Important questions

1. “On the arid lands there will spring up industrial colonies without smoke and without smokestacks; forests of glass tubes will extend over the plains and glass buildings will rise everywhere; inside of these will take place the photochemical processes that hitherto have been the guarded secret of the plants, but that will have been mastered by human industry which will know how to make them bear even more abundant fruit than nature, for nature is not in a hurry and mankind is.” Giacomo Ciamician Science36, 385 (1912)

2. Biomimetic approaches and role of biological processes as paradigms for solar to fuel LBNL Workshop “Solar to Fuel - Future Challenges and Solutions” 28-29 March 2005 Important questions Can bio-inspired constructs play a role in large scale solar energy conversion? Provide models for the capture and transformation of solar energy? Or, does the nature of biological energy conversion preclude it serving as a paradigm large scale energy production to meet human needs?

3. Global energy flow Is biological energy conversion sufficiently large scale to be relevant? Approximately 4 x1021 J of chemical energy stored in photosynthetic biomass per year. Power is about 125 TW

4. Solar energy conversion emf pmf Non-biological Biological Photoinduced electron transfer reaction centers (molecular-level photovoltaics, emf) photovoltaics emf membrane distribution H+ H+ wire distribution other electrical work • Transducers for: • synthesis work • mechanical work • transport work • driving complex non-linear • processes Halophilic Archaea, bacterioplankton

5. Bio-inspired catalysts for sustainable large scale energy production and conversion Photosynthetic organisms provide myriad examples of catalysis including several essential redox ones that operate with essentially no overpotential. These include: 2H2O = 4H+ + 4e- + O2 oxygen evolving complex H2 = 2H+ + 2e- hydrogenase O2 + 4H+ + 4e- + 4H+(pumped) = 2H2O + 4H+(pumped) complex 4 With these three enzymes nature has provided the basic paradigms for fuel cell operation and regeneration of hydrogen and oxygen.

6. Questions regarding artificial photosynthesis, water oxidation, oxygen reduction and hydrogen production. Why doesn’t complex 4, cytochrome c oxygen oxido-reductase, operate in reverse? O2 + 4H+ + 4e- + 4H+(pumped) = 2H2O + 4H+(pumped) complex 4 Can the oxygen evolving complex (oec) operate in reverse? 2H2O = 4H+ + 4e- + O2 oec Can the catalytically active sites of redox enzymes be assembled in artificial constructs and electrically coupled to electrodes? Sufficient density of catalytic sites on electrodes to make real-life energy fluxes possible? 1 amp/cm2 See:Basic Research Needs for Hydrogen Production, Storage, and Use. The workshop report is available as a 3 MB pdf file on the BES website:  http://www.sc.doe.gov/bes/hydrogen.pdf

7. Characteristics of biological catalytic activity: slower, molecular recognition near thermodynamic limit efficiency highly specific, molecular recognition robustness through replacement/self repair Characteristics of present day human-engineered catalytic activity: faster sacrifice efficiency for speed (overpotential) less specific robustness inherent (but some easily poisoned) Evolution of bio-inspired catalysis includes elements from both sides

8. But, perhaps the most important characteristic of biological catalysts is that

9. Biological catalyst do not come wired to electrodes Nature does not use metallic conductors and emf in either synthesis or energy-yielding processes (in the sense that human do). A molecule - metal interface must be made. Molecular wire, redox relay shuttle, conducting polymer, redox hydrogel, or other means of electrically connecting catalytic site to electrode.

