Advances in systems metabolic engineering of autotrophic carbon oxide-fixing biocatalysts towards a circular economy

High levels of anthropogenic CO2 emissions are driving the warming of global climate. If this pattern of increasing emissions does not change, it will cause further climate change with severe consequences for the human population. On top of this, the increasing accumulation of solid waste within the linear economy model is threatening global biosustainability. The magnitude of these challenges requires several approaches to capture and utilize waste carbon and establish a circular economy. Microbial gas fermentation presents an exciting opportunity to capture carbon oxides from gaseous and solid waste streams with high feedstock flexibility and selectivity. Here we discuss available microbial systems and review in detail the metabolism of both anaerobic acetogens and aerobic hydrogenotrophs and their ability to utilize C1 waste feedstocks. More specifically, we provide an overview of the systems-level understanding of metabolism, key metabolic pathways, scale-up opportunities and commercial successes, and the most recent technological advances in strain and process engineering. Finally, we also discuss in detail the gaps and opportunities to advance the understanding of these autotrophic biocatalysts for the efficient and economically viable production of bioproducts from recycled carbon. •Carbon-fixing anaerobic acetogens and aerobic hydrogenotrophs are promising platforms for carbon-negative biomanufacturing.•Systems metabolic engineering is a powerful approach to unlock the potential of these platforms and their unique metabolism.•Available engineering strategies to efficiently modify acetogens and hydrogenotrophs are discussed.•Industrial gas fermentation efforts are showcased including first commercial scale operations and new process strategies.•Gaps and opportunities to advance the understanding and engineering of these autotrophic biocatalysts are highlighted.