An adaptive biomolecular condensation response is conserved across environmentally divergent species

Samantha Keyport Kik, Dana Christopher, Hendrik Glauninger, Caitlin Wong Hickernell, Jared A. M. Bard, Kyle M. Lin, Allison H. Squires, Michael Ford, Tobin R. Sosnick and D. Allan Drummond ()
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Samantha Keyport Kik: The University of Chicago
Dana Christopher: The University of Chicago
Hendrik Glauninger: The University of Chicago
Caitlin Wong Hickernell: The University of Chicago
Jared A. M. Bard: The University of Chicago
Kyle M. Lin: The University of Chicago
Allison H. Squires: University of Chicago
Michael Ford: MS Bioworks
Tobin R. Sosnick: The University of Chicago
D. Allan Drummond: The University of Chicago

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract Cells must sense and respond to sudden maladaptive environmental changes—stresses—to survive and thrive. Across eukaryotes, stresses such as heat shock trigger conserved responses: growth arrest, a specific transcriptional response, and biomolecular condensation of protein and mRNA into structures known as stress granules under severe stress. The composition, formation mechanism, adaptive significance, and even evolutionary conservation of these condensed structures remain enigmatic. Here we provide a remarkable view into stress-triggered condensation, its evolutionary conservation and tuning, and its integration into other well-studied aspects of the stress response. Using three morphologically near-identical budding yeast species adapted to different thermal environments and diverged by up to 100 million years, we show that proteome-scale biomolecular condensation is tuned to species-specific thermal niches, closely tracking corresponding growth and transcriptional responses. In each species, poly(A)-binding protein—a core marker of stress granules—condenses in isolation at species-specific temperatures, with conserved molecular features and conformational changes modulating condensation. From the ecological to the molecular scale, our results reveal previously unappreciated levels of evolutionary selection in the eukaryotic stress response, while establishing a rich, tractable system for further inquiry.

Date: 2024
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DOI: 10.1038/s41467-024-47355-9

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