Eukaryotic cell biology is temporally coordinated to support the energetic demands of protein homeostasis

John S. O’Neill (), Nathaniel P. Hoyle, J. Brian Robertson, Rachel S. Edgar, Andrew D. Beale, Sew Y. Peak-Chew, Jason Day, Ana S. H. Costa, Christian Frezza and Helen C. Causton ()
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John S. O’Neill: MRC Laboratory of Molecular Biology
Nathaniel P. Hoyle: MRC Laboratory of Molecular Biology
J. Brian Robertson: Middle Tennessee State University
Rachel S. Edgar: Imperial College
Andrew D. Beale: MRC Laboratory of Molecular Biology
Sew Y. Peak-Chew: MRC Laboratory of Molecular Biology
Jason Day: University of Cambridge
Ana S. H. Costa: University of Cambridge
Christian Frezza: University of Cambridge
Helen C. Causton: Columbia University Medical Center

Nature Communications, 2020, vol. 11, issue 1, 1-11

Abstract: Abstract Yeast physiology is temporally regulated, this becomes apparent under nutrient-limited conditions and results in respiratory oscillations (YROs). YROs share features with circadian rhythms and interact with, but are independent of, the cell division cycle. Here, we show that YROs minimise energy expenditure by restricting protein synthesis until sufficient resources are stored, while maintaining osmotic homeostasis and protein quality control. Although nutrient supply is constant, cells sequester and store metabolic resources via increased transport, autophagy and biomolecular condensation. Replete stores trigger increased H+ export which stimulates TORC1 and liberates proteasomes, ribosomes, chaperones and metabolic enzymes from non-membrane bound compartments. This facilitates translational bursting, liquidation of storage carbohydrates, increased ATP turnover, and the export of osmolytes. We propose that dynamic regulation of ion transport and metabolic plasticity are required to maintain osmotic and protein homeostasis during remodelling of eukaryotic proteomes, and that bioenergetic constraints selected for temporal organisation that promotes oscillatory behaviour.

Date: 2020
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DOI: 10.1038/s41467-020-18330-x

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