10. O2 O2 water water Schematic of wiring enzyme with relay or directly to electrode Mox/Mred E 0.82 V - EoM EoM O2 water 0.82 V Perfect electrode SHE ~ O.82 V E Low beta “molecular wire” at low bias connecting E to electrode Electron tunneling 10 pA current

11. Methods of wiring redox enzyme to electrode

12. Wiring with a rotaxane molecular shuttle Katz et al., Angew. Chem. Int. Ed. 43, 3292-3300 (2004)

13. Amine oxidase wired to gold electrode Hess et al., J. Am. Chem. Soc. 125, 7156-7157 (2003)

14. Calculated optimal electron transfer rates log ket = 13 - (1.2 - 0.8r)(R -3.6) Dutton and coworkers Nature,402, 47–52 (1999) Nature, 355, 796–802 (1992)

15. Parameters for bio-catalyzed O2 reduction at fuel cell cathode Catalytic site 4H+ O2 2H2O Molecule - metal interface. Molecular wire, redox relay shuttle, conducting polymer, redox hydrogel, or other means of electrically connecting catalytic site to electrode 4e- Cathode Metallic conductor to RL, current at least 1 A/cm2 Current will depend on: Number of sites/cm2 Turnover number/site Carrying capacity of interface

16. Cu ions at the active site of phenoxazinone synthase, a multicopper oxidase Max footprint ~ 9 nm2 (suppose 3x3nm squares) ~1x1013 sites/cm2 102 s-1 turnover? (what limits turnover?) 1x1015 turnovers/cm2/s 4x1015 electrons/s cm2/s (4 e-/turnover) About 700 µA/cm2 As water oxidizer Solar driver at AM1.5 ~ 20 mA/cm2 =1.25x1017 e-/cm2 Turnover appears rate limiting O2 + 4e- + 4H+ 2H2O 2H2O  4H+ + 4e- + O2 ? ~ 1 nm ~2 nm Francisco and Allen, 2005

17. Carrying capacity of interface How much current can be pushed through a “molecular wire” In single molecule conducting AFM studies of conducting polymers and molecules with low Beta, currents of about 10 pA are observed at low bias. 10 pA corresponds to ~ 6x107 e-s-1 This easily exceeds by orders of magnitude the turnover number of any enzymes under consideration. Therefore, kcat limits current. J. Am. Chem. Soc. 127,11384-1385 (2005)

18. Consider bio-inspired catalysts for improved fuel cells

19. Two fuel cells, same cathodic rxn Mitochondrion as a fuel cell 2NADH + O2 2NAD+ + 2H2O Conversion of electrochemical potential to biochemical work with high (> 90%?) efficiency Good cathode H2/air fuel cell 2H2 + O2 2H2O Conversion of electrochemical potential to work meeting human needs with modest efficiency (~ 50%). Not so good cathode

20. Eloss at 1.5 A/cm2: 400 mV (68%) 70 mV (12%) 120 mV (20%) major losses due to poor cathode kinetics (ORR)  minor losses by ohmic resistance (50% RH+,membrane, 50% Rcontact)  significant voltage/power-density via FF/DM optimization (mass-tx) Voltage Loss Contributions - H2/Air (H2/air (s=2/2) at 150kPa, 80C, and 100%RH - 0.4mgPt-cathode/cm2) Thanks to Frank DiSalvo Source: H. Gastieger, GM Fuel Cell Division

21. Enzymatic reduction of O2 to H2O And some questions that come up 1) Current density 2) V loss to overpotential 3) Availability of enzyme 4) Assembly on electrode 5) Robustness S. C. Barton et al., J. Am. Chem. Soc., 123, 5802 (2001)

22. Proposed mechanism for O2 reduction by a multicopper oxidase There is a lot of chemistry going on here - no wonder it is slow S. C. Barton, et al.,Chem. Rev., 104, 4867-4886 (2004)

23. Schematic of the overpotential problem S. C. Barton, et al.,Chem. Rev., 104, 4867-4886 (2004)

24. Example of a small scale biofuel cell using the mitochondrial cathodic reaction Examples of small (energy) scale devices using biocatalysis include Adam Heller’s glucose sensor. Many examples in literature of working systems. Very small scale - µW - power production.

25. A fuel cell anode without Pt? Less complicated chemistry and Pt works well, but, it there enough of it? Can the H2/H+ reaction be catalyzed by Fe?

