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| Status |
Public on Jul 31, 2023 |
| Title |
An adaptive biomolecular condensation response is conserved across environmentally divergent species |
| Organisms |
Kluyveromyces marxianus; Saccharomyces cerevisiae; Saccharomyces kudriavzevii |
| Experiment type |
Expression profiling by high throughput sequencing
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| Summary |
Cellular responses to maladaptive environmental changes—stresses—allow for organismal adaptation to diverse and dynamic conditions. Across the tree of life, cells upregulate a highly conserved transcriptional program in response to so-called proteotoxic stresses such as heat shock. Correspondingly, in eukaryotes, these stresses induce the formation of biomolecular condensates, clusters of mRNA and protein which are referred to as stress granules under severe stress. However, major questions remain about this stress-induced response. How conserved is the condensation response relative to the transcriptional response? How does it vary across environmental niches, and to what extent does it correspond with the conserved transcriptional response? To answer these fundamental questions, we studied the growth, transcriptional, and condensation heat-induced stress responses in three fungal species adapted to thrive in different thermal environments: cryophilic S. kudriavzevii, mesophilic S. cerevisiae, and thermotolerant K. marxianus. Here we show that transcriptional heat shock responses track each species’ evolved temperature range of growth. Further, orthologous proteins—including poly(A)-binding protein, Pab1, a core marker of stress granules—form condensates in vivo at temperatures systematically tuned to the temperature at which the organisms activate the transcriptional heat shock response and slow their growth. In vitro, purified Pab1 from each species condenses autonomously at niche-specific temperatures. Homologous mutations in Pab1 cause similar shifts in relative condensation temperature across species, and crucially, mutations which suppress condensation in vitro also reduce fitness during heat stress. Our findings indicate that stress-induced protein condensation is adaptive, conserved, integrated with the growth and transcriptional responses, and tuned to features of the cellular and organismal environment to initiate at niche-specific levels.
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| Overall design |
Total RNA was extracted from three yeast species - S. cerevisiae, S. kudriavzevii, and K. marxianus - with and without an 8 minute, species specific heat shock. There are two biological replicates for each species and temperature.
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| Contributor(s) |
Keyport Kik S, Bard JA, Drummond DA |
| Citation(s) |
38605014 |
| NIH grant(s) |
| Grant ID |
Grant title |
Affiliation |
Name |
| R35 GM144278 |
Function and Regulation of Stress-Induced Adaptive Condensates |
UNIVERSITY OF CHICAGO |
David Allan Drummond |
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| Submission date |
Jun 08, 2023 |
| Last update date |
May 02, 2024 |
| Contact name |
D Allan Drummond |
| E-mail(s) |
dadrummond@uchicago.edu
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| Organization name |
University of Chicago
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| Street address |
929 E 57th Street
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| City |
Chicago |
| State/province |
IL |
| ZIP/Postal code |
60637 |
| Country |
USA |
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| Platforms (3) |
| GPL27812 |
Illumina NovaSeq 6000 (Saccharomyces cerevisiae) |
| GPL29573 |
Illumina NovaSeq 6000 (Kluyveromyces marxianus) |
| GPL33472 |
Illumina NovaSeq 6000 (Saccharomyces kudriavzevii) |
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| Samples (12)
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| Relations |
| BioProject |
PRJNA981544 |
| Supplementary file |
Size |
Download |
File type/resource |
| GSE234499_Keyport-Kik_2023_TPMs.tsv.gz |
964.1 Kb |
(ftp)(http) |
TSV |
| GSE234499_Keyport-Kik_2023_counts.tsv.gz |
332.1 Kb |
(ftp)(http) |
TSV |
| GSE234499_RAW.tar |
320.0 Kb |
(http)(custom) |
TAR (of TSV) |
SRA Run Selector |
| Raw data are available in SRA |
| Processed data are available on Series record |
| Processed data provided as supplementary file |
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