3-ammonium-1propanethiyl, 2c (n = 3), and 4-ammonium-1-butanethiyl 2d (n = 4) were all readily and cleanly formed via CID of the protonated S-nitrosoamines, H3N+(CH2)nSNO (eq 1, data not shown). All of these distonic ammonium thiyl radical cations undergo ion−molecule reactions with substrates that have been designed as probes for the radical sites of distonic ions.18 These reactions proceed via radical abstraction from the substrate. In the case of dimethyl disulfide, an •SCH3 group is abstracted (eq 2, Supporting Information Figure S1), whereas allyl bromide and allyl iodide react via allyl-group transfer (eq 3, Supporting Information Figure S2) and allyl-group transfer in competition with iodine atom abstraction, respectively (eqs 4 and 5, Supporting Information Figure S3).
exponential decay for pseudo-first-order kinetics (Supporting Information Figure S4) suggests that these distonic ions are not contaminated by isomeric impurities. Calculated Hydrogen-Bond Strengths and Reaction Profiles. One plausible explanation for the observed reactivity orders is that the chain length modulates the strength of the hydrogen bond that may form between the sulfhydryl radical site and the ammonium ion, and this in turn modifies its reactivity. Although 1-ammonium-1-methanethiyl, 2a (n = 1) cannot be formed experimentally as the required 1-amino-1methanethiol precursor is unavailable,39−41 we have nonetheless used DFT calculations to examine its structure and reactivity together with those of the related 2b−2d. 2c has the shortest calculated hydrogen bond between the ammonium hydrogen and the sulfur radical (2.21 Å, Figure 1), suggesting
H3N+(CH 2)n S• + CH3SSCH3 → H3N+(CH 2)n SSCH3 + CH3S•
(2)
H3N+(CH 2)n S• + CH 2CHCH 2Br → H3N+(CH 2)n SCH 2CHCH 2 + Br •
(3)
H3N+(CH 2)n S• + CH 2CHCH 2I → H3N+(CH 2)n SCH 2CHCH 2 + I•
(4)
H3N+(CH 2)n S• + CH 2CHCH 2I → H3N+(CH 2)n SI + CH 2CHCH 2•
Figure 1. DFT-calculated structures (B3-LYP/def2-SVP) and relative energies (ΔG, ΔH in parentheses, B98/def2-TZVP, kJ mol−1) of hydrogen-bonded conformations 2a−2d and extended conformations 2b′−2d′ of the ammonium thiyl radicals.
(5)
For all neutral substrates, the following qualitative reactivity order was observed: 2b > 2d > 2c. To quantify these reactivity orders, careful rate measurements were carried out using different concentrations of neutrals on different days. Table 1 summarizes the rates for the reactions of the ammonium thiyl radicals with dimethyl disulfide, allyl bromide, and allyl iodide, as well as the branching ratios of the products from these reactions. Dimethyl disulfide is the least reactive reagent, giving the following order of reaction efficiencies: 2b (56) > 2d (40) > 2c (35). The reaction efficiency order for allyl bromide is 2b (67) > 2d (59) > 2c (44). The reactions with allyl iodide are essentially at the collision rate, although 2c is slightly less reactive. Finally, the fact that the radical ion population completely reacts away with all substrates at long reaction times and exhibits the expected
that this is the strongest hydrogen bond among the distonic ammonium thiyl radical cations. To gain further insights into the stabilities of these intramolecular hydrogen bonds, the extended conformations of 2b′−2d′ were calculated.42 In each case, these were found to be less stable than the corresponding hydrogen-bonded conformations (Figure 1).43 Comparing the free energies and enthalpies of the hydrogen-bonded and extended conformations suggests that the relative hydrogenbond strengths are in the order 2c > 2d > 2b. This is nicely consistent with the experimentally observed reactivities. To obtain a more direct connection with the experimental reactivities, we next examined the barriers for the radical C
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Figure 2. DFT-calculated structures (B3-LYP/def2-SVP) and relative energies (B98/def2-TZVP, kJ mol−1) of transition structures for the reactions of the ammonium thiyl radicals 2a−2d: (a) with dimethyl disulfide; (b) with allyl iodide leading to allyl abstraction via attack at carbon; (c) with allyl iodide leading to abstraction via attack at iodine.
