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.

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Main Authors: De Groot, Arjan, Roche, David, Fernandez, Bernard, Ludanyi, Monika, Cruveiller, Stéphane, Pignol, David, Vallenet, David, Armengaud, Jean, Blanchard, Laurence
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Online Access:http://agritrop.cirad.fr/602176/
http://agritrop.cirad.fr/602176/1/Publi6.pdf
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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
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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
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