Ribosome Profiling of <italic toggle="yes">Synechocystis</italic> Reveals Altered Ribosome Allocation at Carbon Starvation

ABSTRACT Cyanobacteria experience both rapid and periodic fluctuations in light and inorganic carbon (Ci) and have evolved regulatory mechanisms to respond to these, including extensive posttranscriptional gene regulation. We report the first genome-wide ribosome profiling data set for cyanobacteria...

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Autores principales:	Jan Karlsen, Johannes Asplund-Samuelsson, Quentin Thomas, Michael Jahn, Elton P. Hudson
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	cyanobacteria gene regulation light stress translational control Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d03cde2239e942c3acf0b88cd89af540
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spelling	oai:doaj.org-article:d03cde2239e942c3acf0b88cd89af5402021-12-02T18:15:43ZRibosome Profiling of <italic toggle="yes">Synechocystis</italic> Reveals Altered Ribosome Allocation at Carbon Starvation10.1128/mSystems.00126-182379-5077https://doaj.org/article/d03cde2239e942c3acf0b88cd89af5402018-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00126-18https://doaj.org/toc/2379-5077ABSTRACT Cyanobacteria experience both rapid and periodic fluctuations in light and inorganic carbon (Ci) and have evolved regulatory mechanisms to respond to these, including extensive posttranscriptional gene regulation. We report the first genome-wide ribosome profiling data set for cyanobacteria, where ribosome occupancy on mRNA is quantified with codon-level precision. We measured the transcriptome and translatome of Synechocystis during autotrophic growth before (high carbon [HC] condition) and 24 h after removing CO2 from the feedgas (low carbon [LC] condition). Ribosome occupancy patterns in the 5′ untranslated region suggest that ribosomes can assemble there and slide to the Shine-Dalgarno site, where they pause. At LC, total translation was reduced by 80% and ribosome pausing was increased at stop and start codons and in untranslated regions, which may be a sequestration mechanism to inactivate ribosomes in response to rapid Ci depletion. Several stress response genes, such as thioredoxin M (sll1057), a putative endonuclease (slr0915), protease HtrA (slr1204), and heat shock protein HspA (sll1514) showed marked increases in translational efficiency at LC, indicating translational control in response to Ci depletion. Ribosome pause scores within open reading frames were mostly constant, though several ribosomal proteins had significantly altered pause score distributions at LC, which might indicate translational regulation of ribosome biosynthesis in response to Ci depletion. We show that ribosome profiling is a powerful tool to decipher dynamic gene regulation strategies in cyanobacteria. IMPORTANCE Ribosome profiling accesses the translational step of gene expression via deep sequencing of ribosome-protected mRNA footprints. Pairing of ribosome profiling and transcriptomics data provides a translational efficiency for each gene. Here, the translatome and transcriptome of the model cyanobacterium Synechocystis were compared under carbon-replete and carbon starvation conditions. The latter may be experienced when cyanobacteria are cultivated in poorly mixed bioreactors or engineered to be product-secreting cell factories. A small fraction of genes (<200), including stress response genes, showed changes in translational efficiency during carbon starvation, indicating condition-dependent translation-level regulation. We observed ribosome occupancy in untranslated regions, possibly due to an alternative translation initiation mechanism in Synechocystis. The higher proportion of ribosomes residing in untranslated regions during carbon starvation may be a mechanism to quickly inactivate superfluous ribosomes. This work provides the first ribosome profiling data for cyanobacteria and reveals new regulation strategies for coping with nutrient limitation.Jan KarlsenJohannes Asplund-SamuelssonQuentin ThomasMichael JahnElton P. HudsonAmerican Society for Microbiologyarticlecyanobacteriagene regulationlight stresstranslational controlMicrobiologyQR1-502ENmSystems, Vol 3, Iss 5 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	cyanobacteria gene regulation light stress translational control Microbiology QR1-502
