IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37957-0.html
   My bibliography  Save this article

Dynamic fluctuations in a bacterial metabolic network

Author

Listed:
  • Shuangyu Bi

    (Max Planck Institute for Terrestrial Microbiology and Center for Synthetic Microbiology (SYNMIKRO)
    Shandong University)

  • Manika Kargeti

    (Max Planck Institute for Terrestrial Microbiology and Center for Synthetic Microbiology (SYNMIKRO))

  • Remy Colin

    (Max Planck Institute for Terrestrial Microbiology and Center for Synthetic Microbiology (SYNMIKRO))

  • Niklas Farke

    (University of Tübingen)

  • Hannes Link

    (University of Tübingen)

  • Victor Sourjik

    (Max Planck Institute for Terrestrial Microbiology and Center for Synthetic Microbiology (SYNMIKRO))

Abstract

The operation of the central metabolism is typically assumed to be deterministic, but dynamics and high connectivity of the metabolic network make it potentially prone to generating fluctuations. However, time-resolved measurements of metabolite levels in individual cells that are required to characterize such fluctuations remained a challenge, particularly in small bacterial cells. Here we use single-cell metabolite measurements based on Förster resonance energy transfer, combined with computer simulations, to explore the real-time dynamics of the metabolic network of Escherichia coli. We observe that steplike exposure of starved E. coli to glycolytic carbon sources elicits large periodic fluctuations in the intracellular concentration of pyruvate in individual cells. These fluctuations are consistent with predicted oscillatory dynamics of E. coli metabolic network, and they are primarily controlled by biochemical reactions around the pyruvate node. Our results further indicate that fluctuations in glycolysis propagate to other cellular processes, possibly leading to temporal heterogeneity of cellular states within a population.

