Genome-wide profiling of Hfq-bound RNAs reveals the iron-responsive small RNA RusT in Caulobacter crescentus
ABSTRACTThe alphaproteobacterium Caulobacter crescentus thrives in oligotrophic environments and is able to optimally exploit minimal resources by entertaining an intricate network of gene expression control mechanisms. Numerous transcriptional activators and repressors have been reported to contrib...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2024-04-01
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| Series: | mBio |
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| Online Access: | https://journals.asm.org/doi/10.1128/mbio.03153-23 |
| _version_ | 1797215313030283264 |
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| author | Laura N. Vogt Gaël Panis Anna Schäpers Nikolai Peschek Michaela Huber Kai Papenfort Patrick H. Viollier Kathrin S. Fröhlich |
| author_facet | Laura N. Vogt Gaël Panis Anna Schäpers Nikolai Peschek Michaela Huber Kai Papenfort Patrick H. Viollier Kathrin S. Fröhlich |
| author_sort | Laura N. Vogt |
| collection | DOAJ |
| description | ABSTRACTThe alphaproteobacterium Caulobacter crescentus thrives in oligotrophic environments and is able to optimally exploit minimal resources by entertaining an intricate network of gene expression control mechanisms. Numerous transcriptional activators and repressors have been reported to contribute to these processes, but only few studies have focused on regulation at the post-transcriptional level in C. crescentus. Small RNAs (sRNAs) are a prominent class of regulators of bacterial gene expression, and most sRNAs characterized today engage in direct base-pairing interactions to modulate the translation and/or stability of target mRNAs. In many cases, the ubiquitous RNA chaperone, Hfq, contributes to the establishment of RNA-RNA interactions. Although the deletion of the hfq gene is associated with a severe loss of fitness in C. crescentus, the RNA ligands of the chaperone have remained largely unexplored. Here we report on the identification of coding and non-coding transcripts associated with Hfq in C. crescentus and demonstrate Hfq-dependent post-transcriptional regulation in this organism. We show that the Hfq-bound sRNA RusT is transcriptionally controlled by the NtrYX two-component system and induced in response to iron starvation. By combining RusT pulse expression with whole-genome transcriptome analysis, we determine 16 candidate target transcripts that are deregulated, many of which encode outer membrane transporters. We hence suggest RusT to support remodeling of the C. crescentus cell surface when iron supplies are limited.IMPORTANCEThe conserved RNA-binding protein Hfq contributes significantly to the adaptation of bacteria to different environmental conditions. Hfq not only stabilizes associated sRNAs but also promotes inter-molecular base-pairing interactions with target transcripts. Hfq plays a pivotal role for growth and survival, controlling central metabolism and cell wall synthesis in the oligotroph Caulobacter crescentus. However, direct evidence for Hfq-dependent post-transcriptional regulation and potential oligotrophy in C. crescentus has been lacking. Here, we identified sRNAs and mRNAs associated with Hfq in vivo, and demonstrated the requirement of Hfq for sRNA-mediated regulation, particularly of outer membrane transporters in C. crescentus. |
| first_indexed | 2024-04-24T11:28:05Z |
| format | Article |
| id | doaj.art-bc383bbcea4c4457b3e173ba419444e4 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-04-24T11:28:05Z |
| publishDate | 2024-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-bc383bbcea4c4457b3e173ba419444e42024-04-10T13:01:15ZengAmerican Society for MicrobiologymBio2150-75112024-04-0115410.1128/mbio.03153-23Genome-wide profiling of Hfq-bound RNAs reveals the iron-responsive small RNA RusT in Caulobacter crescentusLaura N. Vogt0Gaël Panis1Anna Schäpers2Nikolai Peschek3Michaela Huber4Kai Papenfort5Patrick H. Viollier6Kathrin S. Fröhlich7Institute of Microbiology, Faculty of Biological Sciences, Friedrich Schiller University, Jena, GermanyDepartment of Microbiology and Molecular Medicine, Faculty of Medicine/Centre Médical Universitaire, University of Geneva, Geneva, SwitzerlandDepartment