Dataset Information

RNA sequencing and proteogenomics reveal the importance of leaderless mRNAs in the radiation-tolerant bacterium Deinococcus deserti.

ABSTRACT: 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.

SUBMITTER: de Groot A

PROVIDER: S-EPMC4007540 | biostudies-literature | 2014 Apr

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

RNA sequencing and proteogenomics reveal the importance of leaderless mRNAs in the radiation-tolerant bacterium Deinococcus deserti.

de Groot Arjan A Roche David D Fernandez Bernard B Ludanyi Monika M Cruveiller Stéphane S Pignol David D Vallenet David D Armengaud Jean J Blanchard Laurence L

Genome biology and evolution 20140401 4

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 ...[more]

PMID: 24723731

Similar Datasets

Project description:Environmental DNA uptake by certain bacteria and its integration into their genome create genetic diversity and new phenotypes. DNA processing protein A (DprA) is part of a multiprotein complex and facilitates the natural transformation (NT) phenotype in most bacteria. Deinococcus radiodurans, an extremely radioresistant bacterium, is efficient in NT, and its genome encodes nearly all of the components of the natural competence complex. Here, we have characterized the DprA protein of this bacterium (DrDprA) for the known characteristics of DprA proteins of other bacteria and the mechanisms underlying the DNA-RecA interaction. DrDprA has three domains. In vitro studies showed that purified recombinant DrDprA binds to both single-strand DNA (ssDNA) and double-strand DNA (dsDNA) and is able to protect ssDNA from nucleolytic degradation. DrDprA showed a strong interaction with DrRecA and facilitated RecA-catalyzed functions in vivo. Mutational studies identified DrDprA amino acid residues crucial for oligomerization, the interaction with DrRecA, and DNA binding. Furthermore, we showed that both oligomerization and DNA binding properties of DrDprA are integral to its support of the DrRecA-catalyzed strand exchange reaction (SER) in vitro. Together, these data suggested that DrDprA is largely structurally conserved with other DprA homologs but shows some unique structure-function features like the existence of an additional C-terminal Drosophila melanogaster Miasto-like protein 1 (DML1) domain, equal affinities for ssDNA and dsDNA, and the collective roles of oligomerization and DNA binding properties in supporting DrRecA functions. IMPORTANCE Bacteria can take up extracellular DNA (eDNA) by natural transformation (NT). Many bacteria, including Deinococcus radiodurans, have constitutive competence systems and can take up eDNA throughout their growth phase. DprA (DNA processing protein A) is a transformation-specific recombination mediator protein (RMP) that plays a role in bacterial NT, and the absence of this gene significantly reduces the transformation efficiencies of both chromosomal and plasmid DNA. NT helps bacteria survive under adverse conditions and contributes to genetic diversity in bacteria. The present work describes the characterization of DprA from D. radiodurans and will add to the existing knowledge of DprA biology.

Dataset Information

RNA sequencing and proteogenomics reveal the importance of leaderless mRNAs in the radiation-tolerant bacterium Deinococcus deserti.

Publications

RNA sequencing and proteogenomics reveal the importance of leaderless mRNAs in the radiation-tolerant bacterium Deinococcus deserti.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets