IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-49579-1.html
   My bibliography  Save this article

ATP biosensor reveals microbial energetic dynamics and facilitates bioproduction

Author

Listed:
  • Xinyue Mu

    (Washington University in St. Louis)

  • Trent D. Evans

    (Washington University in St. Louis)

  • Fuzhong Zhang

    (Washington University in St. Louis
    Division of Biological & Biomedical Sciences, Washington University in St. Louis
    Institute of Materials Science & Engineering, Washington University in St. Louis)

Abstract

Adenosine-5’-triphosphate (ATP), the primary energy currency in cellular processes, drives metabolic activities and biosynthesis. Despite its importance, understanding intracellular ATP dynamics’ impact on bioproduction and exploiting it for enhanced bioproduction remains largely unexplored. Here, we harness an ATP biosensor to dissect ATP dynamics across different growth phases and carbon sources in multiple microbial strains. We find transient ATP accumulations during the transition from exponential to stationary growth phases in various conditions, coinciding with fatty acid (FA) and polyhydroxyalkanoate (PHA) production in Escherichia coli and Pseudomonas putida, respectively. We identify carbon sources (acetate for E. coli, oleate for P. putida) that elevate steady-state ATP levels and boost FA and PHA production. Moreover, we employ ATP dynamics as a diagnostic tool to assess metabolic burden, revealing bottlenecks that limit limonene bioproduction. Our results not only elucidate the relationship between ATP dynamics and bioproduction but also showcase its value in enhancing bioproduction in various microbial species.

