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Transcriptional Frameshifting Rescues Citrobacter rodentium Type VI Secretion by the Production of Two Length Variants from the Prematurely Interrupted tssM Gene
- Source :
- PLoS Genetics, PLoS Genetics, Public Library of Science, 2014, 10 ( e1004869 ), ⟨10.1371/journal.pgen.1004869⟩, PLoS Genetics, Vol 10, Iss 12, p e1004869 (2014), PLoS Genetics, 2014, 10 ( e1004869 ), ⟨10.1371/journal.pgen.1004869⟩
- Publication Year :
- 2014
- Publisher :
- HAL CCSD, 2014.
-
Abstract
- The Type VI secretion system (T6SS) mediates toxin delivery into both eukaryotic and prokaryotic cells. It is composed of a cytoplasmic structure resembling the tail of contractile bacteriophages anchored to the cell envelope through a membrane complex composed of the TssL and TssM inner membrane proteins and of the TssJ outer membrane lipoprotein. The C-terminal domain of TssM is required for its interaction with TssJ, and for the function of the T6SS. In Citrobacter rodentium, the tssM1 gene does not encode the C-terminal domain. However, the stop codon is preceded by a run of 11 consecutive adenosines. In this study, we demonstrate that this poly-A tract is a transcriptional slippery site that induces the incorporation of additional adenosines, leading to frameshifting, and hence the production of two TssM1 variants, including a full-length canonical protein. We show that both forms of TssM1, and the ratio between these two forms, are required for the function of the T6SS in C. rodentium. Finally, we demonstrate that the tssM gene associated with the Yersinia pseudotuberculosis T6SS-3 gene cluster is also subjected to transcriptional frameshifting.<br />Author Summary Nonstandard decoding mechanisms lead to the synthesis of different protein variants from a single DNA sequence. These mechanisms are particularly important when the genome length has to be limited such as viral genomes, limited by the available space in the capsid, or to synthesize two different polypeptides that have distinct functional properties. Here, we report that tssM, a gene encoded within the Citrobacter rodentium Type VI secretion (T6S) gene cluster, is interrupted by a premature stop codon; however, the stop codon is preceded by a slippery site constituted by 11 consecutive adenosines. Reiterative transcription leads to the incorporation of additional nucleotides in the mRNA and therefore restores the original framing. As a consequence, two different TssM variants are created by transcriptional frameshifting, including a full-length 130-kDa protein and an 88-kDa truncated variant. We further show that both forms, and the ratio between these two forms, are required for the function of the transport apparatus. Interestingly, a similar mechanism regulates the synthesis of two TssM variants in Yersinia pseudotuberculosis.
- Subjects :
- System
Cancer Research
Target cells
TRANSLATIONAL FRAMESHIFT
Gene Identification and Analysis
PROTEIN
Shigella flexneri
Suppression, Genetic
Gene cluster
Citrobacter rodentium
Protein Isoforms
Frameshift Mutation
Bacterial Secretion Systems
Translational frameshift
Genetics (clinical)
0303 health sciences
Interbacterial competition
Slippage
ENTEROAGGREGATIVE ESCHERICHIA-COLI
INTERBACTERIAL COMPETITION
Enteroaggregative Escherichia coli
Bacterial Pathogens
Medical Microbiology
Codon, Nonsense
EFFECTORS
Bacterial outer membrane
Research Article
lcsh:QH426-470
DNA transcription
Molecular Sequence Data
Biology
Microbiology
Molecular Genetics
03 medical and health sciences
Bacterial Proteins
Microbial Control
Genetics
Inner membrane
Secretion
Amino Acid Sequence
Gram Negative Bacteria
Microbial Pathogens
Molecular Biology
Gene
Ecology, Evolution, Behavior and Systematics
030304 developmental biology
Type VI secretion system
SHIGELLA-FLEXNERI
Evolutionary Biology
[SDV.GEN]Life Sciences [q-bio]/Genetics
Biology and life sciences
Base Sequence
Organisms, Genetically Modified
030306 microbiology
Protein
Membrane Proteins
Bacteriology
Sequence Analysis, DNA
AGROBACTERIUM-TUMEFACIENS
Effectors
Molecular biology
Organismal Evolution
Gene regulation
lcsh:Genetics
SLIPPAGE
Agrobacterium tumefaciens
Microbial Evolution
TARGET-CELLS
Gene expression
Gene Function
SYSTEM
Subjects
Details
- Language :
- English
- ISSN :
- 15537390 and 15537404
- Database :
- OpenAIRE
- Journal :
- PLoS Genetics, PLoS Genetics, Public Library of Science, 2014, 10 ( e1004869 ), ⟨10.1371/journal.pgen.1004869⟩, PLoS Genetics, Vol 10, Iss 12, p e1004869 (2014), PLoS Genetics, 2014, 10 ( e1004869 ), ⟨10.1371/journal.pgen.1004869⟩
- Accession number :
- edsair.doi.dedup.....7861fe1152c2740186511d8655989148
- Full Text :
- https://doi.org/10.1371/journal.pgen.1004869⟩