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Generation of an Escherichia coli strain growing on methanol via the ribulose monophosphate cycle

Author

Listed:
  • Philipp Keller

    (ETH Zurich)

  • Michael A. Reiter

    (ETH Zurich)

  • Patrick Kiefer

    (ETH Zurich)

  • Thomas Gassler

    (ETH Zurich)

  • Lucas Hemmerle

    (ETH Zurich
    Ecole Polytechnique Fédérale de Lausanne)

  • Philipp Christen

    (ETH Zurich)

  • Elad Noor

    (Weizmann Institute of Science)

  • Julia A. Vorholt

    (ETH Zurich)

Abstract

Methanol is a liquid with high energy storage capacity that holds promise as an alternative substrate to replace sugars in the biotechnology industry. It can be produced from CO2 or methane and its use does not compete with food and animal feed production. However, there are currently only limited biotechnological options for the valorization of methanol, which hinders its widespread adoption. Here, we report the conversion of the industrial platform organism Escherichia coli into a synthetic methylotroph that assimilates methanol via the energy efficient ribulose monophosphate cycle. Methylotrophy is achieved after evolution of a methanol-dependent E. coli strain over 250 generations in continuous chemostat culture. We demonstrate growth on methanol and biomass formation exclusively from the one-carbon source by 13C isotopic tracer analysis. In line with computational modeling, the methylotrophic E. coli strain optimizes methanol oxidation by upregulation of an improved methanol dehydrogenase, increasing ribulose monophosphate cycle activity, channeling carbon flux through the Entner-Doudoroff pathway and downregulating tricarboxylic acid cycle enzymes. En route towards sustainable bioproduction processes, our work lays the foundation for the efficient utilization of methanol as the dominant carbon and energy resource.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32744-9
    DOI: 10.1038/s41467-022-32744-9
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    References listed on IDEAS

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    Cited by:

    1. 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.
    2. Liang-Yu Nieh & Frederic Y.-H. Chen & Hsin-Wei Jung & Kuan-Yu Su & Chao-Yin Tsuei & Chun-Ting Lin & Yue-Qi Lee & James C. Liao, 2024. "Evolutionary engineering of methylotrophic E. coli enables fast growth on methanol," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Simone Bachleitner & Özge Ata & Diethard Mattanovich, 2023. "The potential of CO2-based production cycles in biotechnology to fight the climate crisis," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    4. Yeonhwa Yu & Yongfan Shi & Young Wan Kwon & Yoobin Choi & Yusik Kim & Jeong-Geol Na & June Huh & Jeewon Lee, 2024. "A rationally designed miniature of soluble methane monooxygenase enables rapid and high-yield methanol production in Escherichia coli," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. Enrico Orsi & Pablo Ivan Nikel & Lars Keld Nielsen & Stefano Donati, 2023. "Synergistic investigation of natural and synthetic C1-trophic microorganisms to foster a circular carbon economy," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    6. Cong Zhang & Di-Fei Zhou & Meng-Ying Wang & Ya-Zhen Song & Chong Zhang & Ming-Ming Zhang & Jing Sun & Lu Yao & Xu-Hua Mo & Zeng-Xin Ma & Xiao-Jie Yuan & Yi Shao & Hao-Ran Wang & Si-Han Dong & Kai Bao , 2024. "Phosphoribosylpyrophosphate synthetase as a metabolic valve advances Methylobacterium/Methylorubrum phyllosphere colonization and plant growth," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    7. Maren Nattermann & Sebastian Wenk & Pascal Pfister & Hai He & Seung Hwan Lee & Witold Szymanski & Nils Guntermann & Fayin Zhu & Lennart Nickel & Charlotte Wallner & Jan Zarzycki & Nicole Paczia & Nina, 2023. "Engineering a new-to-nature cascade for phosphate-dependent formate to formaldehyde conversion in vitro and in vivo," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    8. Bernd M. Mitic & Christina Troyer & Lisa Lutz & Michael Baumschabl & Stephan Hann & Diethard Mattanovich, 2023. "The oxygen-tolerant reductive glycine pathway assimilates methanol, formate and CO2 in the yeast Komagataella phaffii," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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