26. A synthetic active site mimic of iron-only hydrogenase - a bio-inspired anode Active site of all-iron hydrogenase Synthetic analogue Synthetic analogue shows catalytic H+ reduction on vitreous carbon electrode Tard et al., (Pickett), Nature, 433, 610 (2005); N&V 433, 589 (2005)

27. Structure of the synthetic active site mimic of iron-only hydrogenase from DFT calculations H+ reduction on a vitreous carbon electrode at 200 mV more positive than electrode alone. Tard et al., (Pickett), Nature, 433, 610 (2005)

28. Mimicking Hydrogenase Synthetic model of active site of an Fe-only hydrogenase Thomas B. Rauchfuss, et al., J. Am. Chem. Soc., 2001, 123, 9476

29. Solar energy conversion emf pmf Non-biological Biological Photoinduced electron transfer reaction centers (molecular-level photovoltaics, emf) photovoltaics emf Separate charge membrane distribution H+ H+ wire distribution other electrical work • Transducers for: • synthesis work • mechanical work • transport work • driving complex non-linear • processes Halophilic Archaea, bacterioplankton

31. Photosynthetic reaction centers

32. Energetics and electron transport pathways of PS N.B. Thanks to B Blankenship

33. Artificial reaction centers • Basis is photoinduced electron transfer • Minimum requirements • Donor chromophore (P) • Suitable electron acceptor (A) • Electronic coupling • Useful systems require more complexity -Secondary donor or acceptor hn P-A 1P-A 1P-A P•+-A•–

34. A carotenoporphyrin-fullerene triad

35. Light energy stored as electrochemical energy Dipole moment ~160 D Smirnov, S. N.; Liddell, P. A.; Vlassiouk, I. V.; Teslja, A.; Kuciauskas,D.; Braun,C. L.; Moore, A. L.; Moore, T. A.; and Gust, D. J. Phys. Chem. A, 2003, 107, 7567-7573 The best C-P-C60 triads: Yield of charge separated state ~ 100% Stored energy ~1.0 electron volt Lifetime = hundreds of ns at room temp. 1 microsecond at 8K C  -P-C60 •+ •-

36. Energy levels for artificial reaction centers. e V 2 . 0 1 D - P - A 1 . 8 1 . 6 • + • - D - P - A 1 . 4 • + • - D - P - A 1 . 2 1 . 0 0 . 8 0 . 6 0 . 4 0 . 2 D - P - A Nature views D.+-P-A.- as redox potential, not as a source of emf. Subsequent energy conserving processes are based on redox chemsitry. Nature does not use emf to drive synthesis. Apparently more energy stored here than at this point in time in reaction centers 0

37. Solar energy conversion emf pmf Non-biological Biological Photoinduced electron transfer reaction centers (molecular-level photovoltaics, emf) photovoltaics emf membrane distribution This is what is really needed H+ H+ wire distribution other electrical work • Transducers for: • synthesis work • mechanical work • transport work • driving complex non-linear • processes Halophilic Archaea, bacterioplankton

38. Contrast of bio-catalysis with human-engineered catalysis. Mainstream energy-transducing redox processes Biological Human engineered Living organisms use FeS centers, Fe, Cu, Mn and sometimes Ni Catalysis often involves covalent intermediates with catalytic sites having distinct 3-dimensional architecture. A necessary feature of enzymatic catalytic mechanisms for lowering G‡ C-C bond cleavage facile. Pathways to synthesize meOH, etOH, CH4 from CO2 Carbon, Pt with alloys and intermetalic compounds, efforts span periodic table Emphasis on surface structure. No good catalysts for C-C bond cleavage in context of low temp fuel cell Demonstrated using enzymes in small scale systems

39. PtBi Platinum vs. PtBi Pt (111) plane Pt-Pt 2.77 Å (001) plane Pt-Pt 4.32 Å Thanks to Frank DiSalvo

40. Ordered Intermetallic e.g. BiPt Alloy; e.g. Pt/Ru (1:1) (A) (B) Alloys vs. Ordered Intermetallics 2 “Electrocatalytic Oxidation of Formic Acid at an Ordered Intermetallic PtBi Surface”, E. Casado-Rivera, Z. Gál, A.C.D. Angelo, C. Lind, F.J. DiSalvo, and H.D. Abruña, Chem. Phys. Chem.4, 193-199 (2003) Thanks to Frank DiSalvo

