Bacterial tRNA 2′-O-methylation is dynamically regulated under stress conditions and modulates innate immune response

Abstract

Abstract RNA modifications are a well-recognized way of gene expression regulation at the post-transcriptional level. Despite the importance of this level of regulation, current knowledge on modulation of tRNA modification status in response to stress conditions is far from being complete. While it is widely accepted that tRNA modifications are rather dynamic, such variations are mostly assessed in terms of total tRNA, with only a few instances where changes could be traced to single isoacceptor species. Using Escherichia coli as a model system, we explored stress-induced modulation of 2′-O-methylations in tRNAs by RiboMethSeq. This analysis and orthogonal analytical measurements by LC-MS show substantial, but not uniform, increase of the Gm18 level in selected tRNAs under mild bacteriostatic antibiotic stress, while other Nm modifications remain relatively constant. The absence of Gm18 modification in tRNAs leads to moderate alterations in E. coli mRNA transcriptome, but does not affect polysomal association of mRNAs. Interestingly, the subset of motility/chemiotaxis genes is significantly overexpressed in ΔTrmH mutant, this corroborates with increased swarming motility of the mutant strain. The stress-induced increase of tRNA Gm18 level, in turn, reduced immunostimulation properties of bacterial tRNAs, which is concordant with the previous observation that Gm18 is a suppressor of Toll-like receptor 7 (TLR7)-mediated interferon release. This documents an effect of stress induced modulation of tRNA modification that acts outside protein translation.

Autoren

Adeline Galvanin
Lea-Marie Vogt
Antonia Grober
Isabel Freund
Lilia Ayadi
Valerie Bourguignon-Igel
Larissa Bessler
Dominik Jacob
Tatjana Eigenbrod
Virginie Marchand
Alexander Dalpke
Mark Helm
Yuri Motorin

DOI

10.1093/nar/gkaa1123

eISSN

1362-4962

ISSN

0305-1048

Ausgabe der Veröffentlichung

22

Zeitschrift

Nucleic Acids Research

Sprache

en

Online publication date

2020

Paginierung

12833 - 12844

Datum der Veröffentlichung

2020

Status

Published

Herausgeber

Oxford University Press (OUP)

Herausgeber URL

http://dx.doi.org/10.1093/nar/gkaa1123

Datum der Datenerfassung

2020

Titel

Bacterial tRNA 2′-O-methylation is dynamically regulated under stress conditions and modulates innate immune response

Ausgabe der Zeitschrift

48

Datenquelle: Crossref

Abstract

RNA modifications are a well-recognized way of gene expression regulation at the post-transcriptional level. Despite the importance of this level of regulation, current knowledge on modulation of tRNA modification status in response to stress conditions is far from being complete. While it is widely accepted that tRNA modifications are rather dynamic, such variations are mostly assessed in terms of total tRNA, with only a few instances where changes could be traced to single isoacceptor species. Using Escherichia coli as a model system, we explored stress-induced modulation of 2'-O-methylations in tRNAs by RiboMethSeq. This analysis and orthogonal analytical measurements by LC-MS show substantial, but not uniform, increase of the Gm18 level in selected tRNAs under mild bacteriostatic antibiotic stress, while other Nm modifications remain relatively constant. The absence of Gm18 modification in tRNAs leads to moderate alterations in E. coli mRNA transcriptome, but does not affect polysomal association of mRNAs. Interestingly, the subset of motility/chemiotaxis genes is significantly overexpressed in ΔTrmH mutant, this corroborates with increased swarming motility of the mutant strain. The stress-induced increase of tRNA Gm18 level, in turn, reduced immunostimulation properties of bacterial tRNAs, which is concordant with the previous observation that Gm18 is a suppressor of Toll-like receptor 7 (TLR7)-mediated interferon release. This documents an effect of stress induced modulation of tRNA modification that acts outside protein translation.

Addresses

Université de Lorraine, CNRS, IMoPA (UMR7365), F54000 Nancy, France.

