Solar‐Driven Methanogenesis through Microbial Ecosystem Engineering on Carbon Nitride

• Published in: Angewandte Chemie 2024-11, Vol.136 (48), p.n/a
• Main Authors: Kalathil, Shafeer, Rahaman, Motiar, Lam, Erwin, Augustin, Teresa L., Greer, Heather F., Reisner, Erwin
• Format: Article
• Language: English
• Subjects: Bioengineering; Biohybrids; Carbon; Carbon dioxide; Carbon nitride; Chemical reactions; Conductive protein filaments; Electron transfer; Electron transport; Filaments; Methanogenesis; Microorganisms; Photosynthesis; Solar fuels; Sustainable production
• ISSN: 0044-8249; 1521-3757
• DOI: 10.1002/ange.202409192

Semi‐biological photosynthesis combines synthetic photosensitizers with microbial catalysts to produce sustainable fuels and chemicals from CO2. However, the inefficient transfer of photoexcited electrons to microbes leads to limited CO2 utilization, restricting the catalytic performance of such biohybrid assemblies. Here, we introduce a biological engineering solution to address the inherently sluggish electron uptake mechanism of a methanogen, Methanosarcina barkeri (M. barkeri), by coculturing it with an electron transport specialist, Geobacter sulfurreducens KN400 (KN400), an adapted strain rich with multiheme c‐type cytochromes (c‐Cyts) and electrically conductive protein filaments (e‐PFs) made of polymerized c‐Cyts with enhanced capacity for extracellular electron transfer (EET). Integration of this M. barkeri‐KN400 co‐culture with a synthetic photosensitizer, carbon nitride, demonstrates that c‐Cyts and e‐PFs, emanating from live KN400, transport photoexcited electrons efficiently from the carbon nitride to M. barkeri for methanogenesis with remarkable long‐term stability and selectivity. The demonstrated cooperative interaction between two microbes via direct interspecies electron transfer (DIET) and the photosensitizer to assemble a semi‐biological photocatalyst introduces an ecosystem engineering strategy in solar chemistry to drive sustainable chemical reactions. Microbial ecosystem engineering enables efficient solar‐driven methanogenesis over a biohybrid photocatalyst. The syntrophic coculture of Methanosarcina barkeri (M. barkeri) with the electron transport specialist Geobacter sulfurreducens KN400 (KN400) over carbon nitride produced a semi‐biological photocatalyst for the sunlight‐driven methane synthesis from carbon dioxide.