Natural photosynthesis, which harvests 130 TW of solar energy to generate up to 115 billion metric tons of biomass annually from the reduction of CO₂, provides motivation for the development of artificial systems that can capture the energy of the sun to convert CO₂ and H₂O to value-added chemicals of societal benefit. However, such an approach has not been fully realized owing to a host of unmet basic scientific challenges. For example, enzymes isolated from microorganisms and plants can selectively catalyze CO₂ reduction with low energy barriers; however, they do not self-repair outside their native cellular context and are often intolerant to oxygen. Consequently, bio-derived CO₂-reducing catalytic systems are not directly applicable to oxygen- containing CO₂ sources such as flue gas.

Another challenge for artificial photosynthesis is the selective synthesis of complex organic molecules. Nature transforms CO₂ into a variety of complex molecules using a limited number of biosynthetic intermediates as building blocks. However, in the case of artificial photosynthesis, the selection of such an intermediate is difficult: ideally, mass transport requires it to be water-soluble, and it should also be easily incorporated into many biosynthetic pathways.

—Liu et al.

The basic concept of the UC Berkeley strategy is to interface biocatalysts in their native cellular environments directly with semiconductor light-absorbers for unassisted solar CO₂ reduction. They envisioned a two-step strategy that mimics natural photosynthesis, in which light capture by a biocompatible nanowire array can interface and directly provide reducing equivalents to living organisms for the targeted synthesis of a variety of value-added chemical products from CO₂ fixation.

Schematics of a general artificial photosynthetic approach. (a) The proposed approach for solar-powered CO2 fixation includes four general components: (1) harvesting solar energy; (2) generating reducing equivalents; (3) reducing CO2 to biosynthetic intermediates; and (4) producing value-added chemicals. Such an approach combines the advantages of solid-state devices with living organisms. (b) As a proof of concept, under mild conditions sunlight can provide the energy to directly treat exhaust gas and generate acetate as the biosynthetic intermediate, which is upgraded into liquid fuels, biopolymers, and pharmaceutical precursors. For improved process yield, S. ovata and E. coli are placed in two separate containers. FPP = farnesyl pyrophosphate. Credit: ACS, Liu et al. Click to enlarge.

This is, the researchers point out, a different approach that of conventional microbial electrosynthesis, in which microbes do not directly interact with light-absorbing devices.

For the proof of principle, they used silicon and titanium dioxide nanowire arrays as the light-capturing units and the anaerobic bacterium Sporomusa ovata as the bio-catalyst. S. ovata can reduce CO₂ under mild conditions and produce acetate. Acetate is a biosynthetic precursor to a variety of value added chemicals—including functionalized aliphatics and aromatics, lipids, alkanes and complex natural products—via acetyl coenzyme A (acetyl-CoA).

The hybrid nanowire array/bacteria system produced acetic acid under aerobic conditions (21% O₂) with low overpotential (η < 200 mV), high Faradaic efficiency (up to 90%), and long-term stability (up to 200 h).

The acetate (∼6 g/L) produced by the nanowire/S. ovata combination was then activated to acetyl-CoA by genetically engineered Escherichia coli and used as a building block for a variety of value-added chemicals, such as n-butanol, polyhydroxybutyrate (PHB) polymer, and three different isoprenoid natural products.

The yield of target molecules was as high as 26% for n-butanol, 25% for one of the isoprenoid compounds (amorphadiene), and up to 52% for PHB biopolymer. Taking into account the 0.38% efficiency from CO₂ to acetic acid, the researchers calculated a solar energy-conversion efficiency of 0.20% from CO₂ to PHB biopolymer.

Synthetic enzymatic pathways for the biosynthesis of target organic compounds. Each product was produced in a different genetically engineered E. coli strain. All pathways begin with acetyl-CoA, which was generated by the activation of solar-derived acetate. In addition to these described pathways, some of the acetyl-CoA are expected to be diverted into the TCA cycle for redox balancing. IPP, isopentenyl pyrophosphate; DMAPP, dimethylallyl pyrophosphate. ACS, acetyl-CoA synthase; phaA, acetoacetyl-CoA thiolase/synthase; hbd, phaB, 3-hydroxybutyryl-CoA dehydrogenase; crt, crotonase; ter, trans-enoyl-CoA reductase; adhE2, bifunctional butyraldehyde and butanol dehydrogenase; phaC, PHA synthase; AtoB, acetyl-CoA acetyltransferase; HMGS, hydroxymethylglutaryl-CoA synthase; tHMGR, truncated hydroxymethylglutaryl-CoA reductase; MK, mevalonate kinase; PMK, phosphomevalonate kinase; PMD, phosphomevalonate decarboxylase; IDI, isopentenyl diphosphate-isomerase; IspA, farnesyl diphosphate synthase; ADS, amorphadiene synthase; EAS, epi-aristolochene cyclase; CAS, cadinene synthase. Credit: ACS, Liu et al., Supporting Information. Click to enlarge.

Overall, the production of different organic products with vastly different synthetic pathways proves the versatility of the integrated approach starting from one common bio-chemical building block, analogous to natural photosynthesis.

The results reported here outline a solar-energy conversion process that combines the strengths of semiconductor nano-devices and bacterium-based biocatalysts. Key advantages of the nanowire-based device are the enhanced oxygen tolerance that allows exhaust gas to be directly fed into the system, thereby enabling use of strict anaerobes with aerobes, as well as the high measured CO₂ fixation activity of the nanowire−bacteria hybrid. Moreover, this modular platform simplifies the overall system design by allowing for the production of a variety of molecular targets, without any setup change in the components for light capture and CO₂ reduction into acetate, by varying only the downstream microorganisms.

—Liu et al.

Resources

• Chong Liu, Joseph J. Gallagher, Kelsey K. Sakimoto, Eva M. Nichols, Christopher J. Chang, Michelle C. Y. Chang, and Peidong Yang (2015) “Nanowire–Bacteria Hybrids for Unassisted Solar Carbon Dioxide Fixation to Value-Added Chemicals” Nano Letters doi: 10.1021/acs.nanolett.5b01254