Global food demand is increasing, but current food production is limited by the low energy conversion efficiency of photosynthesis (~1% or less). Traditional breeding and genetic engineering methods to improve photosynthetic efficiency have shown limited success. Artificial photosynthesis offers a potential solution by circumventing the limitations of biological photosynthesis, such as low solar energy capture and inefficient CO₂ reduction. While previous studies have demonstrated artificial photosynthesis systems producing reduced species like CO, formate, methanol, and H₂, these systems have limitations in supporting the growth of most food-producing organisms. Acetate, a soluble two-carbon substrate, is readily metabolized by a broad range of organisms and can be electrochemically produced. This research aimed to develop a hybrid inorganic-biological system for food production using electrochemically produced acetate as a carbon and energy source, thereby decoupling food production from biological photosynthesis.

Several studies have explored artificial photosynthesis systems for converting CO₂ and H₂O into reduced species. However, these systems often face challenges, including low selectivity for desirable products and the toxicity of intermediate metabolites produced during the biological metabolism of some substrates (formate and methanol). Acetate has emerged as a more promising substrate due to its solubility and widespread metabolic compatibility. Previous research primarily focused on acetate incorporation into specific metabolites, such as lipids. This study expands on this by investigating the utilization of acetate as a primary carbon source for a broader range of organisms, including those used for food production.

The study developed a two-step electrochemical process to convert CO₂ into acetate. The first step uses a silver catalyst to convert CO₂ into CO, and the second step uses a copper catalyst to convert CO into acetate. A 5 M NaOH scrubber was introduced between the two steps to improve acetate selectivity. The resulting effluent, containing acetate and other by-products, was used as a carbon and energy source for various food-producing organisms. Organisms included *Chlamydomonas reinhardtii* (a photosynthetic alga capable of heterotrophic growth), *Saccharomyces cerevisiae* (yeast), several species of mushroom-producing fungi, and nine crop plants (lettuce, rice, cowpea, green pea, canola, tomato, pepper, tobacco, and *Arabidopsis thaliana*). The growth of these organisms was evaluated under different conditions, including in the dark for heterotrophic growth. Heavy isotope ¹³C-acetate was used to track acetate incorporation into the biomass of the crop plants, analyzing the ¹³C enrichment in various metabolites through LC-MS. The energy efficiency of the artificial photosynthesis system, powered by photovoltaics, was compared to biological photosynthesis.

The two-step CO₂ electrolysis system achieved a 57% carbon selectivity towards acetate, the highest reported to date. The system produced effluents with high acetate-to-electrolyte ratios (up to 0.75), sufficient to support the growth of various organisms. *Chlamydomonas reinhardtii* grew successfully in the dark using effluent-derived acetate as the sole carbon and energy source, yielding 0.28 g algae per g acetate. *Saccharomyces cerevisiae* also grew using effluent-derived acetate, achieving comparable growth to glucose-based media. Several species of mushroom-producing fungi were successfully cultivated on a solid substrate using effluent-derived acetate. ¹³C-labeling experiments demonstrated that acetate is incorporated into the biomass of various crops, including lettuce, rice, green pea, jalapeño pepper, canola, tomato, cowpea, tobacco and Arabidopsis, through major metabolic pathways such as the TCA cycle, amino acid biosynthesis, and gluconeogenesis. The analysis showed that the artificial photosynthesis system, powered by photovoltaics, is significantly more energy-efficient than biological photosynthesis. For algae production, the artificial system showed almost a fourfold increase in solar-to-biomass energy conversion efficiency compared to typical crop plants. For yeast production, the efficiency was almost 18 times higher.

The findings demonstrate the feasibility of producing food using a hybrid inorganic-biological artificial photosynthesis system that is independent of biological photosynthesis. The high carbon selectivity and high acetate-to-electrolyte ratios achieved in the electrolyser system are key advancements. The successful cultivation of diverse food-producing organisms, including a photosynthetic alga in the dark, using electrochemically derived acetate highlights the versatility of this approach. The significantly higher energy efficiency compared to traditional biological photosynthesis suggests the potential for this technology to significantly reduce the land and energy footprint of food production. The broad applicability of acetate as a carbon and energy source across various plant species further emphasizes the potential for widespread adoption. This technology may be particularly valuable in situations requiring high energy efficiency and limited space, such as space exploration or controlled-environment agriculture.

This study successfully demonstrates a hybrid inorganic-biological system for food production that surpasses the efficiency of biological photosynthesis. The high acetate selectivity achieved in the two-step electrolyzer system, coupled with the ability to cultivate a diverse range of food-producing organisms using the electrochemically derived acetate, provides a promising pathway for sustainable and efficient food production. Future research could focus on optimizing the electrolysis process, enhancing acetate utilization in plants, exploring other food-producing organisms, and scaling up the system for industrial applications.

While the study demonstrates the potential of the system, several limitations exist. The current system requires relatively high energy inputs for electrolysis, and the cost-effectiveness of this approach needs further investigation. Further optimization is required to improve the tolerance of certain crop plants to higher acetate concentrations, allowing for enhanced biomass production. The long-term effects of the other by-products in the effluent on organism health and food safety need to be studied more thoroughly. The scalability and cost-effectiveness of the technology for widespread use need to be thoroughly explored before large-scale implementation.