Selective Translation of Low Abundance and Upregulated Transcripts in <named-content content-type="genus-species">Halobacterium salinarum</named-content>

ABSTRACT When organisms encounter an unfavorable environment, they transition to a physiologically distinct, quiescent state wherein abundant transcripts from the previous active growth state continue to persist, albeit their active transcription is downregulated. In order to generate proteins for t...

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Autores principales:	Adrián López García de Lomana, Ulrike Kusebauch, Arjun V. Raman, Min Pan, Serdar Turkarslan, Alan P. R. Lorenzetti, Robert L. Moritz, Nitin S. Baliga
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	translational regulation selective translation transcription-translation interplay ribosome heterogeneity transcriptomics ribosome profiling Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/afdd33dca81b494c9cf8fa5d14208085
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spelling	oai:doaj.org-article:afdd33dca81b494c9cf8fa5d142080852021-12-02T19:47:35ZSelective Translation of Low Abundance and Upregulated Transcripts in <named-content content-type="genus-species">Halobacterium salinarum</named-content>10.1128/mSystems.00329-202379-5077https://doaj.org/article/afdd33dca81b494c9cf8fa5d142080852020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00329-20https://doaj.org/toc/2379-5077ABSTRACT When organisms encounter an unfavorable environment, they transition to a physiologically distinct, quiescent state wherein abundant transcripts from the previous active growth state continue to persist, albeit their active transcription is downregulated. In order to generate proteins for the new quiescent physiological state, we hypothesized that the translation machinery must selectively translate upregulated transcripts in an intracellular milieu crowded with considerably higher abundance transcripts from the previous active growth state. Here, we have analyzed genome-wide changes in the transcriptome (RNA sequencing [RNA-seq]), changes in translational regulation and efficiency by ribosome profiling across all transcripts (ribosome profiling [Ribo-seq]), and protein level changes in assembled ribosomal proteins (sequential window acquisition of all theoretical mass spectra [SWATH-MS]) to investigate the interplay of transcriptional and translational regulation in Halobacterium salinarum as it transitions from active growth to quiescence. We have discovered that interplay of regulatory processes at different levels of information processing generates condition-specific ribosomal complexes to translate preferentially pools of low abundance and upregulated transcripts. Through analysis of the gene regulatory network architecture of H. salinarum, Escherichia coli, and Saccharomyces cerevisiae, we demonstrate that this conditional, modular organization of regulatory programs governing translational systems is a generalized feature across all domains of life. IMPORTANCE Our findings demonstrate conclusively that low abundance and upregulated transcripts are preferentially translated, potentially by environment-specific translation systems with distinct ribosomal protein composition. We show that a complex interplay of transcriptional and posttranscriptional regulation underlies the conditional and modular regulatory programs that generate ribosomes of distinct protein composition. The modular regulation of ribosomal proteins with other transcription, translation, and metabolic genes is generalizable to bacterial and eukaryotic microbes. These findings are relevant to how microorganisms adapt to unfavorable environments when they transition from active growth to quiescence by generating proteins from upregulated transcripts that are in considerably lower abundance relative to transcripts associated with the previous physiological state. Selective translation of transcripts by distinct ribosomes could form the basis for adaptive evolution to new environments through a modular regulation of the translational systems.Adrián López García de LomanaUlrike KusebauchArjun V. RamanMin PanSerdar TurkarslanAlan P. R. LorenzettiRobert L. MoritzNitin S. BaligaAmerican Society for Microbiologyarticletranslational regulationselective translationtranscription-translation interplayribosome heterogeneitytranscriptomicsribosome profilingMicrobiologyQR1-502ENmSystems, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	translational regulation selective translation transcription-translation interplay ribosome heterogeneity transcriptomics ribosome profiling Microbiology QR1-502