Suggested Citation

  • Xinyue Mu & Trent D. Evans & Fuzhong Zhang, 2024. "ATP biosensor reveals microbial energetic dynamics and facilitates bioproduction," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49579-1
    DOI: 10.1038/s41467-024-49579-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-49579-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-49579-1?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. Pamela P. Peralta-Yahya & Fuzhong Zhang & Stephen B. del Cardayre & Jay D. Keasling, 2012. "Microbial engineering for the production of advanced biofuels," Nature, Nature, vol. 488(7411), pages 320-328, August.
    2. Mark A. Lobas & Rongkun Tao & Jun Nagai & Mira T. Kronschläger & Philip M. Borden & Jonathan S. Marvin & Loren L. Looger & Baljit S. Khakh, 2019. "A genetically encoded single-wavelength sensor for imaging cytosolic and cell surface ATP," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    3. Pamela P. Peralta-Yahya & Mario Ouellet & Rossana Chan & Aindrila Mukhopadhyay & Jay D. Keasling & Taek Soon Lee, 2011. "Identification and microbial production of a terpene-based advanced biofuel," Nature Communications, Nature, vol. 2(1), pages 1-8, 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. Das, Manali & Patra, Pradipta & Ghosh, Amit, 2020. "Metabolic engineering for enhancing microbial biosynthesis of advanced biofuels," Renewable and Sustainable Energy Reviews, Elsevier, vol. 119(C).
    2. Ulugbek Azimov & Victor Okoro & Hector H. Hernandez, 2021. "Recent Progress and Trends in the Development of Microbial Biofuels from Solid Waste—A Review," Energies, MDPI, vol. 14(19), pages 1-23, September.
    3. Scaife, Mark A. & Merkx-Jacques, Alexandra & Woodhall, David L. & Armenta, Roberto E., 2015. "Algal biofuels in Canada: Status and potential," Renewable and Sustainable Energy Reviews, Elsevier, vol. 44(C), pages 620-642.
    4. Fernand, Francois & Israel, Alvaro & Skjermo, Jorunn & Wichard, Thomas & Timmermans, Klaas R. & Golberg, Alexander, 2017. "Offshore macroalgae biomass for bioenergy production: Environmental aspects, technological achievements and challenges," Renewable and Sustainable Energy Reviews, Elsevier, vol. 75(C), pages 35-45.
    5. Liu, Zihe & Moradi, Hamideh & Shi, Shuobo & Darvishi, Farshad, 2021. "Yeasts as microbial cell factories for sustainable production of biofuels," Renewable and Sustainable Energy Reviews, Elsevier, vol. 143(C).
    6. Maity, Sunil K., 2015. "Opportunities, recent trends and challenges of integrated biorefinery: Part II," Renewable and Sustainable Energy Reviews, Elsevier, vol. 43(C), pages 1446-1466.
    7. Long, Feng & Liu, Weiguo & Jiang, Xia & Zhai, Qiaolong & Cao, Xincheng & Jiang, Jianchun & Xu, Junming, 2021. "State-of-the-art technologies for biofuel production from triglycerides: A review," Renewable and Sustainable Energy Reviews, Elsevier, vol. 148(C).
    8. Acheampong, Michael & Ertem, Funda Cansu & Kappler, Benjamin & Neubauer, Peter, 2017. "In pursuit of Sustainable Development Goal (SDG) number 7: Will biofuels be reliable?," Renewable and Sustainable Energy Reviews, Elsevier, vol. 75(C), pages 927-937.
    9. Ke-Na Feng & Yue Zhang & Mingfang Zhang & Yan-Long Yang & Ji-Kai Liu & Lifeng Pan & Ying Zeng, 2023. "A flavin-monooxygenase catalyzing oxepinone formation and the complete biosynthesis of vibralactone," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    10. Danielle L. Schmitt & Stephanie D. Curtis & Anne C. Lyons & Jin-fan Zhang & Mingyuan Chen & Catherine Y. He & Sohum Mehta & Reuben J. Shaw & Jin Zhang, 2022. "Spatial regulation of AMPK signaling revealed by a sensitive kinase activity reporter," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    11. Shihui Yang & Wei Wang & Hui Wei & Stefanie Van Wychen & Philip T. Pienkos & Min Zhang & Michael E. Himmel, 2016. "Comparison of Nitrogen Depletion and Repletion on Lipid Production in Yeast and Fungal Species," Energies, MDPI, vol. 9(9), pages 1-12, August.
    12. Liu, Kaimin & Fu, Jianqin & Deng, Banglin & Yang, Jing & Tang, Qijun & Liu, Jingping, 2014. "The influences of pressure and temperature on laminar flame propagations of n-butanol, iso-octane and their blends," Energy, Elsevier, vol. 73(C), pages 703-715.
    13. Su, HaiFeng & Lin, JiaFu & Tan, FuRong, 2017. "Progress and perspective of biosynthetic platform for higher-order biofuels," Renewable and Sustainable Energy Reviews, Elsevier, vol. 80(C), pages 801-826.
    14. Flemming Holtorf & Paul I. Barton, 2024. "Tighter Bounds on Transient Moments of Stochastic Chemical Systems," Journal of Optimization Theory and Applications, Springer, vol. 200(1), pages 104-149, January.
    15. Shannon Trombley & Jackson Powell & Pavithran Guttipatti & Andrew Matamoros & Xiaohui Lin & Tristan O’Harrow & Tobias Steinschaden & Leann Miles & Qin Wang & Shuchao Wang & Jingyun Qiu & Qingyang Li &, 2023. "Glia instruct axon regeneration via a ternary modulation of neuronal calcium channels in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    16. Chen, Hong-Ge & Zhang, Y.-H. Percival, 2015. "New biorefineries and sustainable agriculture: Increased food, biofuels, and ecosystem security," Renewable and Sustainable Energy Reviews, Elsevier, vol. 47(C), pages 117-132.
    17. Sadhukhan, Jhuma & Lloyd, Jon R. & Scott, Keith & Premier, Giuliano C. & Yu, Eileen H. & Curtis, Tom & Head, Ian M., 2016. "A critical review of integration analysis of microbial electrosynthesis (MES) systems with waste biorefineries for the production of biofuel and chemical from reuse of CO2," Renewable and Sustainable Energy Reviews, Elsevier, vol. 56(C), pages 116-132.
    18. Aivett Bilbao & Nathalie Munoz & Joonhoon Kim & Daniel J. Orton & Yuqian Gao & Kunal Poorey & Kyle R. Pomraning & Karl Weitz & Meagan Burnet & Carrie D. Nicora & Rosemarie Wilton & Shuang Deng & Ziyu , 2023. "PeakDecoder enables machine learning-based metabolite annotation and accurate profiling in multidimensional mass spectrometry measurements," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    19. Graham Rockwell & Nicholas J Guido & George M Church, 2013. "Redirector: Designing Cell Factories by Reconstructing the Metabolic Objective," PLOS Computational Biology, Public Library of Science, vol. 9(1), pages 1-15, January.
    20. 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.

    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:15:y:2024:i:1:d:10.1038_s41467-024-49579-1. 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.