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Apr 14, 2016 - The Dow Chemical Company, Marlborough, Massachusetts 01752, United States. §. Department of Chemistry, Yale University, New Haven, ...
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Effect of Chloride Depletion on the Magnetic Properties and the Redox Leveling of the Oxygen-Evolving Complex in Photosystem II Muhamed Amin,*,† Ravi Pokhrel,‡ Gary W. Brudvig,§ Ashraf Badawi,† and S. S. A. Obayya† †

Center for Photonics and Smart Materials, Zewail City of Science and Technology, Sheikh Zayed District, 6th of October City, 12588 Giza, Egypt ‡ The Dow Chemical Company, Marlborough, Massachusetts 01752, United States § Department of Chemistry, Yale University, New Haven, Connecticut 06520-8107, United States S Supporting Information *

ABSTRACT: Chloride is an essential cofactor in the oxygenevolution reaction that takes place in photosystem II (PSII). The oxygen-evolving complex (OEC) is oxidized in a linear four-step photocatalytic cycle in which chloride is required for the OEC to advance beyond the S2 state. Here, using density functional theory, we compare the energetics and spin configuration of two different states of the Mn4CaO5 cluster in the S2 state: state A with Mn13+ and B with Mn43+ with and without chloride. The calculations suggest that model B with an S = 5/2 ground state occurs in the chloride-depleted PSII, which may explain the presence of the EPR signal at g = 4.1. Moreover, we use multiconformer continuum electrostatics to study the effect of chloride depletion on the redox potential associated with the S1/S2 and S2/S3 transitions.

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INTRODUCTION The process of water splitting catalyzed by the oxygen-evolving complex (OEC) in photosystem II (PSII) produces the oxygen required for life, in an efficient use of solar power.1,2 The OEC is oxidized by the primary donor chlorophyll P680 in a four-step photochemical cycle called the S-state cycle. The OEC advances through five Sn states during catalysis. The S0 state is the most reduced state, and the S4 state is the most oxidized state of the OEC in the catalytic cycle.3 The OEC contains four manganese ions and one calcium ion connected through μ-oxo bridges. The metal ions are coordinated by several amino acids in the D1 and the CP43 subunits. In addition, there are chloride ions in the second coordination shell identified by X-ray diffraction and serial Xray crystallographic techniques.4,5 The role of chloride ion in water oxidization in PSII is still under investigation. While the S2 state can be formed without Cl−, depletion of chloride blocks the transition from the S2 to S3 catalytic states, thereby shutting down water oxidation at the OEC.6−8 Chloride has also been proposed to regulate the redox potential of the OEC.9 X-ray structures of PSII have shown that the chlorides and the amino acid residues near the OEC participate in the same hydrogen-bonding network, which is thought to form the network for proton transfer from the OEC to the lumen.10−12 The effect of chloride depletion on the structure and spin state of the OEC has been characterized primarily by using continuous-wave electron paramagnetic resonance (EPR) spectroscopy. Although the dark-stable state of the OEC, the © 2016 American Chemical Society

S1 state, is EPR-silent in perpendicular mode EPR spectroscopy, the S2 state is EPR-active. In the presence of chloride, a g = 2 multiline signal characteristic of the spin-coupled manganese ions is observed in the S2 state. However, upon depletion of chloride, a different g = 4.1 signal is observed.13 When chloride is replenished, the g = 2 S2 signal reappears in lieu of the g = 4.1 signal.14 When other monovalent anions such as iodide replace chloride in PSII, a similar shift in equilibrium toward the g = 4.1 form is observed.15−18 The g = 2 and g = 4.1 signals arise from two different spin isomers in the S2 state of the OEC. The g = 2 signal arises from the S = 1/2 ground state, and the g = 4.1 signal arises from the S = 5/2 ground state.19 Although the generation of the g = 4.1 EPR signal in native PSII is possible by other techniques,19 in this work we will only discuss the g = 4.1 EPR signal induced by chloride depletion. Computational studies have further shown that the identity of the manganese ion oxidized in the S1 to S2 transition leads to two different S2 states.20 Although chloride is not a ligand to any manganese ions in the OEC, the change in equilibrium favoring the S = 5/2 isomer upon chloride depletion provides a handle to probe the mechanism by which chloride depletion affects the structure and spin state of the OEC in the S2 state. Molecular dynamics (MD) and Monte Carlo (MC) simulations suggested that chloride depletion induces the formation of a salt bridge between D1-D61 and D2-K317, Received: April 7, 2016 Revised: April 12, 2016 Published: April 14, 2016 4243

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Figure 1. Energetics of S2 state configurations A and B with and without chloride. To the left, the oxidation of Mn4 is favored by 10.4 kcal/mol in the native state. To the right, chloride is depleted and oxidation of Mn1 is favored by 13 kcal/mol. The higher energy structures are placed on the top. The red sticks represent oxygen atoms, with magenta spheres for Mn (light blue: carbon; dark blue: nitrogen; white: hydrogen). All amino acids in the model (see Methods section) and water molecules except the Mn4-bound water W1 are removed for clarity.

two configurations were calculated using the Ising Hamiltonian. The full spectrum of the energy levels resulting from the magnetic coupling of the high-spin Mn centers was obtained by constructing the Heisenberg−van Vleck Hamiltonian and diagonalizing the corresponding matrix.24 The ground states of A and B have total spins of S = 1/2 and S = 5/2, respectively. The energy of A is 10.4 kcal/mol lower than B. However, it should be kept in mind that approximations made in the calculations such as the neglect of finite temperature effects, dynamics, and the protein environment further apart from the OEC also influence the energetics as well as the choice of computational parameters such as the exchange-correlation density functional. The optimized structures for A and B show that the Mn4−Cl and D2-K317−Cl distances decreased, while the D2-K317− D61 distance increased compared to the starting X-ray structure (Table 1). However, because Mn4 has an incomplete coordination shell in B, it is not attached to the Mn3O4Ca2+

which blocks the proton-exit channel and inhibits the redox leveling required to advance through the catalytic cycle.21 In addition, D61 plays an important role in forming the g = 2 S2 state by abstracting a proton from water 1 (W1, see Figure 1) when Mn4 is oxidized. This proton binding is the reason that the S1 to S2 transition is significantly less pH dependent than the other S state transitions.22 In this paper, we studied the energetics of two isoelectronic S2-state configurations of the Mn4CaO5 cluster: configuration A Mn(III, IV3) with Mn13+ and B Mn(IV3, III) (Figure 1) with Mn43+. Density functional theory (DFT) was used to compute the energetics of configurations A and B with and without chloride. The computed energetics of configurations A and B in the presence and absence of chloride can provide further understanding regarding the change in the S2 state EPR signal of the OEC upon chloride depletion. In addition, we used multiconformer continuum electrostatics (MCCE)23 to calculate the redox potential Em for the S1/S2 and S2/S3 transitions in chloridedepleted complete PSII with the terminal waters not allowed to lose protons to D1-D61 or to the solution.

Table 1. Optimized Bond Lengths for Different Configurations with and without Chloride in the S2 Statea

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RESULTS AND DISCUSSION Chloride depletion is known to block the S2/S3 transition. MD and MC simulations suggest that chloride depletion induces the formation of a salt bridge between D1-D61 and D2-K317, hindering the ability of D1-D61 to abstract protons from the OEC.21 Here we use DFT to study the energetics of the OEC with and without chloride for the A and B configurations. In addition, we calculate the exchange coupling constants to identify the actual spin of the ground state for all configurations and compare them with the EPR measurements. Then, we use a classical model to study the effect of chloride depletion on the redox leveling of the OEC in PSII. Configurations A and B in Native State. The geometries of A and B were optimized in the high spin state with total spin multiplicity of 14, and the exchange coupling constants for the

Cl− removed

native Mn1−Mn2 Mn2−Mn3 Mn1−Mn3 Mn4−Mn3 Mn1−O5 M4−O5 Mn4−Cl D61−K317 Cl−K317

X-ray

A

B

A

B

2.67 2.70 3.24 2.86 2.70 2.32 6.59 4.17 3.28

2.80 2.78 3.39 2.72 3.06 1.89 4.42 5.11 3.13

2.74 2.76 2.86 3.07 1.85 3.03 4.36 5.15 3.19

2.77 2.75 3.40 2.73 3.38 1.80

2.74 2.76 2.86 3.23 1.85 3.46

2.60

2.59

a

The D61−K317 distance is measured between the nearest oxygen of the carboxylate group of D61 and the nitrogen of K317. All distances are in units of angstroms.