of Biology I, Microbiology, Ludwig-Maximilians-University Munich, Munich, GermanyInstitute of Microbiology, Faculty of Biological Sciences, Friedrich Schiller University, Jena, GermanyInstitute of Microbiology, Faculty of Biological Sciences, Friedrich Schiller University, Jena, GermanyInstitute of Microbiology, Faculty of Biological Sciences, Friedrich Schiller University, Jena, GermanyDepartment of Microbiology and Molecular Medicine, Faculty of Medicine/Centre Médical Universitaire, University of Geneva, Geneva, SwitzerlandInstitute of Microbiology, Faculty of Biological Sciences, Friedrich Schiller University, Jena, GermanyABSTRACTThe alphaproteobacterium Caulobacter crescentus thrives in oligotrophic environments and is able to optimally exploit minimal resources by entertaining an intricate network of gene expression control mechanisms. Numerous transcriptional activators and repressors have been reported to contribute to these processes, but only few studies have focused on regulation at the post-transcriptional level in C. crescentus. Small RNAs (sRNAs) are a prominent class of regulators of bacterial gene expression, and most sRNAs characterized today engage in direct base-pairing interactions to modulate the translation and/or stability of target mRNAs. In many cases, the ubiquitous RNA chaperone, Hfq, contributes to the establishment of RNA-RNA interactions. Although the deletion of the hfq gene is associated with a severe loss of fitness in C. crescentus, the RNA ligands of the chaperone have remained largely unexplored. Here we report on the identification of coding and non-coding transcripts associated with Hfq in C. crescentus and demonstrate Hfq-dependent post-transcriptional regulation in this organism. We show that the Hfq-bound sRNA RusT is transcriptionally controlled by the NtrYX two-component system and induced in response to iron starvation. By combining RusT pulse expression with whole-genome transcriptome analysis, we determine 16 candidate target transcripts that are deregulated, many of which encode outer membrane transporters. We hence suggest RusT to support remodeling of the C. crescentus cell surface when iron supplies are limited.IMPORTANCEThe conserved RNA-binding protein Hfq contributes significantly to the adaptation of bacteria to different environmental conditions. Hfq not only stabilizes associated sRNAs but also promotes inter-molecular base-pairing interactions with target transcripts. Hfq plays a pivotal role for growth and survival, controlling central metabolism and cell wall synthesis in the oligotroph Caulobacter crescentus. However, direct evidence for Hfq-dependent post-transcriptional regulation and potential oligotrophy in C. crescentus has been lacking. Here, we identified sRNAs and mRNAs associated with Hfq in vivo, and demonstrated the requirement of Hfq for sRNA-mediated regulation, particularly of outer membrane transporters in C. crescentus.https://journals.asm.org/doi/10.1128/mbio.03153-23Caulobactersmall RNAHfqiron starvationNtrYX |
| spellingShingle | Laura N. Vogt Gaël Panis Anna Schäpers Nikolai Peschek Michaela Huber Kai Papenfort Patrick H. Viollier Kathrin S. Fröhlich Genome-wide profiling of Hfq-bound RNAs reveals the iron-responsive small RNA RusT in Caulobacter crescentus mBio Caulobacter small RNA Hfq iron starvation NtrYX |
| title | Genome-wide profiling of Hfq-bound RNAs reveals the iron-responsive small RNA RusT in Caulobacter crescentus |
| title_full | Genome-wide profiling of Hfq-bound RNAs reveals the iron-responsive small RNA RusT in Caulobacter crescentus |
| title_fullStr | Genome-wide profiling of Hfq-bound RNAs reveals the iron-responsive small RNA RusT in Caulobacter crescentus |
| title_full_unstemmed | Genome-wide profiling of Hfq-bound RNAs reveals the iron-responsive small RNA RusT in Caulobacter crescentus |
| title_short | Genome-wide profiling of Hfq-bound RNAs reveals the iron-responsive small RNA RusT in Caulobacter crescentus |
| title_sort | genome wide profiling of hfq bound rnas reveals the iron responsive small rna rust in caulobacter crescentus |
| topic | Caulobacter small RNA Hfq iron starvation NtrYX |
| url | https://journals.asm.org/doi/10.1128/mbio.03153-23 |
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