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Peroxisomal compartmentalization of amino acid biosynthesis reactions imposes an upper limit on compartment size

Author

Listed:
  • Ying Gu

    (The Francis Crick Institute
    King’s College London)

  • Sara Alam

    (The Francis Crick Institute
    King’s College London
    Medical Research Council London Institute of Medical Sciences)

  • Snezhana Oliferenko

    (The Francis Crick Institute
    King’s College London)

Abstract

Cellular metabolism relies on just a few redox cofactors. Selective compartmentalization may prevent competition between metabolic reactions requiring the same cofactor. Is such compartmentalization necessary for optimal cell function? Is there an optimal compartment size? Here we probe these fundamental questions using peroxisomal compartmentalization of the last steps of lysine and histidine biosynthesis in the fission yeast Schizosaccharomyces japonicus. We show that compartmentalization of these NAD+ dependent reactions together with a dedicated NADH/NAD+ recycling enzyme supports optimal growth when an increased demand for anabolic reactions taxes cellular redox balance. In turn, compartmentalization constrains the size of individual organelles, with larger peroxisomes accumulating all the required enzymes but unable to support both biosynthetic reactions at the same time. Our reengineering and physiological experiments indicate that compartmentalized biosynthetic reactions are sensitive to the size of the compartment, likely due to scaling-dependent changes within the system, such as enzyme packing density.

Suggested Citation

  • Ying Gu & Sara Alam & Snezhana Oliferenko, 2023. "Peroxisomal compartmentalization of amino acid biosynthesis reactions imposes an upper limit on compartment size," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41347-x
    DOI: 10.1038/s41467-023-41347-x
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    References listed on IDEAS

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    1. Erez Persi & Miquel Duran-Frigola & Mehdi Damaghi & William R. Roush & Patrick Aloy & John L. Cleveland & Robert J. Gillies & Eytan Ruppin, 2018. "Systems analysis of intracellular pH vulnerabilities for cancer therapy," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    2. Mohammad Tauqeer Alam & Viridiana Olin-Sandoval & Anna Stincone & Markus A. Keller & Aleksej Zelezniak & Ben F. Luisi & Markus Ralser, 2017. "The self-inhibitory nature of metabolic networks and its alleviation through compartmentalization," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
    3. Ying Gu & Snezhana Oliferenko, 2019. "Cellular geometry scaling ensures robust division site positioning," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
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