The 3'UTR-derived sRNA RsaG coordinates redox homeostasis and metabolism adaptation in response to glucose-6- phosphate uptake in Staphylococcus aureus
Staphylococcus aureus RsaG is a 3′-untranslated region (3′UTR) derived sRNA from the conserved uhpT gene encoding a glucose-6-phosphate (G6P) transporter expressed in response to extracellular G6P. The transcript uhpT-RsaG undergoes degradation from 5′- to 3′-end by the action of the exoribonucleases J1/J2, which are blocked by a stable hairpin structure at the 5′-end of RsaG, leading to its accumulation. RsaG together with uhpT is induced when bacteria are internalized into host cells or in the presence of mucus-secreting cells. Using MS2-affinity purification coupled with RNA sequencing, several RNAs were identified as targets including mRNAs encoding the transcriptional factors Rex, CcpA, SarA, and the sRNA RsaI. Our data suggested that RsaG contributes to the control of redox homeostasis and adjusts metabolism to changing environmental conditions. RsaG uses different molecular mechanisms to stabilize, degrade, or repress the translation of its mRNA targets. Although RsaG is conserved only in closely related species, the uhpT 3′UTR of the ape pathogen S. simiae harbors an sRNA, whose sequence is highly different, and which does not respond to G6P levels. Our results hypothesized that the 3′UTRs from UhpT transporter encoding mRNAs could have rapidly evolved to enable adaptation to host niches.
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Format: | artículo biblioteca |
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Wiley-Blackwell
2022-01
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Subjects: | 3′UTR-derived sRNA, Redox homeostasis, Staphylococcus aureus, |
Online Access: | http://hdl.handle.net/10261/283125 http://dx.doi.org/10.13039/501100001665 http://dx.doi.org/10.13039/501100004794 http://dx.doi.org/10.13039/501100002915 http://dx.doi.org/10.13039/501100003768 |
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dig-idab-es-10261-2831252022-11-18T02:46:30Z The 3'UTR-derived sRNA RsaG coordinates redox homeostasis and metabolism adaptation in response to glucose-6- phosphate uptake in Staphylococcus aureus Desgranges, Emma Barrientos, Laura Herrgott, Lucas Marzi, Stefano Toledo-Arana, Alejandro Moreau, Karan Vandenesch, François Romby, Pascale Caldelari, Isabelle Centre National de la Recherche Scientifique (France) Agence Nationale de la Recherche (France) Université de Strasbourg Fondation pour la Recherche Médicale 3′UTR-derived sRNA Redox homeostasis Staphylococcus aureus Staphylococcus aureus RsaG is a 3′-untranslated region (3′UTR) derived sRNA from the conserved uhpT gene encoding a glucose-6-phosphate (G6P) transporter expressed in response to extracellular G6P. The transcript uhpT-RsaG undergoes degradation from 5′- to 3′-end by the action of the exoribonucleases J1/J2, which are blocked by a stable hairpin structure at the 5′-end of RsaG, leading to its accumulation. RsaG together with uhpT is induced when bacteria are internalized into host cells or in the presence of mucus-secreting cells. Using MS2-affinity purification coupled with RNA sequencing, several RNAs were identified as targets including mRNAs encoding the transcriptional factors Rex, CcpA, SarA, and the sRNA RsaI. Our data suggested that RsaG contributes to the control of redox homeostasis and adjusts metabolism to changing environmental conditions. RsaG uses different molecular mechanisms to stabilize, degrade, or repress the translation of its mRNA targets. Although RsaG is conserved only in closely related species, the uhpT 3′UTR of the ape pathogen S. simiae harbors an sRNA, whose sequence is highly different, and which does not respond to G6P levels. Our results hypothesized that the 3′UTRs from UhpT transporter encoding mRNAs could have rapidly evolved to enable adaptation to host niches. This work was supported by the Centre National de la Recherche Scientifique (CNRS), by the French National Research Agency ANR (ANR-18-CE12-0025-04 CoNoCo to P.R.). This work of the Interdisciplinary Thematic Institute IMCBio, as part of the ITI 2021–2028 program of the University of Strasbourg, CNRS, and Inserm was supported by IdEx Unistra (ANR-10-IDEX-0002), SFRI-STRAT'US (ANR 20-SFRI-0012), and by EUR IMCBio (IMCBio ANR-17-EURE-0023) under the framework of the French Investments for the Future Program. ED and LB were supported by the “Fondation pour la Recherche Médicale” (FDT201904007957 and ECO202006011534) 2022-11-17T11:30:13Z 2022-11-17T11:30:13Z 2022-01 2022-11-17T11:30:13Z artículo doi: 10.1111/mmi.14845 issn: 0950-382X e-issn: 1365-2958 Molecular Microbiology 117: 193-214 (2022) http://hdl.handle.net/10261/283125 10.1111/mmi.14845 http://dx.doi.org/10.13039/501100001665 http://dx.doi.org/10.13039/501100004794 http://dx.doi.org/10.13039/501100002915 http://dx.doi.org/10.13039/501100003768 http://dx.doi.org/10.1111/mmi.14845 Sí none Wiley-Blackwell |
