Renewable-fuels generation has emphasized water splitting to produce hydrogen and oxygen. For accelerated technology adoption, bridging hydrogen to liquid fuels is critical to the translation of solar-driven water splitting to current energy infrastructures. One approach to establishing this connection is to use the hydrogen from water splitting to reduce carbon dioxide to generate liquid fuels via a biocatalyst.

—Torella et al.

Schematic diagram of bioelectrochemical cell. Water oxidation takes place at the cobalt phosphate (CoPi) anode with proton reduction taking place at the nickel molybdenum zinc (NiMoZn) or stainless-steel (SS) cathode. CO2 is continuously sparged into the cell. The wild-type (wt) bacterium Ralstonia eutropha (Re) H16 oxidizes H2 using oxygen-tolerant hydrogenases (H2ase) to generate reduced cofactors (e.g., NADPH) and ATP, and uses these to reduce CO2 to 3-phosphoglycerate (3PG) via the Calvin cycle. 3PG is then converted into biomass in wt ReH16 or may be diverted in metabolically engineered Re2133-pEG12 into isopropanol. Credit: PNAS, Torella et al. Click to enlarge.

In the system, water-splitting catalysis is performed using catalysts that are made of earth-abundant metals and enable low overpotential water splitting. The resulting hydrogen is then fed to R. eutropha. An enzyme takes the hydrogen back to protons and electrons, then combines them with carbon dioxide to replicate—making more cells (i.e., biomass).

Based on discoveries made earlier by Anthony Sinskey, professor of microbiology and of health sciences and technology at MIT, new pathways in the bacterium are metabolically engineered to make isopropanol.

The fully integrated microbial–inorganic system was engineered based on a cobalt phosphate (CoP_i) water-splitting anode, with NiMoZn or stainless-steel (SS) 304 mesh 60 cathodes to generate O₂ and H₂ (41), which in turn was used to fix carbon to biomass in wild-type (wt) Ralstonia eutropha H16 and to isopropanol in an engineered strain of R. eutropha, Re2133-pEG12.

For the former, the team achieved a maximal bioelectrochemical efficiency of 17.8% for biomass; for the latter, a maximal bioelectrochemical efficiency of 3.9% for isopropanol. This bioelectrochemical isopropanol fuel yield (216 mg/L) is the highest yet reported.

The researchers attributed the high efficiencies to the ability to perform water splitting at lower cell voltages owing to the more efficient OER and HER catalysis.

This work lays a foundation for realizing liquid fuel production based on solar water splitting and provides an important and general proof-of-principle demonstration that inorganic and biological materials can be interfaced to achieve solar-to-fuels storage schemes that are not realized by either system in isolation. Moreover, it shows that integrated inorganic–biological hybrid systems may offer yields beyond those available to photosynthetic organisms for the production of fuels.

—Torella et al.

The co-first authors are Joseph Torella, a recent PhD graduate from the HMS Department of Systems Biology, and Christopher Gagliardi, a postdoctoral fellow in the Harvard Department of Chemistry and Chemical Biology.

This is a proof of concept that you can have a way of harvesting solar energy and storing it in the form of a liquid fuel. Dan’s formidable discovery of the catalyst really set this off, and we had a mission of wanting to interface some kinds of organisms with the harvesting of solar energy. It was a perfect match.

—Pamela Silver

Silver and Nocera began collaborating two years ago, shortly after Nocera came to Harvard from MIT. They shared an interest in “personalized energy”—the concept of making energy locally, as opposed to the current centralized system. Local energy would be attractive in the developing world.

The advantage of interfacing the inorganic catalyst with biology is you have an unprecedented platform for chemical synthesis that you don’t have with inorganic catalysts alone. Solar-to-chemical production is the heart of this paper, and so far we’ve been using plants for that, but we are using the unprecedented ability of biology to make lots of compounds.

—Brendan Colón, a graduate student in systems biology in the Silver lab and co-author

The team’s immediate challenge is to increase the bionic leaf’s ability to translate solar energy to biomass by optimizing the catalyst and the bacteria. Their goal is 5% efficiency, compared to nature’s rate of 1% efficiency for photosynthesis to turn sunlight into biomass.

We’re almost at a 1 percent efficiency rate of converting sunlight into isopropanol. There have been 2.6 billion years of evolution, and Pam and I working together a year and a half have already achieved the efficiency of photosynthesis.

—Daniel Nocera

This work was supported by Air Force Office of Scientific Research Grant FA9550-09-1-0689, Office of Naval Research Multidisciplinary University Research Initiative Award N00014-11-1-0725 and a National Science Foundation Graduate Research Fellowship.

Resources

• Joseph P. Torella, Christopher J. Gagliardi, Janice S. Chen, D. Kwabena Bediako, Brendan Colón, Jeffery C. Way, Pamela A. Silver, and Daniel G. Nocera (2015) “Efficient solar-to-fuels production from a hybrid microbial–water-splitting catalyst system” PNAS doi: 10.1073/pnas.1424872112