“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 CiamicianScience 36, 385 (1912)

“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 CiamicianScience 36, 385 (1912)

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?

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

Global energy flow

Approximately 4 x1021 J of chemical energy stored in photosynthetic biomass per year.

Power is about 125 TW

Is biological energy conversion sufficiently large scale to be relevant?

Solar energy conversionSolar energy conversionBiologicalBiologicalNon-biologicalNon-biological Photoinduced Photoinduced

electron transferelectron transfer photovoltaicsphotovoltaics

emfemf

wire distributionwire distribution

other electricalother electricalworkwork

reaction centersreaction centers(molecular-level(molecular-levelphotovoltaics, emf)photovoltaics, emf)

emfemf pmfpmf

membrane distributionmembrane distributionHH++

Transducers for:• synthesis work• mechanical work• transport work• driving complex non-linear processes

HH++

Halophilic Archaea,Halophilic Archaea,bacterioplanktonbacterioplankton

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.

Bio-inspired catalysts for sustainable large scale energy production and conversion

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

Questions regarding artificial photosynthesis, water oxidation, oxygen reduction and hydrogen production.

Evolution of bio-inspired catalysis includes elements from both sides

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)

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

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 connectingcatalytic site to electrode.

SHEPerfect electrode

0.82 V

O2

water

EMox/Mred

O2

water0.82 V - EoM Eo

M

EO2

water

Low beta “molecular wire” at low bias connecting E to electrodeElectron tunneling 10 pA current

~ O.82 V

Schematic of wiring enzyme with relay or directly to electrode

Methods of wiring redox enzyme to electrode

Katz et al., Angew. Chem. Int. Ed. 43, 3292-3300 (2004)

Wiring with a rotaxane molecular shuttle

Hess et al., J. Am. Chem. Soc. 125, 7156-7157 (2003)

Amine oxidase wired to gold electrode

log ket = 13 - (1.2 - 0.8)(R -3.6)

Calculated optimal electron transfer rates

Dutton and coworkers Nature, 402, 47–52 (1999) Nature, 355, 796–802 (1992)

Parameters for bio-catalyzed O2 reduction at fuel cell cathode

Metallic conductorto RL, current at least 1 A/cm2

2H2O

Cathode

Molecule - metal interface. Molecular wire, redox relay shuttle, conducting polymer, redox hydrogel, or other means of electrically connectingcatalytic site to electrode

O2

4H+

4e-

Catalytic site

Current will depend on:Number of sites/cm2

Turnover number/siteCarrying capacity of interface

Francisco and Allen, 2005

Cu ions at the active site of phenoxazinone synthase, a multicopper oxidase

O2 + 4e- + 4H+ 2H2O2H2O 4H+ + 4e- + O2 ?

~ 1 nm

~2

nm

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 oxidizerSolar driver at AM1.5~ 20 mA/cm2

=1.25x1017 e-/cm2

Turnover appears rate limiting

Carrying capacity of interfaceHow 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)

Consider bio-inspired catalysts for improved fuel cells

Two fuel cells, same cathodic rxn

H2/air fuel cell

2H2 + O2 2H2O

Conversion of electrochemical potential to work meeting human needs with modest efficiency (~ 50%).

Not so good cathode

Mitochondrion as a fuel cell

2NADH + O2 2NAD+ + 2H2O

Conversion of electrochemical potential to biochemical workwith high (> 90%?) efficiency

Good cathode

Voltage Loss Contributions - H2/Air

significant voltage/power-density via FF/DM optimization (mass-tx)

120 mV (20%)

(H2/air (s=2/2) at 150kPa, 80C, and 100%RH - 0.4mgPt-cathode/cm2)

Eloss at 1.5 A/cm2:

400 mV (68%)

major losses due to poor cathode kinetics (ORR)

70 mV (12%)

minor losses by ohmic resistance (50% RH+,membrane, 50% Rcontact)

Source: H. Gastieger, GM Fuel Cell DivisionThanks to Frank DiSalvo

Enzymatic reduction of O2 to H2O

And some questions that come up1) Current density2) V loss to overpotential3) Availability of enzyme4) Assembly on electrode5) Robustness S. C. Barton et al., J. Am. Chem. Soc., 123, 5802 (2001)

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)

Schematic of the overpotential problem

S. C. Barton, et al., Chem. Rev., 104, 4867-4886 (2004)

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.

Example of a small scale biofuel cell using the mitochondrial cathodic reaction

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?

A synthetic active site mimic of iron-only hydrogenase - a bio-inspired anode

Tard et al., (Pickett), Nature, 433, 610 (2005); N&V 433, 589 (2005)

Active site of all-iron hydrogenase

Synthetic analogue

Synthetic analogue shows catalytic H+ reduction on vitreous carbon electrode

Structure of the synthetic active site mimic of iron-only hydrogenase from DFT calculations

Tard et al., (Pickett), Nature, 433, 610 (2005)

H+ reduction on a vitreous carbon electrode at 200 mV more positive than electrode alone.