Suggested Citation

  • Shuangyu Bi & Manika Kargeti & Remy Colin & Niklas Farke & Hannes Link & Victor Sourjik, 2023. "Dynamic fluctuations in a bacterial metabolic network," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37957-0
    DOI: 10.1038/s41467-023-37957-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37957-0
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-37957-0?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Christopher V. Rao & Denise M. Wolf & Adam P. Arkin, 2002. "Control, exploitation and tolerance of intracellular noise," Nature, Nature, vol. 420(6912), pages 231-237, November.
    2. Kevin S. Farquhar & Daniel A. Charlebois & Mariola Szenk & Joseph Cohen & Dmitry Nevozhay & Gábor Balázsi, 2019. "Role of network-mediated stochasticity in mammalian drug resistance," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    3. Daniel J. Kiviet & Philippe Nghe & Noreen Walker & Sarah Boulineau & Vanda Sunderlikova & Sander J. Tans, 2014. "Stochasticity of metabolism and growth at the single-cell level," Nature, Nature, vol. 514(7522), pages 376-379, October.
    4. Avigdor Eldar & Michael B. Elowitz, 2010. "Functional roles for noise in genetic circuits," Nature, Nature, vol. 467(7312), pages 167-173, September.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Lucy Ham & Megan A. Coomer & Kaan Öcal & Ramon Grima & Michael P. H. Stumpf, 2024. "A stochastic vs deterministic perspective on the timing of cellular events," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    2. Vera Bettenworth & Simon Vliet & Bartosz Turkowyd & Annika Bamberger & Heiko Wendt & Matthew McIntosh & Wieland Steinchen & Ulrike Endesfelder & Anke Becker, 2022. "Frequency modulation of a bacterial quorum sensing response," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Jessica A Lee & Siavash Riazi & Shahla Nemati & Jannell V Bazurto & Andreas E Vasdekis & Benjamin J Ridenhour & Christopher H Remien & Christopher J Marx, 2019. "Microbial phenotypic heterogeneity in response to a metabolic toxin: Continuous, dynamically shifting distribution of formaldehyde tolerance in Methylobacterium extorquens populations," PLOS Genetics, Public Library of Science, vol. 15(11), pages 1-38, November.
    4. Mohammad Soltani & Cesar A Vargas-Garcia & Duarte Antunes & Abhyudai Singh, 2016. "Intercellular Variability in Protein Levels from Stochastic Expression and Noisy Cell Cycle Processes," PLOS Computational Biology, Public Library of Science, vol. 12(8), pages 1-23, August.
    5. Kazunari Iwamoto & Yuki Shindo & Koichi Takahashi, 2016. "Modeling Cellular Noise Underlying Heterogeneous Cell Responses in the Epidermal Growth Factor Signaling Pathway," PLOS Computational Biology, Public Library of Science, vol. 12(11), pages 1-18, November.
    6. Junjie Luo & Jun Wang & Ting Martin Ma & Zhirong Sun, 2010. "Reverse Engineering of Bacterial Chemotaxis Pathway via Frequency Domain Analysis," PLOS ONE, Public Library of Science, vol. 5(3), pages 1-8, March.
    7. Ankit Gupta & Mustafa Khammash, 2022. "Frequency spectra and the color of cellular noise," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    8. Lee, Julian, 2023. "Poisson distributions in stochastic dynamics of gene expression: What events do they count?," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 630(C).
    9. Georg Fritz & Judith A Megerle & Sonja A Westermayer & Delia Brick & Ralf Heermann & Kirsten Jung & Joachim O Rädler & Ulrich Gerland, 2014. "Single Cell Kinetics of Phenotypic Switching in the Arabinose Utilization System of E. coli," PLOS ONE, Public Library of Science, vol. 9(2), pages 1-12, February.
    10. Laura Corrales-Guerrero & Asaf Tal & Rinat Arbel-Goren & Vicente Mariscal & Enrique Flores & Antonia Herrero & Joel Stavans, 2015. "Spatial Fluctuations in Expression of the Heterocyst Differentiation Regulatory Gene hetR in Anabaena Filaments," PLOS Genetics, Public Library of Science, vol. 11(4), pages 1-21, April.
    11. Singh, Abhyudai & Vahdat, Zahra & Xu, Zikai, 2019. "Time-triggered stochastic hybrid systems with two timer-dependent resets," OSF Preprints u8fzg, Center for Open Science.
    12. Ming Ni & Antoine L Decrulle & Fanette Fontaine & Alice Demarez & Francois Taddei & Ariel B Lindner, 2012. "Pre-Disposition and Epigenetics Govern Variation in Bacterial Survival upon Stress," PLOS Genetics, Public Library of Science, vol. 8(12), pages 1-11, December.
    13. Jan Hasenauer & Christine Hasenauer & Tim Hucho & Fabian J Theis, 2014. "ODE Constrained Mixture Modelling: A Method for Unraveling Subpopulation Structures and Dynamics," PLOS Computational Biology, Public Library of Science, vol. 10(7), pages 1-17, July.
    14. Sourabh Lahiri & Philippe Nghe & Sander J Tans & Martin Luc Rosinberg & David Lacoste, 2017. "Information-theoretic analysis of the directional influence between cellular processes," PLOS ONE, Public Library of Science, vol. 12(11), pages 1-26, November.
    15. Burton W Andrews & Pablo A Iglesias, 2007. "An Information-Theoretic Characterization of the Optimal Gradient Sensing Response of Cells," PLOS Computational Biology, Public Library of Science, vol. 3(8), pages 1-9, August.
    16. Martiny, Emil S. & Jensen, Mogens H. & Heltberg, Mathias S., 2022. "Detecting limit cycles in stochastic time series," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 605(C).
    17. Ziya Kalay & Takahiro K Fujiwara & Akihiro Kusumi, 2012. "Confining Domains Lead to Reaction Bursts: Reaction Kinetics in the Plasma Membrane," PLOS ONE, Public Library of Science, vol. 7(3), pages 1-8, March.
    18. Margaritis Voliotis & Philipp Thomas & Ramon Grima & Clive G Bowsher, 2016. "Stochastic Simulation of Biomolecular Networks in Dynamic Environments," PLOS Computational Biology, Public Library of Science, vol. 12(6), pages 1-18, June.
    19. Gabriele Micali & Gerardo Aquino & David M Richards & Robert G Endres, 2015. "Accurate Encoding and Decoding by Single Cells: Amplitude Versus Frequency Modulation," PLOS Computational Biology, Public Library of Science, vol. 11(6), pages 1-21, June.
    20. Chen, Aimin & Tian, Tianhai & Chen, Yiren & Zhou, Tianshou, 2022. "Stochastic analysis of a complex gene-expression model," Chaos, Solitons & Fractals, Elsevier, vol. 160(C).

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37957-0. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.