spellingShingle	translational regulation selective translation transcription-translation interplay ribosome heterogeneity transcriptomics ribosome profiling Microbiology QR1-502 Adrián López García de Lomana Ulrike Kusebauch Arjun V. Raman Min Pan Serdar Turkarslan Alan P. R. Lorenzetti Robert L. Moritz Nitin S. Baliga Selective Translation of Low Abundance and Upregulated Transcripts in <named-content content-type="genus-species">Halobacterium salinarum</named-content>
description	ABSTRACT When organisms encounter an unfavorable environment, they transition to a physiologically distinct, quiescent state wherein abundant transcripts from the previous active growth state continue to persist, albeit their active transcription is downregulated. In order to generate proteins for the new quiescent physiological state, we hypothesized that the translation machinery must selectively translate upregulated transcripts in an intracellular milieu crowded with considerably higher abundance transcripts from the previous active growth state. Here, we have analyzed genome-wide changes in the transcriptome (RNA sequencing [RNA-seq]), changes in translational regulation and efficiency by ribosome profiling across all transcripts (ribosome profiling [Ribo-seq]), and protein level changes in assembled ribosomal proteins (sequential window acquisition of all theoretical mass spectra [SWATH-MS]) to investigate the interplay of transcriptional and translational regulation in Halobacterium salinarum as it transitions from active growth to quiescence. We have discovered that interplay of regulatory processes at different levels of information processing generates condition-specific ribosomal complexes to translate preferentially pools of low abundance and upregulated transcripts. Through analysis of the gene regulatory network architecture of H. salinarum, Escherichia coli, and Saccharomyces cerevisiae, we demonstrate that this conditional, modular organization of regulatory programs governing translational systems is a generalized feature across all domains of life. IMPORTANCE Our findings demonstrate conclusively that low abundance and upregulated transcripts are preferentially translated, potentially by environment-specific translation systems with distinct ribosomal protein composition. We show that a complex interplay of transcriptional and posttranscriptional regulation underlies the conditional and modular regulatory programs that generate ribosomes of distinct protein composition. The modular regulation of ribosomal proteins with other transcription, translation, and metabolic genes is generalizable to bacterial and eukaryotic microbes. These findings are relevant to how microorganisms adapt to unfavorable environments when they transition from active growth to quiescence by generating proteins from upregulated transcripts that are in considerably lower abundance relative to transcripts associated with the previous physiological state. Selective translation of transcripts by distinct ribosomes could form the basis for adaptive evolution to new environments through a modular regulation of the translational systems.
format	article
author	Adrián López García de Lomana Ulrike Kusebauch Arjun V. Raman Min Pan Serdar Turkarslan Alan P. R. Lorenzetti Robert L. Moritz Nitin S. Baliga
author_facet	Adrián López García de Lomana Ulrike Kusebauch Arjun V. Raman Min Pan Serdar Turkarslan Alan P. R. Lorenzetti Robert L. Moritz Nitin S. Baliga
author_sort	Adrián López García de Lomana
title	Selective Translation of Low Abundance and Upregulated Transcripts in <named-content content-type="genus-species">Halobacterium salinarum</named-content>
title_short	Selective Translation of Low Abundance and Upregulated Transcripts in <named-content content-type="genus-species">Halobacterium salinarum</named-content>
title_full	Selective Translation of Low Abundance and Upregulated Transcripts in <named-content content-type="genus-species">Halobacterium salinarum</named-content>
title_fullStr	Selective Translation of Low Abundance and Upregulated Transcripts in <named-content content-type="genus-species">Halobacterium salinarum</named-content>
title_full_unstemmed	Selective Translation of Low Abundance and Upregulated Transcripts in <named-content content-type="genus-species">Halobacterium salinarum</named-content>
title_sort	selective translation of low abundance and upregulated transcripts in <named-content content-type="genus-species">halobacterium salinarum</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/afdd33dca81b494c9cf8fa5d14208085
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Selective Translation of Low Abundance and Upregulated Transcripts in <named-content content-type="genus-species">Halobacterium salinarum</named-content>

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