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The Journal of Physical Chemistry B cubane, and the Mn4−Cl distance is shorter. In addition, the oxidation of Mn4 reduces the pKa of W1, which led to deprotonation of W1 during geometry optimization. After this proton transfer from W1 to D61 in A, the distance between Mn4 and the oxygen of W1 is 1.97 Å vs 2.17 Å in B. Chloride Depletion. After removing chloride from the model structures of A and B, we reoptimized these structures and the energy levels were obtained as done in the native state. Model B with a S = 5/2 ground state is lower in electronic energy by 12.5 kcal/mol than model A with a S = 1/2 ground state in the chloride-depleted model. Chloride depletion has been found to be responsible for changing the observed EPR signal from the g = 2 “multiline” signal to the g = 4.1 signal in the S2 state.25 Pantazis and coworkers have proposed that the observation of the S2 state multiline EPR signal is due to the formation of configuration A (Figure 1), while the S2 state g = 4.1 is attributed to the formation of configuration B.20 Thus, our calculations suggest that observation of the g = 4.1 signal upon chloride depletions may result from the formation of configuration B. The optimized structure of both A and B in the chloridedepleted model show the formation of a salt-bridge between D61 and D2-K317 in agreement with our previous MD and MC simulations.21 The Mn−Mn distances reported in Table 1 show a significant change of the Mn1−Mn3 and Mn3−Mn4 distances between A and B. The EXAFS study of the S2 g = 4 state at 130 K by Liang and co-workers indicates that the second shell of the backscatterers from Mn absorber contains peaks at 2.73 and 2.85 Å assigned to the Mn−Mn distances.26 However, the 2.85 Å peak did not appear in a sample containing the S2 multiline signal. These structural changes result from stabilization of configuration B at 130 K. In agreement with previous calculations,20 our calculations suggest that the Mn1−Mn3 distance decreases by 0.5 Å when B is formed (Table 1). Thus, we propose that the 2.85 Å peak corresponds to the Mn1−Mn3 distance of configuration B. The energy difference resulting from the removal of chloride may be attributed to the pKa shift of W1 upon oxidation of Mn4, in addition to the flexibility of Mn4 in B, which can reduce the energy. As shown in previous work on Mn model compounds, the oxidation of Mn(III) causes a pKa shift of a Mn(III)-bound water ligand of ∼10 pH units.27 This shift makes it highly favorable for W1 to transfer its proton to D61 when Mn4 is oxidized in the native protein. However, when chloride is depleted and D61 forms a salt bridge with D2-K317, D61 cannot abstract a proton from W1, which makes A potentially energetically unfavorable. Hydrogen Bond Network and Model Limitations. The DFT study by Pantazis and co-workers using a model that did not include chloride and D2-K317 suggested that A and B are almost isoenergetic.20 Thus, to validate our calculations, we recalculated the energies of A and B after removing chloride and D2-K317 and fixing all the computational parameters (basis sets, exchange-correlation functional, and spin multiplicity). The energy difference reduced from 10.4 to 3.4 kcal/mol when chloride and D2-K317 are removed, which is similar to the obtained results by Pantazis and co-workers. Figure 2 (1) shows a comparison of the XFEL structure (S1 state) and the optimized DFT structure of configuration A (S2 state). In the structure of A, the chloride has moved 2.2 Å toward the Mn4O5Ca2+ cluster and forms a hydrogen bond with W2, which perturbs the ligand environment around Mn4. The

Figure 2. To the left (1) the X-ray structure (PDB code: 4UB6) shown in magenta superimposed on the DFT structure of A shown in orange. To the right (2) the structure of A is overlaid on the structure of A− (optimized without including Cl− and D2-K317). The two structures almost identical except for the proton position of W2 due to the hydrogen bond formed with Cl−.

