Nanowire-bacteria hybrids for unassisted solar carbon dioxide fixation to value-added chemicals

Abstract

Direct solar-powered production of value-added chemicals from CO2 and H2O, a process that mimics natural photosynthesis, is of fundamental and practical interest. In natural photosynthesis, CO2 is first reduced to common biochemical building blocks using solar energy, which are subsequently used for the synthesis of the complex mixture of molecular products that form biomass. Here we report an artificial photosynthetic scheme that functions via a similar two-step process by developing a biocompatible light-capturing nanowire array that enables a direct interface with microbial systems. As a proof of principle, we demonstrate that a hybrid semiconductor nanowire-bacteria system can reduce CO2 at neutral pH to a wide array of chemical targets, such as fuels, polymers, and complex pharmaceutical precursors, using only solar energy input. The high-surface-area silicon nanowire array harvests light energy to provide reducing equivalents to the anaerobic bacterium, Sporomusa ovata, for the photoelectrochemical production of 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 resulting acetate (∼6 g/L) can be activated to acetyl coenzyme A (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. As such, interfacing biocompatible solid-state nanodevices with living systems provides a starting point for developing a programmable system of chemical synthesis entirely powered by sunlight.

Keywords: Nanowires; artificial photosynthesis; bacteria; carbon dioxide fixation.

Figure 1. 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; 4) producing value-added chemicals. An integration of materials science and biology, such an approach combines the advantages of solid-state devices with living organisms. b, As a proof of concept, we demonstrate that under mild condition 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.

Figure 2. Unassisted solar-powered acetate production from the nanowire-bacteria hybrid device

a, Cross-sectional SEM image of the three-dimensional network in the nanowire-bacteria hybrid. b & c, Magnified images at different depths of the nanowire array. d, Tafel plots, the logarithmic current density versus applied electrochemical voltage, are plotted for different electrode configurations (n = 2). Detailed data is summarized in Supplementary Fig. 2d. Filled blue circle (“planar, bio”), planar electrode loaded with bacteria; filled yellow circle (“NW, bio”), nanowire electrode loaded with bacteria; open black circle (“planar, abiotic”), bare planar electrode; open red circle (“NW, abiotic”), bare nanowire electrode. e, Measurement of unassisted solar-powered CO₂ reduction for more than five days, n = 6. During the experiment the system was purged with 20% CO₂/80% N₂. In the plot X_acetate is the product selectivity (Faradic efficiency) of acetic acid generation. The scale bars are 5 μm (a) and 1 μm (b & c).

Figure 3. Enhanced oxygen tolerance for nanowire-bacteria hybrids

a, A numerical simulation illustrates that integrating bacteria into a nanowire array allows for the survival of strict anaerobes in an aerobic environment. The oxygen concentration in the electrolyte decreases logarithmically from the nanowire array’s entrance, creating a local anaerobic environment. This is in contrast to the linear decrease of oxygen concentration for a planar electrode (Supplementary Note and Supplementary Fig. 5). b, Experimental demonstration of aerobic CO₂ reduction by S. ovata when Pt was additionally loaded onto the nanowire electrode, n = 3. Constant electrochemical bias (−0.2 V vs. RHE) was applied to the Si nanowire electrode and the current was plotted against time. As highlighted in the plot, the sparging gas of the setup was switched from anaerobic (20% CO₂/80% N₂) to aerobic (21% O₂/10% CO₂/69% N₂) at t = 85 hour.

Figure 4. Biocatalytic production of diverse organic compounds using genetically engineered E. coli

a, Synthetic pathways for the production of a variety of value-added chemicals. Here the names of proteins are listed, and the colors differentiate their genetic origins. In addition to these described pathways, some of the acetyl-CoA are expected to be diverted into the TCA cycle for redox balancing. b, Solar-derived acetic acid from nanowire-bacteria hybrids was used as the feedstock to yield a variety of chemicals in M9-MOPS medium (t = 5 days). No organic substrates were provided except the solar-derived acetic acid, and the acetate-containing medium solution was yielded at aerobic conditions (21% O₂/10% CO₂/69% N₂) under simulated sunlight. Here X_product is acetate-to-product conversion efficiency. n = 3 for all reported values. Blue, Clostridium acetobutylicum; green, Treponema denticola; brown, Ralstonia eutropha; black, E. coli; red, Saccharomyces cerevisiae; light blue, Artemisia annua; purple, Nicotiana tabacum; yellow, Gossypium arboreum. 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 hydroxymethylglutary-CoA reductase; MK, mevalonate kinase; PMK, phosphomevalonate kinase; PMD, phosphomevalonate decarboxylase; IDI, isopentenyl diphosphate-isomerase; IspA, farnesyl diphosphoate synthase; ADS, amorphadiene synthase; EAS, epi-aristolochene cyclase; CAS, cadinene synthase.