Autoren

Adeline Galvanin
Lea-Marie Vogt
Antonia Grober
Isabel Freund
Lilia Ayadi
Valerie Bourguignon-Igel
Larissa Bessler
Dominik Jacob
Tatjana Eigenbrod
Virginie Marchand
Alexander Dalpke
Mark Helm
Yuri Motorin

DOI

10.1093/nar/gkaa1123

eISSN

1362-4962

Externe Identifier

PubMed Identifier: 33275131
PubMed Central ID: PMC7736821

Funding acknowledgements

EPITRAN COST: CA16120
Université de Lorraine:
Grand Est Region: DA592/7
Grand Est Region: SPP1784
Grand Est Region: HE 3397/18-1
Doctoral School ED BioSE (UL, Nancy) ‘Cotutelle’ PhD Fellowship:

Open access

true

ISSN

0305-1048

Ausgabe der Veröffentlichung

22

Zeitschrift

Nucleic acids research

Schlüsselwörter

Humans
Escherichia coli
Interferons
RNA, Transfer
Guanosine
Gene Expression Regulation
RNA Processing, Post-Transcriptional
Methylation
Toll-Like Receptor 7
Immunity, Innate

Sprache

eng

Medium

Print

Open access status

Open Access

Paginierung

12833 - 12844

Datum der Veröffentlichung

2020

Status

Published

Publisher licence

CC BY

Datum der Datenerfassung

2020

Titel

Bacterial tRNA 2'-O-methylation is dynamically regulated under stress conditions and modulates innate immune response.

Sub types

Research Support, Non-U.S. Gov't
research-article
Journal Article

Ausgabe der Zeitschrift

48

Files

https://academic.oup.com/nar/article-pdf/48/22/12833/34906124/gkaa1123.pdf https://europepmc.org/articles/PMC7736821?pdf=render

Datenquelle: Europe PubMed Central

Abstract

RNA modifications are a well-recognized way of gene expression regulation at the post-transcriptional level. Despite the importance of this level of regulation, current knowledge on modulation of tRNA modification status in response to stress conditions is far from being complete. While it is widely accepted that tRNA modifications are rather dynamic, such variations are mostly assessed in terms of total tRNA, with only a few instances where changes could be traced to single isoacceptor species. Using Escherichia coli as a model system, we explored stress-induced modulation of 2'-O-methylations in tRNAs by RiboMethSeq. This analysis and orthogonal analytical measurements by LC-MS show substantial, but not uniform, increase of the Gm18 level in selected tRNAs under mild bacteriostatic antibiotic stress, while other Nm modifications remain relatively constant. The absence of Gm18 modification in tRNAs leads to moderate alterations in E. coli mRNA transcriptome, but does not affect polysomal association of mRNAs. Interestingly, the subset of motility/chemiotaxis genes is significantly overexpressed in ΔTrmH mutant, this corroborates with increased swarming motility of the mutant strain. The stress-induced increase of tRNA Gm18 level, in turn, reduced immunostimulation properties of bacterial tRNAs, which is concordant with the previous observation that Gm18 is a suppressor of Toll-like receptor 7 (TLR7)-mediated interferon release. This documents an effect of stress induced modulation of tRNA modification that acts outside protein translation.

Date of acceptance

2020

Autoren

Adeline Galvanin
Lea-Marie Vogt
Antonia Grober
Isabel Freund
Lilia Ayadi
Valerie Bourguignon-Igel
Larissa Bessler
Dominik Jacob
Tatjana Eigenbrod
Virginie Marchand
Alexander Dalpke
Mark Helm
Yuri Motorin

Autoren-URL

https://www.ncbi.nlm.nih.gov/pubmed/33275131

DOI

10.1093/nar/gkaa1123

eISSN

1362-4962

Externe Identifier

PubMed Central ID: PMC7736821

Ausgabe der Veröffentlichung

22

Zeitschrift

Nucleic Acids Res

Schlüsselwörter

Escherichia coli
Gene Expression Regulation
Guanosine
Humans
Immunity, Innate
Interferons
Methylation
RNA Processing, Post-Transcriptional
RNA, Transfer
Toll-Like Receptor 7

Sprache

eng

Country

England

Paginierung

12833 - 12844

PII

6020192

Datum der Veröffentlichung

2020

Status

Published

Datum, an dem der Datensatz öffentlich gemacht wurde

2021

Titel

Bacterial tRNA 2'-O-methylation is dynamically regulated under stress conditions and modulates innate immune response.

Sub types

Journal Article
Research Support, Non-U.S. Gov't

Ausgabe der Zeitschrift

48

Datenquelle: PubMed

Bacterial tRNA 2′-O-methylation is dynamically regulated under stress conditions and modulates innate immune response

Files

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