Aminoglycoside tolerance in Vibrio cholerae engages translational reprogramming associated with queuosine tRNA modification
Tgt is the enzyme modifying the guanine (G) in tRNAs with GUN anticodon to queuosine (Q). tgt is required for optimal growth of Vibrio cholerae in the presence of sub-lethal aminoglycoside concentrations. We further explored here the role of the Q34 in the efficiency of codon decoding upon tobramyci...
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eLife Sciences Publications Ltd
2025-01-01
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| author | Louna Fruchard Anamaria Babosan Andre Carvalho Manon Lang Blaise Li Magalie Duchateau Quentin Giai Gianetto Mariette Matondo Frederic Bonhomme Isabelle Hatin Hugo Arbes Céline Fabret Enora Corler Guillaume Sanchez Virginie Marchand Yuri Motorin Olivier Namy Valérie de Crécy-Lagard Didier Mazel Zeynep Baharoglu |
| author_facet | Louna Fruchard Anamaria Babosan Andre Carvalho Manon Lang Blaise Li Magalie Duchateau Quentin Giai Gianetto Mariette Matondo Frederic Bonhomme Isabelle Hatin Hugo Arbes Céline Fabret Enora Corler Guillaume Sanchez Virginie Marchand Yuri Motorin Olivier Namy Valérie de Crécy-Lagard Didier Mazel Zeynep Baharoglu |
| author_sort | Louna Fruchard |
| collection | DOAJ |
| description | Tgt is the enzyme modifying the guanine (G) in tRNAs with GUN anticodon to queuosine (Q). tgt is required for optimal growth of Vibrio cholerae in the presence of sub-lethal aminoglycoside concentrations. We further explored here the role of the Q34 in the efficiency of codon decoding upon tobramycin exposure. We characterized its impact on the overall bacterial proteome, and elucidated the molecular mechanisms underlying the effects of Q34 modification in antibiotic translational stress response. Using molecular reporters, we showed that Q34 impacts the efficiency of decoding at tyrosine TAT and TAC codons. Proteomics analyses revealed that the anti-SoxR factor RsxA is better translated in the absence of tgt. RsxA displays a codon bias toward tyrosine TAT and overabundance of RsxA leads to decreased expression of genes belonging to SoxR oxidative stress regulon. We also identified conditions that regulate tgt expression. We propose that regulation of Q34 modification in response to environmental cues leads to translational reprogramming of transcripts bearing a biased tyrosine codon usage. In silico analysis further identified candidate genes which could be subject to such translational regulation, among which DNA repair factors. Such transcripts, fitting the definition of modification tunable transcripts, are central in the bacterial response to antibiotics. |
| format | Article |
| id | doaj-art-18fa0ef59e3a4aaa898e76f783b09a69 |
| institution | Kabale University |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj-art-18fa0ef59e3a4aaa898e76f783b09a692025-01-06T16:00:16ZengeLife Sciences Publications LtdeLife2050-084X2025-01-011310.7554/eLife.96317Aminoglycoside tolerance in Vibrio cholerae engages translational reprogramming associated with queuosine tRNA modificationLouna Fruchard0Anamaria Babosan1https://orcid.org/0000-0003-3464-5491Andre Carvalho2Manon Lang3Blaise Li4https://orcid.org/0000-0003-3080-1899Magalie Duchateau5https://orcid.org/0000-0001-5475-3065Quentin Giai Gianetto6Mariette Matondo7https://orcid.org/0000-0003-3958-7710Frederic Bonhomme8Isabelle Hatin9Hugo Arbes10Céline Fabret11Enora Corler12Guillaume Sanchez13Virginie Marchand14https://orcid.org/0000-0002-8537-1139Yuri Motorin15Olivier Namy16https://orcid.org/0000-0002-1143-5961Valérie de Crécy-Lagard17https://orcid.org/0000-0002-9955-3785Didier Mazel18https://orcid.org/0000-0001-6482-6002Zeynep Baharoglu19https://orcid.org/0000-0003-3477-2685Institut Pasteur, Université Paris Cité, Unité Plasticité du Génome Bactérien, Paris, France; Sorbonne Université, Collège Doctoral, Paris, FranceInstitut Pasteur, Université Paris Cité, Unité Plasticité du Génome Bactérien, Paris, FranceInstitut Pasteur, Université Paris Cité, Unité Plasticité du Génome Bactérien, Paris, FranceInstitut Pasteur, Université Paris Cité, Unité Plasticité du Génome Bactérien, Paris, FranceInstitut Pasteur, Université Paris Cité, Bioinformatics and Biostatistics Hub, Paris, FranceInstitut Pasteur, Université Paris Cité, Proteomics Platform, Mass Spectrometry for Biology Unit, Paris, FranceInstitut Pasteur, Université Paris Cité, Proteomics Platform, Mass Spectrometry for Biology Unit, Paris, France; Institut Pasteur, Université Paris Cité, Department of Computation Biology, Bioinformatics and Biostatistics