Uncovering the temporal dynamics and regulatory networks of thermal stress response in a hyperthermophile using transcriptomics and proteomics

Gruenberger, Felix and Schmid, Georg and El Ahmad, Zubeir and Fenk, Martin and Vogl, Katharina and Reichelt, Robert and Hausner, Winfried and Urlaub, Henning and Lenz, Christof and Grohmann, Dina (2023) Uncovering the temporal dynamics and regulatory networks of thermal stress response in a hyperthermophile using transcriptomics and proteomics. MBIO: e0217423. ISSN 2150-7511,

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Abstract

Facing rapid fluctuations in their natural environment, extremophiles, like the hyperthermophilic archaeon Pyrococcus furiosus, exhibit remarkable adaptability to extreme conditions. However, our understanding of their dynamic cellular responses remains limited. This study integrates RNA-sequencing and mass spectrometry data, thereby elucidating transcriptomic and proteomic responses to heat and cold shock stress in P. furiosus. Our results reveal rapid and dynamic changes in gene and protein expression following these stress responses. Heat shock triggers extensive transcriptome reprogramming, orchestrated by the transcriptional regulator Phr, targeting a broader gene repertoire than previously demonstrated. For heat shock signature genes, RNA levels swiftly return to baseline upon recovery, while protein levels remain persistently upregulated, reflecting a rapid but sustained response. Intriguingly, cold shock at 4degree celsius elicits distinct short- and long-term responses at both RNA and protein levels. Cluster analysis identified gene sets with either congruent or contrasting trends in RNA and protein changes, representing well-separated arCOG groups tailored to their individual cellular responses. Particularly, upregulation of ribosomal proteins and significant enrichment of 5'-leadered sequences in cold-shock responsive genes suggest that translation regulation is important during cold shock adaption. Further investigating transcriptomic features, we reveal that thermal stress genes are equipped with basal sequence elements, such as strong promoter and poly(U)-terminators, facilitating a regulated response of the respective transcription units. Our study provides a comprehensive overview of the cellular response to temperature stress, advancing our understanding of stress response mechanisms in hyperthermophilic archaea and providing valuable insights into the molecular adaptations that facilitate life in extreme environments.

Item Type: Article
Uncontrolled Keywords: HEAT-SHOCK RESPONSE; COLD-SHOCK; PYROCOCCUS-FURIOSUS; ESCHERICHIA-COLI; RIBOSOME BIOGENESIS; GROWTH TEMPERATURE; GENE-REGULATION; REVERSE GYRASE; RNA; ARCHAEON; archaea; heat shock; cold shock; transcriptomics; proteomics
Subjects: 500 Science > 570 Life sciences
Divisions: Biology, Preclinical Medicine > Institut für Biochemie, Genetik und Mikrobiologie > Lehrstuhl für Mikrobiologie (Archaeenzentrum) > Prof. Dr. Dina Grohmann
Depositing User: Dr. Gernot Deinzer
Date Deposited: 07 Mar 2024 15:36
Last Modified: 07 Mar 2024 15:36
URI: https://pred.uni-regensburg.de/id/eprint/58969

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