A new-to-nature photosynthesis system enhances utilization of one-carbon substrates in Escherichia coli.

Photosynthesis harvests solar energy to convert CO into chemicals, offering a potential solution to reduce atmospheric CO. However, integrating photosynthesis into non-photosynthetic microbes to utilize one-carbon substrates is challenging. Here, a photosynthesis system is reconstructed in E. coli, by integrating light and dark reaction to synthesize bioproducts from one-carbon substrates. A light reaction is reconstructed using the photosystem of photosynthetic bacteria, increasing ATP and NADH contents by 337.9% and 383.7%, respectively. A dark reaction is constructed by designing CO fixation pathway to synthesize pyruvate. By assembling the light and dark reaction, a photosynthesis system is established and further programmed by installing an energy adapter, enabling the production of acetone, malate, and α-ketoglutarate, with a negative carbon footprint of -0.84 ~ -0.23 kgCOe/kg product. Furthermore, light-driven one-carbon trophic growth of E. coli is achieved with a doubling time of 19.86 h. This photosynthesis system provides a green and sustainable approach to enhance one-carbon substrates utilization in the future.