(Me3P)(OC)2Fe

SSFe(CO)2(CN)

H

H+

(Me3P)(OC)2Fe

SSFe(CO)2(CNH)

H

H+

-H2

(Me3P)(OC)2Fe

SSFe(CO)2(CN)

2e- (-1 V vs NHE)

Mimicking Hydrogenase

Synthetic model of active site of an Fe-only hydrogenase

Thomas B. Rauchfuss, et al., J. Am. Chem. Soc., 2001, 123, 9476

Solar energy conversionSolar energy conversionBiologicalBiologicalNon-biologicalNon-biological Photoinduced Photoinduced

electron transferelectron transfer photovoltaicsphotovoltaics

emfemf

wire distributionwire distribution

other electricalother electricalworkwork

reaction centersreaction centers(molecular-level(molecular-levelphotovoltaics, emf)photovoltaics, emf)

emfemf pmfpmf

membrane distributionmembrane distributionHH++

Transducers for:• synthesis work• mechanical work• transport work• driving complex non-linear processes

HH++

Halophilic Archaea,Halophilic Archaea,bacterioplanktonbacterioplankton

Separate charge

Photosynthetic reaction centers

Energetics and electron transport pathways of PS

QuickTime™ and aTIFF (LZW) decompressor

are needed to see this picture.

QuickTime™ and aTIFF (LZW) decompressor

are needed to see this picture.

QuickTime™ and aTIFF (LZW) decompressor

are needed to see this picture.

Thanks to B Blankenship

N.B.

• 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

Artificial reaction centers

P-A 1P-Ah

1P-A P•+-A•–

A carotenoporphyrin-fullerene triad

N CO

NCH 3

N N

N N

HH

H

Liddell, P. A.; Kuciauskas, D.; Sumida, J. P.; Nash, B.; Nguyen, D.; Moore, A. L.;Moore, T. A.; Gust, D. J. Am. Chem. Soc. 1997, 119, 1400-1405

Light energy stored as electrochemical energy

C -P-C60

•+•-

The best C-P-C60 triads:Yield of charge separated state ~ 100%Stored energy ~1.0 electron voltLifetime = hundreds of ns at room temp. 1 microsecond at 8K

Dipole moment ~160 DSmirnov, 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

D-P-A

D•+-P-A•-

D-P•+-A•-

D-1P-A

0

eV

0.2

0.4

0.6

0.8

1.0

1.2

1.4

1.6

1.8

2.0

Apparently more energy stored herethan at this point in time in reaction centers

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.

Energy levels for artificial reaction centers.

Solar energy conversionSolar energy conversionBiologicalBiologicalNon-biologicalNon-biological Photoinduced Photoinduced

electron transferelectron transfer photovoltaicsphotovoltaics

emfemf

wire distributionwire distribution

other electricalother electricalworkwork

reaction centersreaction centers(molecular-level(molecular-levelphotovoltaics, emf)photovoltaics, emf)

emfemf pmfpmf

membrane distributionmembrane distributionHH++

Transducers for:• synthesis work• mechanical work• transport work• driving complex non-linear processes

HH++

Halophilic Archaea,Halophilic Archaea,bacterioplanktonbacterioplankton

This is what is really needed

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

Contrast of bio-catalysis with human-engineered catalysis. Mainstream energy-transducing redox

processes

Human engineered

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

Biological

Platinum vs. PtBi

PtBi(111) plane

Pt-Pt 2.77 Å (001) plane Pt-Pt 4.32 Å

Pt

Thanks to Frank DiSalvo

Alloys vs. Ordered Intermetallics

(A) (B)

Alloy; e.g. Pt/Ru (1:1) Ordered Intermetallic e.g.

BiPt

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

Metals that can be purchased or can be easily synthesized as alkoxides, ethylhanoates,

MOEEAAs:

 

Sc Ti V Cr Mn Fe Co Ni Cu Zn Ga Ge As Se

Y Zr Nb Mo Ru Rh Pd Ag Cd In Sn Sb Te

La Ta Re Ir Pt Hg Tl Pb Bi

Take home message: synthetic tools to prepare nanoparticles of almost any intermetallic compound are now available

Thanks to Frank DiSalvo

Zou et al., Nature 414, 625-627 (2001)

Photochemical oxidation of water by band gap illumination of a semiconductor

First reported for TiO2 in Nature 238, 37-38 (1972)

Structure of the oxygen evolving complex

Ferreira et al. Science 2004

Britt et al., BBA 1655, 158-171 (2004)

Model of the oxygen evolving complex

Britt et al., BBA 1655, 158-171 (2004)

Model for water oxidation by the OEC

McEvoy and Brudvig PCCP 6, 4754-4763 (2004)

Equal time to the east coast

Mn(V)oxo set up for nucleophilic attack on the electropositive oxygen by nearby water coordinated by Ca++

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.

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).

Can 4 one photon processesCan 4 one photon processesboth oxidize water and reduceboth oxidize water and reduceprotons to Hprotons to H22??

Energetics of water oxidation with HEnergetics of water oxidation with H22 formationformationNHE

– 0.93 NAD+ + e- NAD•

0.92

1.23

NADH •+ + e- NADH

P+ + e- P

P+ + e- P*– 0.67– 0.63 TiO2 ECB(FTO, pH8)

– 0.07 SnO2 ECB(ITO, pH7)

2H+ + 2e- H2

4H+ + 4e- + O2 2H2O0.82

– 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.

Deppenmeier, J Bioenergetics and Biomembranes 36, 55-64 (2004)

CH4 synthesis from H2 + CO2 and methanol

For the oxidative branch (up arrows)4CH3OH 3CH4 + CO2 + 2H2O∆G0 = - 106 kJ/mole CH4

4H2 consumed in reductive branch(down arrows)

Energy input from ion gradient

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.

ConclusionBio-inspired energy-converting processes can by imagined