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Engineering a synthetic energy-efficient formaldehyde assimilation cycle in Escherichia coli

Author

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  • Tong Wu

    (Max Planck Institute of Molecular Plant Physiology, Am Mühlenberg 1
    Charité—Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt Universität zu Berlin, Institute of Biochemistry, Charitéplatz 1)

  • Paul A. Gómez-Coronado

    (Max Planck Institute of Molecular Plant Physiology, Am Mühlenberg 1
    Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Str. 10)

  • Armin Kubis

    (Max Planck Institute of Molecular Plant Physiology, Am Mühlenberg 1)

  • Steffen N. Lindner

    (Max Planck Institute of Molecular Plant Physiology, Am Mühlenberg 1
    Charité—Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt Universität zu Berlin, Institute of Biochemistry, Charitéplatz 1)

  • Philippe Marlière

    (TESSSI, The European Syndicate of Synthetic Scientists and Industrialists, 81 rue Réaumur)

  • Tobias J. Erb

    (Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Str. 10)

  • Arren Bar-Even

    (Max Planck Institute of Molecular Plant Physiology, Am Mühlenberg 1)

  • Hai He

    (Max Planck Institute of Molecular Plant Physiology, Am Mühlenberg 1
    Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Str. 10)

Abstract

One-carbon (C1) substrates, such as methanol or formate, are attractive feedstocks for circular bioeconomy. These substrates are typically converted into formaldehyde, serving as the entry point into metabolism. Here, we design an erythrulose monophosphate (EuMP) cycle for formaldehyde assimilation, leveraging a promiscuous dihydroxyacetone phosphate dependent aldolase as key enzyme. In silico modeling reveals that the cycle is highly energy-efficient, holding the potential for high bioproduct yields. Dissecting the EuMP into four modules, we use a stepwise strategy to demonstrate in vivo feasibility of the modules in E. coli sensor strains with sarcosine as formaldehyde source. From adaptive laboratory evolution for module integration, we identify key mutations enabling the accommodation of the EuMP reactions with endogenous metabolism. Overall, our study demonstrates the proof-of-concept for a highly efficient, new-to-nature formaldehyde assimilation pathway, opening a way for the development of a methylotrophic platform for a C1-fueled bioeconomy in the future.

Suggested Citation

  • Tong Wu & Paul A. Gómez-Coronado & Armin Kubis & Steffen N. Lindner & Philippe Marlière & Tobias J. Erb & Arren Bar-Even & Hai He, 2023. "Engineering a synthetic energy-efficient formaldehyde assimilation cycle in Escherichia coli," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-44247-2
    DOI: 10.1038/s41467-023-44247-2
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    References listed on IDEAS

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    1. Elad Noor & Hulda S Haraldsdóttir & Ron Milo & Ronan M T Fleming, 2013. "Consistent Estimation of Gibbs Energy Using Component Contributions," PLOS Computational Biology, Public Library of Science, vol. 9(7), pages 1-11, July.
    2. Philipp Keller & Michael A. Reiter & Patrick Kiefer & Thomas Gassler & Lucas Hemmerle & Philipp Christen & Elad Noor & Julia A. Vorholt, 2022. "Generation of an Escherichia coli strain growing on methanol via the ribulose monophosphate cycle," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Katharine Sanderson, 2011. "Lignocellulose: A chewy problem," Nature, Nature, vol. 474(7352), pages 12-14, June.
    4. Igor W. Bogorad & Tzu-Shyang Lin & James C. Liao, 2013. "Synthetic non-oxidative glycolysis enables complete carbon conservation," Nature, Nature, vol. 502(7473), pages 693-697, October.
    5. Benjamin M. Woolston & Jason R. King & Michael Reiter & Bob Van Hove & Gregory Stephanopoulos, 2018. "Improving formaldehyde consumption drives methanol assimilation in engineered E. coli," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
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