Table 2. Calculated Free Energy Barriers (B98/def2-TZVP, kJ mol−1) and Enthalpy Barriers (B98/def2-TZVP, kJ mol−1, in Parentheses) for Reactions Involving the Amine Thiol Radicals (NH3+(CnH2n)S•) Reacting with Dimethyl Disulfide (DMDS), Allyl Bromide (All-Br), and Allyl Iodide (All-I) n 1 2 3 4 a
DMDS 0.2 8.6 17.9 12.7
(−50.4) (−41.3) (−32.4) (−38.1)
All-Bra 0.9 16.9 25.0 23.6
(−39.9) (−22.7) (−15.4) (−16.6)
All-Bra −17.0 −0.9 7.3 4.7
(−68.2) (−53.2) (−42.4) (−45.8)
All-Ia −31.7 −14.4 −7.3 −8.4
(−67.9) (−51.5) (−45.4) (−44.8)
All-Ia −20.2 −4.4 6.5 3.4
(−70.0) (−55.3) (−43.5) (−47.1)
The reaction center is underlined.
abstraction reactions given by eqs 2−5. Figure 2 and Supporting Information Figure S6 show the key transition structures for the radical abstraction reactions, whereas Table 2 collates the calculated free energy barriers/complexation energies for generation of each of the possible products in these reactions. A comparison of the structures of each of the transition structures with those of the hydrogen-bonded reactant ammonium thiyl radicals, 2a−2d, reveals that the hydrogen bonding is largely maintained in the transition structures. A comparison between the experimental rate and branching ratio data (Table 1) and the calculated activation energies (Table 2) reveals consistent reactivity trends. For any given ammonium thiyl radical, the reactivity is substrate-dependent, with the following order: allyl iodide (fastest) > allyl bromide > dimethyl disulfide (slowest). For all substrates, 3-ammonium-1propanethiyl, 2c, shows the lowest reactivity. This is consistent with the theoretical calculations, which show that 2c has the highest activation barriers, and that it has the highest hydrogenbond energy. The calculated free energy barriers are also in agreement with the experimentally determined branching ratios
associated with the regioselectivity for attack by the thiolate radical onto allyl bromide and allyl iodide. Thus, for the reactions with allyl bromide, the only observed product is the addition of the allyl group to the radical. This is consistent with the free energy barrier for the addition of the allyl group being lower in energy than the barriers for the addition of the bromide. On the contrary, for each of the radical reactions with allyl iodide, the main product formed is the addition of iodide, with a smaller amount of the addition of the allyl group also observed. Again, this is consistent with the calculated free energy barriers, where in this case the transition structure for the addition of the iodide lies lower in energy than that for the addition of the allyl group.
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CONCLUDING REMARKS Intramolecular ionic hydrogen bonding between a sulfur radical and an ammonium hydrogen in ammonium thiolate distonic ions modulates the reactivity of the radical site. Experimentally, the 3-ammonium-1-propanethiyl radical, 2c, exhibits the lowest reactivity of these distonic ions toward all substrates. DFT calculations indicate that the most stable conformation of this D
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(5) Dénès, F.; Pichowicz, M.; Povie, G.; Renaud, P. Thiyl Radicals in Organic Synthesis. Chem. Rev. 2014, 114, 2587−2693. (6) Schöneich, C.; Dillinger, U.; von Bruchhausen, F.; Asmus, K. D. Oxidation of Polyunsaturated Fatty Acids and Lipids Through Thiyl and Sulfonyl Radicals: Reaction Kinetics, and Influence of Oxygen and Structure of Thiyl Radicals. Arch. Biochem. Biophys. 1992, 292, 456− 467. (7) Salamone, M.; Bietti, M. Tuning Reactivity and Selectivity in Hydrogen Atom Transfer from Aliphatic C−H Bonds to Alkoxyl Radicals: Role of Structural and Medium Effects. Acc. Chem. Res. 2015, 48, 2895−2903. (8) Litwinienko, G.; Ingold, K. U. Solvent Effects on the Rates and Mechanisms of Reaction of Phenols with Free Radicals. Acc. Chem. Res. 2007, 40, 222−230. (9) Vaida, V. Perspective: Water Cluster Mediated Atmospheric Chemistry. J. Chem. Phys. 2011, 135, 020901. (10) Lesslie, M.; Piatkivskyi, A.; Lawler, J.; Helgren, T.; Osburn, S.; O’Hair, R. A. J.; Ryzhov, V. The Effects of Intramolecular Hydrogen Bonding on the Reactivity of Phenoxyl Radicals in Model Systems. Int. J. Mass Spectrom. 2015, 390, 124−131. (11) Hopkinson, A. C. Radical Cations of Amino Acids and Peptides: Structures and Stabilities. Mass Spectrom. Rev. 2009, 28, 655−671. (12) Chu, I. K.; Laskin, J. Review: Formation of Peptide Radical Ions Through Dissociative Electron Transfer in Ternary Metal−ligand− peptide Complexes. Eur. Mass Spectrom. 