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Weak acids produced during anaerobic respiration suppress both photosynthesis and aerobic respiration

Author

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  • Xiaojie Pang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Wojciech J. Nawrocki

    (Vrije Universiteit Amsterdam
    Institut de Biologie Physico-Chimique)

  • Pierre Cardol

    (Université de Liège, B22)

  • Mengyuan Zheng

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Jingjing Jiang

    (Chinese Academy of Sciences)

  • Yuan Fang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Wenqiang Yang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Roberta Croce

    (Vrije Universiteit Amsterdam)

  • Lijin Tian

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

Abstract

While photosynthesis transforms sunlight energy into sugar, aerobic and anaerobic respiration (fermentation) catabolizes sugars to fuel cellular activities. These processes take place within one cell across several compartments, however it remains largely unexplored how they interact with one another. Here we report that the weak acids produced during fermentation down-regulate both photosynthesis and aerobic respiration. This effect is mechanistically explained with an “ion trapping” model, in which the lipid bilayer selectively traps protons that effectively acidify subcellular compartments with smaller buffer capacities – such as the thylakoid lumen. Physiologically, we propose that under certain conditions, e.g., dim light at dawn, tuning down the photosynthetic light reaction could mitigate the pressure on its electron transport chains, while suppression of respiration could accelerate the net oxygen evolution, thus speeding up the recovery from hypoxia. Since we show that this effect is conserved across photosynthetic phyla, these results indicate that fermentation metabolites exert widespread feedback control over photosynthesis and aerobic respiration. This likely allows algae to better cope with changing environmental conditions.

Suggested Citation

  • Xiaojie Pang & Wojciech J. Nawrocki & Pierre Cardol & Mengyuan Zheng & Jingjing Jiang & Yuan Fang & Wenqiang Yang & Roberta Croce & Lijin Tian, 2023. "Weak acids produced during anaerobic respiration suppress both photosynthesis and aerobic respiration," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39898-0
    DOI: 10.1038/s41467-023-39898-0
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    References listed on IDEAS

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    1. Benjamin Bailleul & Nicolas Berne & Omer Murik & Dimitris Petroutsos & Judit Prihoda & Atsuko Tanaka & Valeria Villanova & Richard Bligny & Serena Flori & Denis Falconet & Anja Krieger-Liszkay & Stefa, 2015. "Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms," Nature, Nature, vol. 524(7565), pages 366-369, August.
    2. Graham Peers & Thuy B. Truong & Elisabeth Ostendorf & Andreas Busch & Dafna Elrad & Arthur R. Grossman & Michael Hippler & Krishna K. Niyogi, 2009. "An ancient light-harvesting protein is critical for the regulation of algal photosynthesis," Nature, Nature, vol. 462(7272), pages 518-521, November.
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