orientations of the hydrogen atoms of W2 are shown for A and A− (A optimized without chloride and D2-K317) in Figure 2 (2) and the distances to Mn4 are reported in Table S1. The hydrogen atoms of W2 in A are pointing further from Mn4, which is energetically favorable due to the electrostatic repulsion. Although B− experiences similar electrostatic repulsion, the effect of this repulsion is less because Mn4 is in the Mn(III) oxidation state. Thus, we suggest that A is more favorable due to the electrostatic interactions between Mn4 and W2, in addition to Mn4 and chloride. As the OEC advances in the S-state cycle and accumulates positive charges, the chloride is expected to move toward the cluster due to the electrostatic interactions. However, there are not enough waters in the crystallographic model around the chloride, which may impose constraints on the chloride movements. In addition, some other structural elements may impose more constraints on the chloride movement. To account for these constraints, the backbone of Glu333, Asn181, Leu321, and Val185 should be added to the model. Thus, this issue needs to be investigated further by combining molecular dynamics simulation and DFT to understand the interaction between the chloride and the coordination shell of Mn4. Nevertheless, the inclusion of chloride in the DFT model is important when studying the energetics of the different configurations of the OEC, especially in the advanced S states. To check the validity of our conclusions against A− and B−, D61 was removed from the model to block the OEC from releasing a proton from W1, and the two structures were reoptimized. Instead of being isoenergetic, the energy of B− is lower by 15.2 kcal/mol than A−, when D61 is removed. This suggests that the inability of the OEC to release a proton to D61 in the S2 state is responsible for changing the spin configuration of the ground state of the Mn4O5Ca2+ cluster, which is consistent with the results obtained from the larger model, where D61 formed a salt bridge with D2-K317. Calculations of Reduction Potentials. MCCE is used to calculate the reduction potential of the S1/S2 and S2/S3 transitions of chloride-depleted PSII, where the salt bridge is formed between D61 and D2-K317. The calculations include all protein subunits and amino acids. Because chloride depletion blocks the proton exit channel gated by D61, the OEC is not allowed to lose protons from the terminal waters through the titration. However, the protein may freely respond to the change in the OEC charge in the S-state transitions. The 4245

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calculated values are compared with the values reported for native PSII.22 In the native PSII, Mn4 is oxidized in the S1/S2 transition at 0.70 V (Table 2), and that is coupled to a proton transfer from

S1/S2 S2/S3

chloride-depleted

0.70 V 1.34 V

1.21 V 1.65 V

a The bold values indicate that the Em is for oxidation of Mn4. The values in regular text indicate that the Em is for oxidation of Mn1. The native values are obtained from ref 22.

W1 to D61. However, in the chloride-depleted PSII, D61 is not available for proton abstraction, and W1 cannot lose a proton to the solution, which raises the Em of Mn4. Thus, Mn1 is oxidized instead in this transition at 1.21 V, and a partial proton is lost from H337 and D2-E312. The calculated Em is lower than the reduction potential of P680+ (1.25 V),28 which suggests that the S1/S2 transition is allowed in the chloridedepleted PSII. The reported S2/S3 transition in native PSII is 0.09 V higher than the potential for oxidation of P680. However, this was attributed to the usage of a fixed structure of the S1 state through the simulation. Furthermore, this Em is reduced to 0.9 V when the structure of S3 is used. For more detailed discussion about the Em calculations see ref 22. Through the catalytic cycle, protons are released to the lumen through a proton channel to balance the accumulated positive charges. The interactions between the D61 and D2K317 are dominated by electrostatic attraction,22 and the mutation of D2-K317 to a neutral residue is not expected to block the proton exit channel gated by D61 when the chloride is depleted. For example, the photochemical reaction in the chloride-depleted PSII can be recovered in the D2-K317A mutant, while chloride is required for the D2-K317R mutant.29 Thus, the redox leveling mechanism is not affected by chloride depletion if D2-K317 is mutated to uncharged residue. Because the redox leveling mechanism is suspended by not allowing the OEC to lose protons through the catalytic cycle, Mn4 is oxidized in the S2/S3 transition at a high Em of 1.65 V, which is ∼0.4 V higher than the reduction potential of P680+. However, the protein responds to the accumulated positive charge on the OEC by losing a partial proton from E65, D2E343, and D2-H61 due to the long-range electrostatic interactions.

