Better than platinum? Fuel cells energized by enzymes
Dihydrogen (H2) gas has the potential to be a limitless source of clean energy if simple and efficient methods of production and utilization can be developed. In that regard, using H2 to store electrical energy by means of an electrochemical cell and returning that energy by means of a fuel cell would be among the cleanest and most efficient energy methodologies. This electrochemical apparatus needs to employ robust catalysts for proton reduction and dihydrogen oxidation. In a nonbiological setting, these processes are most readily accomplished at a platinum electrode. Unfortunately, platinum is resource-limited, expensive, and irreversibly inactivated by common trace impurities in H2 gas, such as H2S and CO.
Nature Uses Nickel, Iron, and Sulfur for H2 Production/Activation
In a biological setting, proton reduction and dihydrogen oxidation is most readily accomplished by the sulfur-bridged di-iron and nickel-iron active sites of the hydrogenase enzymes (Fig. 1) (1-8). Almost immediately after their discovery, the prospect of replacing expensive noble metal catalysts by these base metal-containing enzymes was recognized (9). The [FeFe] hydrogenase enzyme from Megasphaera elsdenii has been shown to catalyze proton reduction at pH 7 with overpotentials (10) and catalytic efficiencies (11) that rival platinum electrodes. Armstrong and coworkers (12) recently showed that the [NiFe] hydrogenase enzyme from Allochromatium vinosum, when absorbed onto a graphite electrode, functions as well as platinum for catalytic H2 oxidation (12).
Consensus structures of the active sites of the [NiFe] hydrogenase enzymes derived from D. gigas, Desulfovibrio vulgaris Miyazaki, Desulfovibrio fructosovorans, Desulfovibrio desulfuricans, and Desulfomicrobium baculatum and [FeFe] hydrogenase enzymes derived from D. desulfuricans Hildenborough and Clostridium pasteurianum I. The nature of (L) depends on a number of factors, including the oxidation states of the metal centers, the crystallization conditions, and addition of CO or O2. The nature of X could not be determined from the x-ray diffraction studies.
An attractive feature of these hydrogenase enzyme-modified electrodes as compared with platinum electrodes is that, when exposed to CO, the former quickly regain catalytic activity once the CO gas is removed. On the other hand, the hydrogenase enzymes that have been isolated are derived primarily from strictly anaerobic organisms (obligate anaerobes) and are extremely sensitive to dioxygen, which is a major drawback for their use as electrode materials. For both the [NiFe] and [FeFe] hydrogenase enzymes, dioxygen reacts with the enzyme active site to generate an “overoxidized,” catalytically inactive form of the enzyme, which does not immediately regain catalytic activity once the O2 gas is removed (13). The reactivation of most O2-inactivated [NiFe] and [FeFe] hydrogenase enzymes is a complex and protracted process.
Overcoming the O2 Sensitivity of Hydrogenase Enzymes
The work of Vincent et al. (14) in this issue of PNAS demonstrates the design of an enzyme-modified electrode based on a [NiFe] hydrogenase derived from the aerobic bacterium Ralstonia eutropha. This enzyme continues to function as an H2 oxidation catalyst even in the presence of high concentrations of CO and immediately recovers catalytic activity after exposure to high concentrations of O2. As expected from prior work, control experiments found that enzyme-modified electrodes based on [NiFe] hydrogenase enzymes from the anaerobic bacteria A. vinosum and Desulfovibrio gigas were reversibly inhibited by the addition of CO gas, were immediately rendered catalytically inactive after the introduction of small concentrations of O2, and remained inactive for extended periods of time after the removal of O2 gas.
As proof of principle, Vincent et al. (14) construct a simple fuel cell using two different enzyme-modified electrodes. The anode consists of a graphite electrode modified with a [NiFe] hydrogenase enzyme derived from R. eutropha. The cathode consists of a laccase enzyme from Trametes versicolor. (This laccase enzyme catalyzes the four-electron reduction of O2 to yield two molecules of H2O.) Under open-circuit conditions, this system reaches a voltage of ≈1 V, even in the presence of added CO gas.
Myriad hydrogenase enzymes are present throughout biology. Certain of these enzymes, such as R. eutropha, have managed to adapt to allow themselves to operate under ambient levels of O2 and high levels of CO, but the origin of this unusually high CO and O2 tolerance is unclear. Enzymes with similar functions in similar organisms are expected to have analogous active-site structures. Indeed, the infrared spectral data presented by Vincent et al. (14) suggest that the active site of the membrane-bound [NiFe] hydrogenase enzyme from R. eutropha may be similar to the structurally characterized [NiFe] hydrogenase (Fig. 1). Another stated opinion is that the active site is “nonstandard” (3).
The active-site structures of the [NiFe] and [FeFe] hydrogenase that have been published to date have served as blueprints for the design of small-molecule catalysts and snapshots of various forms of these enzymes (15-20). We anxiously await the crystallization and elucidation of the molecular structure of this amazing [NiFe] hydrogenase enzyme with the hope that it will provide a clue to the origin of its remarkable O2 tolerance. Undoubtedly, the structure of this [NiFe] hydrogenase enzyme will provide insight into how CO- and O2-tolerant small-molecule catalysts for proton reduction and dihydrogen oxidation might be designed.
Footnotes
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↵ * To whom correspondence may be addressed. E-mail: hall{at}mail.chem.tamu.edu or marcetta{at}mail.chem.tamu.edu.
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Author contributions: J.W.T., M.B.H., and M.Y.D. wrote the paper.
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Conflict of interest statement: No conflicts declared.
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See companion article on page 16951.
- Copyright © 2005, The National Academy of Sciences
