RNA sequencing and proteogenomics reveal the importance of leaderless mRNAs in the radiation-tolerant bacterium Deinococcus deserti
Deinococcus deserti is a desiccation- and radiation-tolerant desert bacterium. Differential RNA sequencing (RNA-seq) was performed to explore the specificities of its transcriptome. Strikingly, for 1,174 (60%) mRNAs, the transcription start site was found exactly at (916 cases, 47%) or very close to the translation initiation codon AUG or GUG. Such proportion of leaderless mRNAs, which may resemble ancestral mRNAs, is unprecedented for a bacterial species. Proteomics showed that leaderless mRNAs are efficiently translated in D. deserti. Interestingly, we also found 173 additional transcripts with a 5′-AUG or 5′-GUG that would make them competent for ribosome binding and translation into novel small polypeptides. Fourteen of these are predicted to be leader peptides involved in transcription attenuation. Another 30 correlated with new gene predictions and/or showed conservation with annotated and nonannotated genes in other Deinococcus species, and five of these novel polypeptides were indeed detected by mass spectrometry. The data also allowed reannotation of the start codon position of 257 genes, including several DNA repair genes. Moreover, several novel highly radiation-induced genes were found, and their potential roles are discussed. On the basis of our RNA-seq and proteogenomics data, we propose that translation of many of the novel leaderless transcripts, which may have resulted from single-nucleotide changes and maintained by selective pressure, provides a new explanation for the generation of a cellular pool of small peptides important for protection of proteins against oxidation and thus for radiation/desiccation tolerance and adaptation to harsh environmental conditions.
Main Authors: | , , , , , , , , |
---|---|
Format: | article biblioteca |
Language: | eng |
Online Access: | http://agritrop.cirad.fr/602176/ http://agritrop.cirad.fr/602176/1/Publi6.pdf |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
id |
dig-cirad-fr-602176 |
---|---|
record_format |
koha |
spelling |
dig-cirad-fr-6021762022-09-28T18:01:05Z http://agritrop.cirad.fr/602176/ http://agritrop.cirad.fr/602176/ RNA sequencing and proteogenomics reveal the importance of leaderless mRNAs in the radiation-tolerant bacterium Deinococcus deserti. De Groot Arjan, Roche David, Fernandez Bernard, Ludanyi Monika, Cruveiller Stéphane, Pignol David, Vallenet David, Armengaud Jean, Blanchard Laurence. 2014. Genome Biology and Evolution, 6 (4) : 932-948.https://doi.org/10.1093/gbe/evu069 <https://doi.org/10.1093/gbe/evu069> Researchers RNA sequencing and proteogenomics reveal the importance of leaderless mRNAs in the radiation-tolerant bacterium Deinococcus deserti De Groot, Arjan Roche, David Fernandez, Bernard Ludanyi, Monika Cruveiller, Stéphane Pignol, David Vallenet, David Armengaud, Jean Blanchard, Laurence eng 2014 Genome Biology and Evolution Deinococcus deserti is a desiccation- and radiation-tolerant desert bacterium. Differential RNA sequencing (RNA-seq) was performed to explore the specificities of its transcriptome. Strikingly, for 1,174 (60%) mRNAs, the transcription start site was found exactly at (916 cases, 47%) or very close to the translation initiation codon AUG or GUG. Such proportion of leaderless mRNAs, which may resemble ancestral mRNAs, is unprecedented for a bacterial species. Proteomics showed that leaderless mRNAs are efficiently translated in D. deserti. Interestingly, we also found 173 additional transcripts with a 5′-AUG or 5′-GUG that would make them competent for ribosome binding and translation into novel small polypeptides. Fourteen of these are predicted to be leader peptides involved in transcription attenuation. Another 30 correlated with new gene predictions and/or showed conservation with annotated and nonannotated genes in other Deinococcus species, and five of these novel polypeptides were indeed detected by mass spectrometry. The data also allowed reannotation of the start codon position of 257 genes, including several DNA repair genes. Moreover, several novel highly radiation-induced genes were found, and their potential roles are discussed. On the basis of our RNA-seq and proteogenomics data, we propose that translation of many of the novel leaderless transcripts, which may have resulted from single-nucleotide changes and maintained by selective pressure, provides a new explanation for the generation of a cellular pool of small peptides important for protection of proteins against oxidation and thus for radiation/desiccation tolerance and adaptation to harsh environmental conditions. article info:eu-repo/semantics/article Journal Article info:eu-repo/semantics/publishedVersion http://agritrop.cirad.fr/602176/1/Publi6.pdf text cc_by info:eu-repo/semantics/openAccess https://creativecommons.org/licenses/by/4.0/ https://doi.org/10.1093/gbe/evu069 10.1093/gbe/evu069 info:eu-repo/semantics/altIdentifier/doi/10.1093/gbe/evu069 info:eu-repo/semantics/altIdentifier/purl/https://doi.org/10.1093/gbe/evu069 |