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METHODS

Preparation of the OEC Structure. The calculations start with the 1.95 Å structure of PSII (PDB ID 4UB6)5 obtained by serial femtosecond crystallography to minimize radiation damage. The Mn4O5Ca2+ cluster (Figure 1) is optimized with DFT using the B3LYP density functional30 in Gaussian09.31 The LANL2DZ basis sets with effective core potentials are used for Mn and Ca,32 while 6-31G* is used for the other atoms.33 The model includes the four terminal waters bound to Mn4 and to Ca2+, the side chains of the amino acid ligands to each Mn (D170, E189, H332, E333, D342, A344, and CP43-E354), and the side chains hydrogen bonded to the bridging and terminal oxygens (D61, H337, and CP43-R357). In addition, H190, Y161, chloride, and D2-K317 and 11 crystallographic waters are included in the model (Figure 3). The model includes 227 atoms.

Table 2. Calculated Em Values for the S1/S2 and S2/S3 Transitionsa native

Article

Figure 3. Mn4CaO5 cluster and the amino acids included in the DFT model. Manganese atoms are shown in magenta and labeled as in the crystal structure, oxygen atoms in red, chloride in green, and the calcium atom in green.

The geometry was optimized in the S2 state in the high spin state for two possible configurations: A Mn(III,IV3) where Mn4 is oxidized and B Mn(IV3,III) where Mn1 is oxidized. The backbone atoms are held fixed through the optimization, while the side chains are allowed to relax freely. A and B were reoptimized after removing the chloride and starting from the MD structure in reference 21, keeping all the computational parameters fixed to study the effect of chloride depletion. Starting from the optimized high-spin structures, seven broken symmetry energies were obtained and exchange coupling constants were calculated as explained in refs 24 and 34. Then the Heisenberg−Dirac−van Vleck Hamiltonian matrix is constructed and diagonalized to obtain the full spectrum of the magnetic levels resulting from the spin coupling between the Mn centers.24 MCCE (Multiconformer Continuum Electrostatics) Calculations. MCCE generates a Boltzmann distribution of redox and protonation states of the OEC and protonation and conformations states of the surrounding amino acid side chains. The electrostatic interactions in PSII needed for the Monte Carlo sampling were calculated using DELPHI.35 The

CONCLUSIONS

Simulations in combination with experimental data suggest that the inability of the OEC to transfer a proton to D61 in the S1/ S2 transition in the chloride-depleted PSII causes a change in Mn oxidation states in S2 state. In addition, although the OEC cannot lose protons through the catalytic cycle, the S1/S2 transition is still allowed, as the calculated Em is lower than the reduction potential of P680+. However, the calculated Em of the S2/S3 transition is 1.65 V and the OEC cannot be oxidized by P680+, which suggests that the OEC cannot advance beyond the S2 state. 4246

