A genome-scale atlas reveals complex interplay of transcription and translation in an archaeon

Lorenzetti, Alan Péricles Rodrigues; Kusebauch, Ulrike; Wu, Wei-Ju; Almeida, João Fernando Lourenço de; Turkarslan, Serdar; Lomana, Adrián López García de; Gomes-Filho, José Vicente; Vêncio, Ricardo Z. N.; Moritz, Robert L.; Koide, Tie; Baliga, Nitin S.

doi:10.1101/2022.08.31.505529

Cited by 3 publications

(1 citation statement)

References 118 publications

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“…In addition to transcription factor-based regulation, archaealspecific small RNAs (asRNAs) and RNA-binding proteins like proteins of the Sm-like protein family have been implicated in fine-tuning regulation of stress responses on the posttranscriptional level (43)(44)(45)(46). Despite significant advancements in the field, our understanding of the complex regulatory networks and adaptive mechanisms employed by P. furiosus in response to extreme temperature variations remains limited, especially when considering the time-related aspects of these processes on the RNA and protein level.…”

Section: Introductionmentioning

confidence: 99%

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

Grünberger

Schmid

El-Ahmad

et al. 2023

Preprint

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Extremophiles, such as the hyperthermophilic archaeon Pyrococcus furiosus, thrive under extreme conditions and must rapidly adapt to changes in the physical parameters of their natural environment for short-term and long-term survival. When inhabiting hydrothermal vents, these organisms face substantial temperature gradients, necessitating the evolution of adaptive thermal stress mechanisms. However, the dynamics and coordination of cellular responses at the transcriptome and proteome levels remain underexplored. This study presents an integrated analysis of RNA-sequencing and mass spectrometry data to elucidate the transcriptomic and proteomic responses to heat and cold shock stress and recovery in P. furiosus. Our results reveal surprisingly rapid and dynamic changes in gene and protein expression patterns associated with these stress responses. Heat shock triggers extensive transcriptome reprogramming, orchestrated by the transcriptional regulator Phr, which targets 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 more sustained response. Intriguingly, cold shock at 4 °C elicits distinct short-term and long-term responses at both RNA and protein levels. By conducting a cluster analysis, we identified gene sets with either congruent or contrasting trends in RNA and protein changes. Notably, these clusters represent well-separated arCOG groups and appear to be tailored to their individual cellular responses. Our study provides a comprehensive overview of the cellular response to temperature stress, advancing our understanding of stress response mechanisms in hyperthermophilic archaea and provide valuable insights into the molecular adaptations that facilitate life in extreme environments.

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Section: Introductionmentioning

confidence: 99%

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

Grünberger

Schmid

El-Ahmad

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

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

Grünberger,

Schmid,

El Ahmad

et al. 2023

mBio

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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 4°C 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. IMPORTANCE Extreme environments provide unique challenges for life, and the study of extremophiles can shed light on the mechanisms of adaptation to such conditions. Pyrococcus furiosus , a hyperthermophilic archaeon, is a model organism for studying thermal stress response mechanisms. In this study, we used an integrated analysis of RNA-sequencing and mass spectrometry data to investigate the transcriptomic and proteomic responses of P. furiosus to heat and cold shock stress and recovery. Our results reveal the rapid and dynamic changes in gene and protein expression patterns associated with these stress responses, as well as the coordinated regulation of different gene sets in response to different stressors. These findings provide valuable insights into the molecular adaptations that facilitate life in extreme environments and advance our understanding of stress response mechanisms in hyperthermophilic archaea.

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Low Salt Influences Archaellum-Based Motility, Glycerol Metabolism, and Gas Vesicles Biogenesis in Halobacterium salinarum

2022

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Halobacterium salinarum NRC-1 is an extremophile that grows optimally at 4.3 M NaCl concentration. In spite of being an established model microorganism for the archaea domain, direct comparisons between its proteome and transcriptome during osmotic stress are still not available. Through RNA-seq-based transcriptomics, we compared a low salt (2.6 M NaCl) stress condition with 4.3 M of NaCl and found 283 differentially expressed loci. The more commonly found classes of genes were: ABC-type transporters and transcription factors. Similarities, and most importantly, differences between our findings and previously published datasets in similar experimental conditions are discussed. We validated three important biological processes differentially expressed: gas vesicles production (due to down-regulation of gvpA1b, gvpC1b, gvpN1b, and gvpO1b); archaellum formation (due to down-regulation of arlI, arlB1, arlB2, and arlB3); and glycerol metabolism (due to up-regulation of glpA1, glpB, and glpC). Direct comparison between transcriptomics and proteomics showed 58% agreement between mRNA and protein level changes, pointing to post-transcriptional regulation candidates. From those genes, we highlight rpl15e, encoding for the 50S ribosomal protein L15e, for which we hypothesize an ionic strength-dependent conformational change that guides post-transcriptional processing of its mRNA and, thus, possible salt-dependent regulation of the translation machinery.

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A genome-scale atlas reveals complex interplay of transcription and translation in an archaeon

Cited by 3 publications

References 118 publications

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

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

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

Low Salt Influences Archaellum-Based Motility, Glycerol Metabolism, and Gas Vesicles Biogenesis in Halobacterium salinarum

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