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

Published version
Peer-reviewed

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Authors

O’ Neill, John S.  ORCID logo  https://orcid.org/0000-0003-2204-6096
Hoyle, Nathaniel P.  ORCID logo  https://orcid.org/0000-0002-3250-0494
Robertson, J. Brian 
Edgar, Rachel S. 

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.

Description

Keywords

Article, /631/45/320, /631/45/475, /631/1647/334/2243/1796, /631/553/2701, /49/31, /49/47, /96/35, /82/58, article

Journal Title

Nature Communications

Conference Name

Journal ISSN

2041-1723

Volume Title

11

Publisher

Nature Publishing Group UK