Ribosomes hibernate on mitochondria during cellular stress

Olivier Gemin, Maciej Gluc, Higor Rosa, Michael Purdy, Moritz Niemann, Yelena Peskova, Simone Mattei () and Ahmad Jomaa ()
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Olivier Gemin: Meyerhofstraße 1
Maciej Gluc: University of Virginia
Higor Rosa: Meyerhofstraße 1
Michael Purdy: University of Virginia
Moritz Niemann: Meyerhofstraße 1
Yelena Peskova: University of Virginia
Simone Mattei: Meyerhofstraße 1
Ahmad Jomaa: University of Virginia

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: Abstract Cell survival under nutrient-deprived conditions relies on cells’ ability to adapt their organelles and rewire their metabolic pathways. In yeast, glucose depletion induces a stress response mediated by mitochondrial fragmentation and sequestration of cytosolic ribosomes on mitochondria. This cellular adaptation promotes survival under harsh environmental conditions; however, the underlying mechanism of this response remains unknown. Here, we demonstrate that upon glucose depletion protein synthesis is halted. Cryo-electron microscopy structure of the ribosomes show that they are devoid of both tRNA and mRNA, and a subset of the particles depicted a conformational change in rRNA H69 that could prevent tRNA binding. Our in situ structural analyses reveal that the hibernating ribosomes tether to fragmented mitochondria and establish eukaryotic-specific, higher-order storage structures by assembling into oligomeric arrays on the mitochondrial surface. Notably, we show that hibernating ribosomes exclusively bind to the outer mitochondrial membrane via the small ribosomal subunit during cellular stress. We identify the ribosomal protein Cpc2/RACK1 as the molecule mediating ribosomal tethering to mitochondria. This study unveils the molecular mechanism connecting mitochondrial stress with the shutdown of protein synthesis and broadens our understanding of cellular responses to nutrient scarcity and cell quiescence.

Date: 2024
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DOI: 10.1038/s41467-024-52911-4

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