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Residues and Hydrogen-Bonding Networks. Curr. Opin. Chem. Biol. 2015, 25, 152−8. (13) vanVliet, P.; Rutherford, A. W. Properties of the ChlorideDepleted Oxygen-Evolving Complex of Photosystem II Studied by Electron Paramagnetic Resonance. Biochemistry 1996, 35, 1829−1839. (14) Ono, T.; Zimmerman, J. L.; Inoue, Y.; Rutherford, A. W. EPR Evidence for a Modified S-State Transition in Chloride-Depleted Photosystem II. Biochim. Biophys. Acta, Bioenerg. 1986, 851, 193−201. (15) Ono, T.; Nakayama, H.; Gleiter, H.; Inoue, Y.; Kawamori, A. Modification of the Properties of S2 State in Photosynthetic OxygenEvolving Center by Replacement of Chloride with Other Anions. Arch. Biochem. Biophys. 1987, 256, 618−24. (16) Szalai, V. A.; Brudvig, G. W. Formation and Decay of the S3 EPR Signal Species in Acetate-Inhibited Photosystem II. Biochemistry 1996, 35, 1946−53. (17) Boussac, A.; Ishida, N.; Sugiura, M.; Rappaport, F. Probing the Role of Chloride in Photosystem II from Thermosynechococcus elongatus by Exchanging Chloride for Iodide. Biochim. Biophys. Acta, Bioenerg. 2012, 1817, 802−10. (18) Pokhrel, R.; Brudvig, G. W. Oxygen-Evolving Complex of Photosystem II: Correlating Structure with Spectroscopy. Phys. Chem. Chem. Phys. 2014, 16, 11812−21. (19) Haddy, A.; Lakshmi, K. V.; Brudvig, G. W.; Frank, H. A. Q-Band EPR of the S2 State of Photosystem II Confirms an S = 5/2 Origin of the X-Band g = 4.1 Signal. Biophys. J. 2004, 87, 2885−96. (20) Pantazis, D. A.; Ames, W.; Cox, N.; Lubitz, W.; Neese, F. Two Interconvertible Structures That Explain the Spectroscopic Properties of the Oxygen-Evolving Complex of Photosystem II in the S2 State. Angew. Chem., Int. Ed. 2012, 51, 9935−40. (21) Rivalta, I.; et al. Structural-Functional Role of Chloride in Photosystem II. Biochemistry 2011, 50, 6312−5. (22) Amin, M.; Vogt, L.; Szejgis, W.; Vassiliev, S.; Brudvig, G. W.; Bruce, D.; Gunner, M. R. Proton-Coupled Electron Transfer During the S-State Transitions of the Oxygen-Evolving Complex of Photosystem II. J. Phys. Chem. B 2015, 119, 7366−77. (23) Song, Y.; Mao, J.; Gunner, M. R. MCCE2: Improving Protein Pka Calculations with Extensive Side Chain Rotamer Sampling. J. Comput. Chem. 2009, 30, 2231−47. (24) Pantazis, D. A.; Orio, M.; Petrenko, T.; Zein, S.; Bill, E.; Lubitz, W.; Messinger, J.; Neese, F. A New Quantum Chemical Approach to the Magnetic Properties of Oligonuclear Transition-Metal Complexes: Application to a Model for the Tetranuclear Manganese Cluster of Photosystem II. Chem. - Eur. J. 2009, 15, 5108−5123. (25) Ono, T.; Zimmermann, J. L.; Inoue, Y.; Rutherford, A. W. EPR Evidence for a Modified S-State Transition in Chloride-Depleted Photosystem II. Biochim. Biophys. Acta, Bioenerg. 1986, 851, 193−201. (26) Liang, W.; Latimer, M. J.; Dau, H.; Roelofs, T. A.; Yachandra, V. K.; Sauer, K.; Klein, M. P. Correlation between Structure and Magnetic Spin State of the Manganese Cluster in the Oxygen-Evolving Complex of Photosystem II in the S2 State: Determination by X-Ray Absorption Spectroscopy. Biochemistry 1994, 33, 4923−32. (27) Amin, M.; Vogt, L.; Vassiliev, S.; Rivalta, I.; Sultan, M. M.; Bruce, D.; Brudvig, G. W.; Batista, V. S.; Gunner, M. R. Electrostatic Effects on Proton Coupled Electron Transfer in Oxomanganese Complexes Inspired by the Oxygen-Evolving Complex of Photosystem II. J. Phys. Chem. B 2013, 117, 6217−6226. (28) Rappaport, F.; Guergova-Kuras, M.; Nixon, P. J.; Diner, B. A.; Lavergne, J. Kinetics and Pathways of Charge Recombination in Photosystem II. Biochemistry 2002, 41, 8518−27. (29) Pokhrel, R.; Service, R. J.; Debus, R. J.; Brudvig, G. W. Mutation of Lysine 317 in the D2 Subunit of Photosystem II Alters Chloride Binding and Proton Transport. Biochemistry 2013, 52, 4758−73. (30) Becke, A. D. Density-Functional Thermochemistry 0.3. The Role of Exact Exchange. J. Chem. Phys. 1993, 98, 5648−5652. (31) Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; et al. Gaussian 09, Revision A.1, 2009.

calculations include all protein subunits and cofactors. A detailed description of the methods can be found in ref 22.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcb.6b03545. Mn4−water distances (Table S1); structures of A and B and the J coupling constants for all the states (A and B with and without chloride) (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail [email protected]; phone 732-646-5986 (M.A.). Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Dr. Sandra Luber, Dr. Marilyn Gunner, and Dr. Dimitrios A. Pantazis for helpful discussions. We acknowledge financial support from the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences, U.S. Department of Energy (DE-SC0001423). Biochemical work was supported by the Department of Energy, Office of Basic Energy Sciences, Division of Chemical Sciences (Grant DEFG02-05ER15646 to G.W.B.).

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