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3′UTR-derived sRNA Redox homeostasis Staphylococcus aureus 3′UTR-derived sRNA Redox homeostasis Staphylococcus aureus |
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3′UTR-derived sRNA Redox homeostasis Staphylococcus aureus 3′UTR-derived sRNA Redox homeostasis Staphylococcus aureus Desgranges, Emma Barrientos, Laura Herrgott, Lucas Marzi, Stefano Toledo-Arana, Alejandro Moreau, Karan Vandenesch, François Romby, Pascale Caldelari, Isabelle The 3'UTR-derived sRNA RsaG coordinates redox homeostasis and metabolism adaptation in response to glucose-6- phosphate uptake in Staphylococcus aureus |
description |
Staphylococcus aureus RsaG is a 3′-untranslated region (3′UTR) derived sRNA from the conserved uhpT gene encoding a glucose-6-phosphate (G6P) transporter expressed in response to extracellular G6P. The transcript uhpT-RsaG undergoes degradation from 5′- to 3′-end by the action of the exoribonucleases J1/J2, which are blocked by a stable hairpin structure at the 5′-end of RsaG, leading to its accumulation. RsaG together with uhpT is induced when bacteria are internalized into host cells or in the presence of mucus-secreting cells. Using MS2-affinity purification coupled with RNA sequencing, several RNAs were identified as targets including mRNAs encoding the transcriptional factors Rex, CcpA, SarA, and the sRNA RsaI. Our data suggested that RsaG contributes to the control of redox homeostasis and adjusts metabolism to changing environmental conditions. RsaG uses different molecular mechanisms to stabilize, degrade, or repress the translation of its mRNA targets. Although RsaG is conserved only in closely related species, the uhpT 3′UTR of the ape pathogen S. simiae harbors an sRNA, whose sequence is highly different, and which does not respond to G6P levels. Our results hypothesized that the 3′UTRs from UhpT transporter encoding mRNAs could have rapidly evolved to enable adaptation to host niches. |
author2 |
Centre National de la Recherche Scientifique (France) |
author_facet |
Centre National de la Recherche Scientifique (France) Desgranges, Emma Barrientos, Laura Herrgott, Lucas Marzi, Stefano Toledo-Arana, Alejandro Moreau, Karan Vandenesch, François Romby, Pascale Caldelari, Isabelle |
format |
artículo |
topic_facet |
3′UTR-derived sRNA Redox homeostasis Staphylococcus aureus |
author |
Desgranges, Emma Barrientos, Laura Herrgott, Lucas Marzi, Stefano Toledo-Arana, Alejandro Moreau, Karan Vandenesch, François Romby, Pascale Caldelari, Isabelle |
author_sort |
Desgranges, Emma |
title |
The 3'UTR-derived sRNA RsaG coordinates redox homeostasis and metabolism adaptation in response to glucose-6- phosphate uptake in Staphylococcus aureus |
title_short |
The 3'UTR-derived sRNA RsaG coordinates redox homeostasis and metabolism adaptation in response to glucose-6- phosphate uptake in Staphylococcus aureus |
title_full |
The 3'UTR-derived sRNA RsaG coordinates redox homeostasis and metabolism adaptation in response to glucose-6- phosphate uptake in Staphylococcus aureus |
title_fullStr |
The 3'UTR-derived sRNA RsaG coordinates redox homeostasis and metabolism adaptation in response to glucose-6- phosphate uptake in Staphylococcus aureus |
title_full_unstemmed |
The 3'UTR-derived sRNA RsaG coordinates redox homeostasis and metabolism adaptation in response to glucose-6- phosphate uptake in Staphylococcus aureus |
title_sort |
3'utr-derived srna rsag coordinates redox homeostasis and metabolism adaptation in response to glucose-6- phosphate uptake in staphylococcus aureus |
publisher |
Wiley-Blackwell |
publishDate |
2022-01 |
url |
http://hdl.handle.net/10261/283125 http://dx.doi.org/10.13039/501100001665 http://dx.doi.org/10.13039/501100004794 http://dx.doi.org/10.13039/501100002915 http://dx.doi.org/10.13039/501100003768 |
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