41. Metals that can be purchased or can be easily synthesized as alkoxides, ethylhanoates, MOEEAAs: ScTi VCr Mn Fe Co Ni Cu Zn GaGe As Se Y ZrNbMoRuRh Pd Ag Cd In Sn Sb Te La Ta Re IrPt Hg Tl Pb Bi Take home message: synthetic tools to prepare nanoparticles of almost any intermetallic compound are now available Thanks to Frank DiSalvo

42. Photochemical oxidation of water by band gap illumination of a semiconductor First reported for TiO2 in Nature238, 37-38 (1972) Zou et al., Nature414, 625-627 (2001)

43. Structure of the oxygen evolving complex Ferreira et al. Science 2004

44. Model of the oxygen evolving complex Britt et al., BBA1655, 158-171 (2004)

45. Model for water oxidation by the OEC Britt et al., BBA1655, 158-171 (2004)

46. Equal time to the east coast Mn(V)oxo set up for nucleophilic attack on the electropositive oxygen by nearby water coordinated by Ca++ McEvoy and Brudvig PCCP6, 4754-4763 (2004)

47. Electrolysis of water - anode side Using Si PV cells, 3 in series are necessary to provide the voltage to overcome the overpotential associated with removing electrons from water using available catalysts. Commercial electrolyzers operate at 1.7-1.9 V. In PSII electrons are smoothly removed from water with an oxidant of about 1 V (vs. NHE). Key Question: Can the natural water oxidation system (PSII OEC), which oxidizes water at near the thermodynamic potential, be forced to run faster? OEC never wired to an electrode or driven electrochemically. At 1A/cm2, and an area of 100 nm2 per site (arbitrary), each site would need a turnover of 6x106 s-1. In nature the turnover number is about 1X103 s-1. Possibilities: rough surface, but factor of 102 at most. improve catalytic turnover by factors of 103 to 106??? Hard to imagine given what is known about the chemical steps in the mechanism.

48. NHE – 0.93 NAD+ + e- NAD• P+ + e-P* – 0.67 – 0.63 TiO2 ECB(FTO, pH8) SnO2 ECB(ITO, pH7) – 0.07 0.92 NADH •+ + e- NADH P+ + e-P 1.23 Energetics of water oxidation with H2 formation Can 4 one photon processes both oxidize water and reduce protons to H2? 2H+ + 2e- H2 – 0.42 Well, could be. The reducing side works. In photosynthesis the OEC smoothly oxidizes water to O2 by removing 4 e- using an oxidant that is only ~1 V. 4H+ + 4e- + O22H2O 0.82

49. CH4 synthesis from H2 + CO2 and methanol Energy input from ion gradient For the oxidative branch (up arrows) 4CH3OH  3CH4 + CO2 + 2H2O ∆G0 = - 106 kJ/mole CH4 4H2 consumed in reductive branch (down arrows) Deppenmeier, J Bioenergetics and Biomembranes 36, 55-64 (2004)

50. Conclusion Bio-inspired energy-converting processes can by imagined The milk cow model: Engineer organism to express excess designer enzymes that can be harvested for human use. These would be renewable biocatalyst (even the natural system fails every 10 minutes). Must think in terms of land area for both TW of solar and land area to grow the bacteria, algae and plants to provide the enzymes. Can the active site of key enzymes be mimicked and be made robust? Can the mainstream redox enzymes be driven backwards? Engineer ones that can. Wiring to active site is not rate limiting and tunneling is not hard on the molecules. Main stream 1 A/cm2 chemistry to electricity is hard . Depends on what is discovered for turnover rates when one “substrate” is a metallic source of either electrons or holes. Enzymes not designed by Nature to react with metallic conductors. Can turnover rate be increased? Engineering biocatalysts for better performance. 3-dimensional binding sites likely fundamentally slower than reactions at surfaces. High level of organization required for processes that couple redox to protonmotive force. Do not limit bioinspired constructs to main stream energy processing. Niche applications add up. It is a hard problem.