institution |
CIRAD FR |
collection |
DSpace |
country |
Francia |
countrycode |
FR |
component |
Bibliográfico |
access |
En linea |
databasecode |
dig-cirad-fr |
tag |
biblioteca |
region |
Europa del Oeste |
libraryname |
Biblioteca del CIRAD Francia |
language |
eng |
description |
Deinococcus deserti is a desiccation- and radiation-tolerant desert bacterium. Differential RNA sequencing (RNA-seq) was performed to explore the specificities of its transcriptome. Strikingly, for 1,174 (60%) mRNAs, the transcription start site was found exactly at (916 cases, 47%) or very close to the translation initiation codon AUG or GUG. Such proportion of leaderless mRNAs, which may resemble ancestral mRNAs, is unprecedented for a bacterial species. Proteomics showed that leaderless mRNAs are efficiently translated in D. deserti. Interestingly, we also found 173 additional transcripts with a 5′-AUG or 5′-GUG that would make them competent for ribosome binding and translation into novel small polypeptides. Fourteen of these are predicted to be leader peptides involved in transcription attenuation. Another 30 correlated with new gene predictions and/or showed conservation with annotated and nonannotated genes in other Deinococcus species, and five of these novel polypeptides were indeed detected by mass spectrometry. The data also allowed reannotation of the start codon position of 257 genes, including several DNA repair genes. Moreover, several novel highly radiation-induced genes were found, and their potential roles are discussed. On the basis of our RNA-seq and proteogenomics data, we propose that translation of many of the novel leaderless transcripts, which may have resulted from single-nucleotide changes and maintained by selective pressure, provides a new explanation for the generation of a cellular pool of small peptides important for protection of proteins against oxidation and thus for radiation/desiccation tolerance and adaptation to harsh environmental conditions. |
format |
article |
author |
De Groot, Arjan Roche, David Fernandez, Bernard Ludanyi, Monika Cruveiller, Stéphane Pignol, David Vallenet, David Armengaud, Jean Blanchard, Laurence |
spellingShingle |
De Groot, Arjan Roche, David Fernandez, Bernard Ludanyi, Monika Cruveiller, Stéphane Pignol, David Vallenet, David Armengaud, Jean Blanchard, Laurence RNA sequencing and proteogenomics reveal the importance of leaderless mRNAs in the radiation-tolerant bacterium Deinococcus deserti |
author_facet |
De Groot, Arjan Roche, David Fernandez, Bernard Ludanyi, Monika Cruveiller, Stéphane Pignol, David Vallenet, David Armengaud, Jean Blanchard, Laurence |
author_sort |
De Groot, Arjan |
title |
RNA sequencing and proteogenomics reveal the importance of leaderless mRNAs in the radiation-tolerant bacterium Deinococcus deserti |
title_short |
RNA sequencing and proteogenomics reveal the importance of leaderless mRNAs in the radiation-tolerant bacterium Deinococcus deserti |
title_full |
RNA sequencing and proteogenomics reveal the importance of leaderless mRNAs in the radiation-tolerant bacterium Deinococcus deserti |
title_fullStr |
RNA sequencing and proteogenomics reveal the importance of leaderless mRNAs in the radiation-tolerant bacterium Deinococcus deserti |
title_full_unstemmed |
RNA sequencing and proteogenomics reveal the importance of leaderless mRNAs in the radiation-tolerant bacterium Deinococcus deserti |
title_sort |
rna sequencing and proteogenomics reveal the importance of leaderless mrnas in the radiation-tolerant bacterium deinococcus deserti |
url |
http://agritrop.cirad.fr/602176/ http://agritrop.cirad.fr/602176/1/Publi6.pdf |
work_keys_str_mv |
AT degrootarjan rnasequencingandproteogenomicsrevealtheimportanceofleaderlessmrnasintheradiationtolerantbacteriumdeinococcusdeserti AT rochedavid rnasequencingandproteogenomicsrevealtheimportanceofleaderlessmrnasintheradiationtolerantbacteriumdeinococcusdeserti AT fernandezbernard rnasequencingandproteogenomicsrevealtheimportanceofleaderlessmrnasintheradiationtolerantbacteriumdeinococcusdeserti AT ludanyimonika rnasequencingandproteogenomicsrevealtheimportanceofleaderlessmrnasintheradiationtolerantbacteriumdeinococcusdeserti AT cruveillerstephane rnasequencingandproteogenomicsrevealtheimportanceofleaderlessmrnasintheradiationtolerantbacteriumdeinococcusdeserti AT pignoldavid rnasequencingandproteogenomicsrevealtheimportanceofleaderlessmrnasintheradiationtolerantbacteriumdeinococcusdeserti AT vallenetdavid rnasequencingandproteogenomicsrevealtheimportanceofleaderlessmrnasintheradiationtolerantbacteriumdeinococcusdeserti AT armengaudjean rnasequencingandproteogenomicsrevealtheimportanceofleaderlessmrnasintheradiationtolerantbacteriumdeinococcusdeserti AT blanchardlaurence rnasequencingandproteogenomicsrevealtheimportanceofleaderlessmrnasintheradiationtolerantbacteriumdeinococcusdeserti |
_version_ |
1758027211835703296 |