Hub, Paris, FranceInstitut Pasteur, Université Paris Cité, Proteomics Platform, Mass Spectrometry for Biology Unit, Paris, FranceInstitut Pasteur, Université Paris cité, Epigenetic Chemical Biology Unit, Paris, FranceUniversité Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Gif sur Yvette, FranceUniversité Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Gif sur Yvette, FranceUniversité Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Gif sur Yvette, FranceUniversité Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Gif sur Yvette, FranceUniversité de Lorraine, CNRS, Inserm, UAR2008/US40 IBSLor, Epitranscriptomics and RNA Sequencing Core Facility and UMR7365 IMoPA, Nancy, FranceUniversité de Lorraine, CNRS, Inserm, UAR2008/US40 IBSLor, Epitranscriptomics and RNA Sequencing Core Facility and UMR7365 IMoPA, Nancy, FranceUniversité de Lorraine, CNRS, Inserm, UAR2008/US40 IBSLor, Epitranscriptomics and RNA Sequencing Core Facility and UMR7365 IMoPA, Nancy, FranceUniversité Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Gif sur Yvette, FranceDepartment of Microbiology and Cell Science, University of Florida, Gainesville, United States; University of Florida Genetics Institute, Gainesville, United StatesInstitut Pasteur, Université Paris Cité, Unité Plasticité du Génome Bactérien, Paris, FranceInstitut Pasteur, Université Paris Cité, Unité Plasticité du Génome Bactérien, Paris, FranceTgt is the enzyme modifying the guanine (G) in tRNAs with GUN anticodon to queuosine (Q). tgt is required for optimal growth of Vibrio cholerae in the presence of sub-lethal aminoglycoside concentrations. We further explored here the role of the Q34 in the efficiency of codon decoding upon tobramycin exposure. We characterized its impact on the overall bacterial proteome, and elucidated the molecular mechanisms underlying the effects of Q34 modification in antibiotic translational stress response. Using molecular reporters, we showed that Q34 impacts the efficiency of decoding at tyrosine TAT and TAC codons. Proteomics analyses revealed that the anti-SoxR factor RsxA is better translated in the absence of tgt. RsxA displays a codon bias toward tyrosine TAT and overabundance of RsxA leads to decreased expression of genes belonging to SoxR oxidative stress regulon. We also identified conditions that regulate tgt expression. We propose that regulation of Q34 modification in response to environmental cues leads to translational reprogramming of transcripts bearing a biased tyrosine codon usage. In silico analysis further identified candidate genes which could be subject to such translational regulation, among which DNA repair factors. Such transcripts, fitting the definition of modification tunable transcripts, are central in the bacterial response to antibiotics.https://elifesciences.org/articles/96317Vibrio choleraeepitranscriptomeantibiotic stresstRNA modificationqueuosinepost-transcriptional regulation |
| spellingShingle | Louna Fruchard Anamaria Babosan Andre Carvalho Manon Lang Blaise Li Magalie Duchateau Quentin Giai Gianetto Mariette Matondo Frederic Bonhomme Isabelle Hatin Hugo Arbes Céline Fabret Enora Corler Guillaume Sanchez Virginie Marchand Yuri Motorin Olivier Namy Valérie de Crécy-Lagard Didier Mazel Zeynep Baharoglu Aminoglycoside tolerance in Vibrio cholerae engages translational reprogramming associated with queuosine tRNA modification eLife Vibrio cholerae epitranscriptome antibiotic stress tRNA modification queuosine post-transcriptional regulation |
| title | Aminoglycoside tolerance in Vibrio cholerae engages translational reprogramming associated with queuosine tRNA modification |
| title_full | Aminoglycoside tolerance in Vibrio cholerae engages translational reprogramming associated with queuosine tRNA modification |
| title_fullStr | Aminoglycoside tolerance in Vibrio cholerae engages translational reprogramming associated with queuosine tRNA modification |
| title_full_unstemmed | Aminoglycoside tolerance in Vibrio cholerae engages translational reprogramming associated with queuosine tRNA modification |
| title_short | Aminoglycoside tolerance in Vibrio cholerae engages translational reprogramming associated with queuosine tRNA modification |
| title_sort | aminoglycoside tolerance in vibrio cholerae engages translational reprogramming associated with queuosine trna modification |
| topic | Vibrio cholerae epitranscriptome antibiotic stress tRNA modification queuosine post-transcriptional regulation |
| url | https://elifesciences.org/articles/96317 |
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