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Industrial agriculture is destructive to the environment, pollutes large amounts of water, fosters climate change and cannot guarantee food security for the 21st century. Single-cell protein (SCP) represents a safe alternative with minimal carbon and water footprints, but does not truly improve sustainability or food security when grown on waste products of industrial agriculture. This hypothesis paper proposes autotrophic SCP bioprocess designs which enable sustainable, fail-safe and efficient production of edible biomass from CO2 and N2 or NH3. They can be driven by H2, CO, HCOOH from several sustainable sources and provide versatile options of biowaste upgrading. Most promising designs consist of 2-stages. In the 1st stage, homoacetogenic bacteria fix CO2 and secrete it as acetate with unrivaled yields. In the 2nd stage, selected microbes transform the acetate to edible biomass. Bacteria have various unique features including O2-tolerant hydrogenases, N2-fixation and H2S tolerance. Eukaryotic microalgae are approved as food and exhibit oxygenic photosynthesis which partly replaces solar-panels, seawater desalination and H2O- electrolyzers. Photoheterotrophic growth on acetate allows to decouple the efficient light-reaction from inefficient CO2 fixation. Slow gas mass-transfer, poor light distribution and expensive cell harvest are major challenges arising from the cultivation in liquid media. To cope with this, microbes grow as hydrated biofilms, exposed directly to substrate gases and light. Two suitable bioreactors are presented and adaptations for 2-stage designs are proposed. Since provision with substrates is expensive, two strategies are proposed for the safe extraction of substrates from food-grade as well as non-food-grade biowastes via partial anaerobic digestion. Additionally, alkalic pH and hydroxides formed at the cathode during electrolysis may be used to precipitate CO2 from the air as carbonates. In two use cases, 2-stage designs with solar-powered H2-generation from seawater were estimated to exceed productivity of wheat 20-200 fold. Since for that particular bioprocess design electricity is the dominant cost driver, overall product cost can be estimated to 0,5-1 € per kg dry SCP. When direct and indirect subsidies are taken into account, autotrophic SCP likely outperforms industrial agriculture not only in ecological but also in economical aspects.
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