spellingShingle	cyanobacteria gene regulation light stress translational control Microbiology QR1-502 Jan Karlsen Johannes Asplund-Samuelsson Quentin Thomas Michael Jahn Elton P. Hudson Ribosome Profiling of <italic toggle="yes">Synechocystis</italic> Reveals Altered Ribosome Allocation at Carbon Starvation
description	ABSTRACT Cyanobacteria experience both rapid and periodic fluctuations in light and inorganic carbon (Ci) and have evolved regulatory mechanisms to respond to these, including extensive posttranscriptional gene regulation. We report the first genome-wide ribosome profiling data set for cyanobacteria, where ribosome occupancy on mRNA is quantified with codon-level precision. We measured the transcriptome and translatome of Synechocystis during autotrophic growth before (high carbon [HC] condition) and 24 h after removing CO2 from the feedgas (low carbon [LC] condition). Ribosome occupancy patterns in the 5′ untranslated region suggest that ribosomes can assemble there and slide to the Shine-Dalgarno site, where they pause. At LC, total translation was reduced by 80% and ribosome pausing was increased at stop and start codons and in untranslated regions, which may be a sequestration mechanism to inactivate ribosomes in response to rapid Ci depletion. Several stress response genes, such as thioredoxin M (sll1057), a putative endonuclease (slr0915), protease HtrA (slr1204), and heat shock protein HspA (sll1514) showed marked increases in translational efficiency at LC, indicating translational control in response to Ci depletion. Ribosome pause scores within open reading frames were mostly constant, though several ribosomal proteins had significantly altered pause score distributions at LC, which might indicate translational regulation of ribosome biosynthesis in response to Ci depletion. We show that ribosome profiling is a powerful tool to decipher dynamic gene regulation strategies in cyanobacteria. IMPORTANCE Ribosome profiling accesses the translational step of gene expression via deep sequencing of ribosome-protected mRNA footprints. Pairing of ribosome profiling and transcriptomics data provides a translational efficiency for each gene. Here, the translatome and transcriptome of the model cyanobacterium Synechocystis were compared under carbon-replete and carbon starvation conditions. The latter may be experienced when cyanobacteria are cultivated in poorly mixed bioreactors or engineered to be product-secreting cell factories. A small fraction of genes (<200), including stress response genes, showed changes in translational efficiency during carbon starvation, indicating condition-dependent translation-level regulation. We observed ribosome occupancy in untranslated regions, possibly due to an alternative translation initiation mechanism in Synechocystis. The higher proportion of ribosomes residing in untranslated regions during carbon starvation may be a mechanism to quickly inactivate superfluous ribosomes. This work provides the first ribosome profiling data for cyanobacteria and reveals new regulation strategies for coping with nutrient limitation.
format	article
author	Jan Karlsen Johannes Asplund-Samuelsson Quentin Thomas Michael Jahn Elton P. Hudson
author_facet	Jan Karlsen Johannes Asplund-Samuelsson Quentin Thomas Michael Jahn Elton P. Hudson
author_sort	Jan Karlsen
title	Ribosome Profiling of <italic toggle="yes">Synechocystis</italic> Reveals Altered Ribosome Allocation at Carbon Starvation
title_short	Ribosome Profiling of <italic toggle="yes">Synechocystis</italic> Reveals Altered Ribosome Allocation at Carbon Starvation
title_full	Ribosome Profiling of <italic toggle="yes">Synechocystis</italic> Reveals Altered Ribosome Allocation at Carbon Starvation
title_fullStr	Ribosome Profiling of <italic toggle="yes">Synechocystis</italic> Reveals Altered Ribosome Allocation at Carbon Starvation
title_full_unstemmed	Ribosome Profiling of <italic toggle="yes">Synechocystis</italic> Reveals Altered Ribosome Allocation at Carbon Starvation
title_sort	ribosome profiling of <italic toggle="yes">synechocystis</italic> reveals altered ribosome allocation at carbon starvation
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/d03cde2239e942c3acf0b88cd89af540
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Ribosome Profiling of <italic toggle="yes">Synechocystis</italic> Reveals Altered Ribosome Allocation at Carbon Starvation

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