Food production with plants consumes large amounts of water, occupies large areas of land and cannot guarantee food security beyond the 21st century. Industrial agriculture in particular, is destructive to the environment, fosters climate change in profound ways, deteriorates public health and causes high "hidden costs". Single-cell protein (SCP) represents an alternative with minimal carbon-, water-and land footprints. However, when grown on biowastes of industrial agriculture, heterotrophic SCP does not truly improve sustainability or food security.This hypothesis paper proposes autotrophic SCP bioprocess designs which enable sustainable, fail-safe and efficient production of edible biomass from CO 2 and N 2 or NH 3 . They can be driven by H 2 , CO or HCOOH from several sustainable sources. Besides H 2 O-electrolysis and syngas, surprisingly fossil fuels may provide an effectively carbon-negative and cheap supply of H 2 through the decomposition of CH 4 or oil. Most promising bioprocess designs consist of 2-stages. In the 1 st stage, homoacetogenic bacteria fix CO 2 up to 10 more efficiently than plants, and secrete it as acetate. In the 2 nd stage, selected microbes grow on the acetate and thereby form edible biomass. Bacteria have unique features including N 2 -fixation, H 2 S tolerance and O 2 -tolerant hydrogenases for fast lightindependent growth. Eukaryotic microalgae are already approved as food and exhibit oxygenic photosynthesis which partly replaces solar-panels, seawater desalination and H 2 O-electrolyzers. Photoheterotrophic growth on acetate decouples these benefits from inefficient endogenous CO 2 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 that are exposed directly to substrate gases, and that can be dry-harvested. 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 CO 2 from the air as carbonates. In two use cases, 2-stage designs with solar-powered H 2 -generation from seawater were estimated to exceed productivity of wheat 20-200 fold, for moderate and arid climates respectively. Preliminary cost estimates and data about direct and indirect subsidies of industrial agriculture lead to the hypothesis that autotrophic SCP likely outperforms industrial agriculture not only in ecological but also in economical aspects.