Transcriptional and translational dynamics underlying heat shock response in the thermophilic crenarchaeon Sulfolobus acidocaldarius

Rani Baes, Felix Grünberger, Sébastien Pyr Dit Ruys, Mohea Couturier, Sarah De Keulenaer, Sonja Skevin, Filip Van Nieuwerburgh, Didier Vertommen, Dina Grohmann, Sébastien Ferreira-Cerca, Eveline Peeters

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Abstract

High-temperature stress is critical for all organisms and induces a profound cellular response. For Crenarchaeota, little information is available on how heat shock affects cellular processes and on how this response is regulated. We set out to study heat shock response in the thermoacidophilic model crenarchaeon Sulfolobus acidocaldarius, which thrives in volcanic hot springs and has an optimal growth temperature of 75°C. Pulse-labeling experiments demonstrated that a temperature shift to 86°C induces a drastic reduction of the transcriptional and translational activity, but that RNA and protein neosynthesis still occurs. By combining RNA sequencing and mass spectrometry, an integrated mapping of the transcriptome and proteome was performed. This revealed that heat shock causes an immediate change in the gene expression profile, with RNA levels of half of the genes being affected, followed by a more subtle reprogramming of the protein landscape. Functional enrichment analysis indicated that nearly all cellular processes are affected by heat shock. A limited correlation was observed in the differential expression on the RNA and protein level, suggesting a prevalence of post-transcriptional and post-translational regulation. Furthermore, promoter sequence analysis of heat shock regulon genes demonstrated the conservation of strong transcription initiation elements for highly induced genes, but an absence of a conserved protein-binding motif. It is, therefore, hypothesized that histone-lacking archaea such as Sulfolobales use an evolutionarily ancient regulatory mechanism that relies on temperature-responsive changes in DNA organization and compaction induced by the action of nucleoid-associated proteins, as well as on enhanced recruitment of initiation factors. IMPORTANCE Heat shock response is the ability to respond adequately to sudden temperature increases that could be harmful for cellular survival and fitness. It is crucial for microorganisms living in volcanic hot springs that are characterized by high temperatures and large temperature fluctuations. In this study, we investigated how S. acidocaldarius, which grows optimally at 75°C, responds to heat shock by altering its gene expression and protein production processes. We shed light on which cellular processes are affected by heat shock and propose a hypothesis on underlying regulatory mechanisms. This work is not only relevant for the organism's lifestyle, but also with regard to its evolutionary status. Indeed, S. acidocaldarius belongs to the archaea, an ancient group of microbes that is more closely related to eukaryotes than to bacteria. Our study thus also contributes to a better understanding of the early evolution of heat shock response.

Original languageEnglish
Article numbere0359322
Number of pages23
JournalMBio
Volume14
Issue number5
Early online date29 Aug 2023
DOIs
Publication statusPublished - 31 Oct 2023

Bibliographical note

Funding Information:
This research was supported by Research Foundation Flanders (FWO-Vlaanderen) [PhD fellowship 1134419N to R.B. and Research Projects G021118N and G062820N to E.P.] and by the iBOF project “POSSIBL” [iBOF/21/092] of the Bijzonder Onderzoeksfonds. Research in the S.F.-C. laboratory is generously supported by the German Research Foundation (DFG): individual research grant [FE1622/2-1] and collaborative research centre SFB/CRC 960 [grant SFB960-AP1, SFB960-B13] "RNP biogenesis: assembly of ribosomes and non-ribosomal RNPs and control of their function." D.G. acknowledges funding by the German Research Foundation (grant number SFB/CRC 960 AP7). The authors declare no competing interests.

Funding Information:
We are grateful to Michael Jüttner and Nicolas Alexandre (S.F.-C. lab, University of Regensburg) for their support in setting up S. acidocaldarius pulse-labeling experiments, Gaëtan Herinckx for technical assistance during mass spectrometry sample processing, and Joris Van Lindt for help in troubleshooting the western blotting system on S. acidocaldarius crude lysate. We are grateful to Norio Kurosawa for the gift of the S. acidocaldarius SK-1 strain. This research was supported by Research Foundation Flanders (FWO-Vlaanderen) [PhD fellowship 1134419N to R.B. and Research Projects G021118N and G062820N to E.P.] and by the iBOF project “POSSIBL” [iBOF/21/092] of the Bijzonder Onderzoeksfonds. Research in the S.F.-C. laboratory is generously supported by the German Research Foundation (DFG): individual research grant [FE1622/2-1] and collaborative research centre SFB/CRC 960 [grant SFB960-AP1, SFB960-B13] "RNP biogenesis: assembly of ribosomes and non-ribosomal RNPs and control of their function." D.G. acknowledges funding by the German Research Foundation (grant number SFB/CRC 960 AP7). The authors declare no competing financial interests. Fonds Wetenschappelijk Onderzoek (FWO) 1134419N Rani Baes Fonds Wetenschappelijk Onderzoek (FWO) G021118N, G062820N Eveline Peeters UGent | Bijzonder Onderzoeksfonds UGent (BOF) iBOF/21/092 Eveline Peeters Deutsche Forschungsgemeinschaft (DFG) FE1622/2-1, SFB960-AP1, SFB960-B13 Sebastien Ferreira-Cerca Deutsche Forschungsgemeinschaft (DFG) SFB/CRC960-AP7 Dina Grohmann

Publisher Copyright:
© 2023 Baes et al.

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