2011, 17, 543−556. (13) Tureček, F.; Julian, R. R. Peptide Radicals and Cation Radicals in the Gas Phase. Chem. Rev. 2013, 113, 6691−6733. (14) Oh, H. B.; Moon, B. Radical-driven Peptide Backbone Dissociation Tandem Mass Spectrometry. Mass Spectrom. Rev. 2015, 34, 116−132. (15) Thomas, D. A.; Sohn, C. H.; Gao, J.; Beauchamp, J. L. Hydrogen Bonding Constrains Free Radical Reaction Dynamics at Serine and Threonine Residues in Peptides. J. Phys. Chem. A 2014, 118, 8380−8392. (16) Yates, B. F.; Bouma, W. J.; Radom, L. Detection of the Prototype Phosphonium (CH2PH3), Sulfonium (CH2SH2) and Chloronium (CH2ClH) Ylides by Neutralization-reionization Mass Spectrometry: A Theoretical Prediction. J. Am. Chem. Soc. 1984, 106, 5805−5808. (17) Hammerum, S. Distonic Radical Cations in Gaseous and Condensed Phase. Mass Spectrom. Rev. 1988, 7, 123−202. (18) Stirk, K. M.; Kiminkinen, L. K. M.; Kenttamaa, H. I. Ion− molecule Reactions of Distonic Radical Cations. Chem. Rev. 1992, 92, 1649−1665. (19) Williams, P. E.; Jankiewicz, B. J.; Yang, L.; Kenttämaa, H. I. Properties and Reactivity of Gaseous Distonic Radical Ions with Aryl Radical Sites. Chem. Rev. 2013, 113, 6949−6985. (20) Ryzhov, V.; Lam, A. K. Y.; O’Hair, R. A. J. Gas-Phase Fragmentation of Long-Lived Cysteine Radical Cations Formed via NO Loss from Protonated S-Nitrosocysteine. J. Am. Soc. Mass Spectrom. 2009, 20, 985−995. (21) Lam, A. K. Y.; Ryzhov, V.; O’Hair, R. A. J. Mobile Protons versus Mobile Radicals: Gas Phase Unimolecular Chemistry of Radical Cations of Cysteine Containing Peptides. J. Am. Soc. Mass Spectrom. 2010, 21, 1296−1312. (22) Osburn, S.; Steill, J. D.; Oomens, J.; O’Hair, R. A. J.; van Stipdonk, M.; Ryzhov, V. Structure and Reactivity of the Cysteine Methyl Ester Radical Cation. Chem. - Eur. J. 2011, 17, 873−879. (23) Osburn, S.; Berden, G.; Oomens, J.; O’Hair, R. A. J.; Ryzhov, V. Structure and Reactivity of the N-Acetyl-Cysteine Radical Cation and Anion: Does Radical Migration Occur? J. Am. Soc. Mass Spectrom. 2011, 22, 1794−1803. (24) Osburn, S.; O’Hair, R. A. J.; Ryzhov, V. Gas Phase Reactivity of Sulfur-Based Radical Ions of Cysteine Derivatives and Small Peptides. Int. J. Mass Spectrom. 2012, 316-318, 133−139. (25) Osburn, S.; Berden, G.; Oomens, J.; O’Hair, R. A. J.; Ryzhov, V. S-to-αC Radical Migration in the Radical Cations of Gly-Cys and CysGly. J. Am. Soc. Mass Spectrom. 2012, 23, 1019−1023.
distonic ion involves a six-membered ring configuration and that it has the strongest hydrogen bond of the various ammonium thiolate distonic ions examined. In addition, the calculated barrier heights for radical abstraction from the 3ammonium-1-propanethiyl radical are the highest, consistent with the experimental observations. Our present results are consistent with those obtained previously for related distonic ions that can adopt stable conformations that exhibit intramolecular ionic hydrogen bonding. Thus, both the homocysteinyl radical cation 1b29 and an appropriately substituted phenoxyl radical cation,10 containing six-membered-ring hydrogen-bonded radicals, are found to display lowest reactivities.
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ASSOCIATED CONTENT
* Supporting Information S
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpca.6b08544. Mass spectra showing ion−molecules reactions, kinetic plots for the reactions, DFT calculated structures and relative energies of transition structures for the reactions of the ammonium thiyl radicals 2a−2d with allyl bromide, Cartesian coordinates of all species examined, and a full citation for ref 31 (PDF)
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AUTHOR INFORMATION
Corresponding Authors
*B. Chan. E-mail:
[email protected]. *L. Radom. E-mail:
[email protected]. *R. O’Hair. E-mail:
[email protected]. Fax: (+) 61 3 9347 8124). Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS We thank the Australian Research Council for financial support via the ARC Centre of Excellence for Free Radical Chemistry and Biotechnology, as well as financial support from Nagasaki University and the Japan Society for the Promotion of Science. The authors also gratefully acknowledge the generous allocation of grants for computing time from the National Computational Infrastructure National Facility (NCI NF), Intersect Australia Ltd, RIKEN Advanced Center for Computing and Communication, and the Institute for Molecular Science Japan. Dedicated to Professor Mark S. Gordon on the occasion of his 75th birthday and in recognition of his important contributions to computational quantum chemistry.
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F
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