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Nitrogen limitation reveals large reserves in metabolic and translational capacities of yeast

Author

Listed:
  • Rosemary Yu

    (Chalmers University of Technology
    Chalmers University of Technology)

  • Kate Campbell

    (Chalmers University of Technology
    Chalmers University of Technology)

  • Rui Pereira

    (Chalmers University of Technology
    Chalmers University of Technology)

  • Johan Björkeroth

    (Chalmers University of Technology
    Chalmers University of Technology)

  • Qi Qi

    (Chalmers University of Technology
    Chalmers University of Technology)

  • Egor Vorontsov

    (University of Gothenburg)

  • Carina Sihlbom

    (University of Gothenburg)

  • Jens Nielsen

    (Chalmers University of Technology
    Chalmers University of Technology
    Technical University of Denmark
    BioInnovation Institute, Ole Måløes Vej 3)

Abstract

Cells maintain reserves in their metabolic and translational capacities as a strategy to quickly respond to changing environments. Here we quantify these reserves by stepwise reducing nitrogen availability in yeast steady-state chemostat cultures, imposing severe restrictions on total cellular protein and transcript content. Combining multi-omics analysis with metabolic modeling, we find that seven metabolic superpathways maintain >50% metabolic capacity in reserve, with glucose metabolism maintaining >80% reserve capacity. Cells maintain >50% reserve in translational capacity for 2490 out of 3361 expressed genes (74%), with a disproportionately large reserve dedicated to translating metabolic proteins. Finally, ribosome reserves contain up to 30% sub-stoichiometric ribosomal proteins, with activation of reserve translational capacity associated with selective upregulation of 17 ribosomal proteins. Together, our dataset provides a quantitative link between yeast physiology and cellular economics, which could be leveraged in future cell engineering through targeted proteome streamlining.

Suggested Citation

  • Rosemary Yu & Kate Campbell & Rui Pereira & Johan Björkeroth & Qi Qi & Egor Vorontsov & Carina Sihlbom & Jens Nielsen, 2020. "Nitrogen limitation reveals large reserves in metabolic and translational capacities of yeast," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-15749-0
    DOI: 10.1038/s41467-020-15749-0
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    Cited by:

    1. Ning Qin & Lingyun Li & Xiaozhen Wan & Xu Ji & Yu Chen & Chaokun Li & Ping Liu & Yijie Zhang & Weijie Yang & Junfeng Jiang & Jianye Xia & Shuobo Shi & Tianwei Tan & Jens Nielsen & Yun Chen & Zihe Liu, 2024. "Increased CO2 fixation enables high carbon-yield production of 3-hydroxypropionic acid in yeast," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Iván Domenzain & Benjamín Sánchez & Mihail Anton & Eduard J. Kerkhoven & Aarón Millán-Oropeza & Céline Henry & Verena Siewers & John P. Morrissey & Nikolaus Sonnenschein & Jens Nielsen, 2022. "Reconstruction of a catalogue of genome-scale metabolic models with enzymatic constraints using GECKO 2.0," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Philipp Wendering & Marius Arend & Zahra Razaghi-Moghadam & Zoran Nikoloski, 2023. "Data integration across conditions improves turnover number estimates and metabolic predictions," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    4. Ritu Gupta & Swagata Adhikary & Nidhi Dalpatraj & Sunil Laxman, 2024. "An economic demand-based framework for prioritization strategies in response to transient amino acid limitations," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    5. Manlu Zhu & Xiongfeng Dai, 2024. "Shaping of microbial phenotypes by trade-offs," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

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