The global RNA-binding protein RbpB is a regulator of polysaccharide utilization in Bacteroides thetaiotaomicron
Abstract Paramount to human health, symbiotic bacteria in the gastrointestinal tract rely on the breakdown of complex polysaccharides to thrive in this sugar-deprived environment. Gut Bacteroides are metabolic generalists and deploy dozens of polysaccharide utilization loci (PULs) to forage diverse...
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2025-01-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-55383-8 |
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| author | Ann-Sophie Rüttiger Daniel Ryan Luisella Spiga Vanessa Lamm-Schmidt Gianluca Prezza Sarah Reichardt Madison Langford Lars Barquist Franziska Faber Wenhan Zhu Alexander J. Westermann |
| author_facet | Ann-Sophie Rüttiger Daniel Ryan Luisella Spiga Vanessa Lamm-Schmidt Gianluca Prezza Sarah Reichardt Madison Langford Lars Barquist Franziska Faber Wenhan Zhu Alexander J. Westermann |
| author_sort | Ann-Sophie Rüttiger |
| collection | DOAJ |
| description | Abstract Paramount to human health, symbiotic bacteria in the gastrointestinal tract rely on the breakdown of complex polysaccharides to thrive in this sugar-deprived environment. Gut Bacteroides are metabolic generalists and deploy dozens of polysaccharide utilization loci (PULs) to forage diverse dietary and host-derived glycans. The expression of the multi-protein PUL complexes is tightly regulated at the transcriptional level. However, how PULs are orchestrated at translational level in response to the fluctuating levels of their cognate substrates is unknown. Here, we identify the RNA-binding protein RbpB and a family of noncoding RNAs as key players in post-transcriptional PUL regulation. We demonstrate that RbpB interacts with numerous cellular transcripts, including a paralogous noncoding RNA family comprised of 14 members, the FopS (family of paralogous sRNAs). Through a series of in-vitro and in-vivo assays, we reveal that FopS sRNAs repress the translation of SusC-like glycan transporters when substrates are limited—an effect antagonized by RbpB. Ablation of RbpB in Bacteroides thetaiotaomicron compromises colonization in the mouse gut in a diet-dependent manner. Together, this study adds to our understanding of RNA-coordinated metabolic control as an important factor contributing to the in-vivo fitness of predominant microbiota species in dynamic nutrient landscapes. |
| format | Article |
| id | doaj-art-897bebeba8704d96a28355d9cf7bae82 |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Nature Portfolio |
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| series | Nature Communications |
| spelling | doaj-art-897bebeba8704d96a28355d9cf7bae822025-01-05T12:40:47ZengNature PortfolioNature Communications2041-17232025-01-0116111510.1038/s41467-024-55383-8The global RNA-binding protein RbpB is a regulator of polysaccharide utilization in Bacteroides thetaiotaomicronAnn-Sophie Rüttiger0Daniel Ryan1Luisella Spiga2Vanessa Lamm-Schmidt3Gianluca Prezza4Sarah Reichardt5Madison Langford6Lars Barquist7Franziska Faber8Wenhan Zhu9Alexander J. Westermann10Department of Microbiology, Biocenter, University of WürzburgDepartment of Microbiology, Biocenter, University of WürzburgDepartment of Pathology, Microbiology, and Immunology, Vanderbilt UniversityHelmholtz Institute for RNA-based Infection Research (HIRI), Helmholtz Centre for Infection Research (HZI)Helmholtz Institute for RNA-based Infection Research (HIRI), Helmholtz Centre for Infection Research (HZI)Helmholtz Institute for RNA-based Infection Research (HIRI), Helmholtz Centre for Infection Research (HZI)Department of Pathology, Microbiology, and Immunology, Vanderbilt UniversityHelmholtz Institute for RNA-based Infection Research (HIRI), Helmholtz Centre for Infection Research (HZI)Helmholtz Institute for RNA-based Infection Research (HIRI), Helmholtz Centre for Infection Research (HZI)Department of Pathology, Microbiology, and Immunology, Vanderbilt UniversityDepartment of Microbiology, Biocenter, University of WürzburgAbstract Paramount to human health, symbiotic bacteria in the gastrointestinal tract rely on the breakdown of complex polysaccharides to thrive in this sugar-deprived environment. Gut Bacteroides are metabolic generalists and deploy dozens of polysaccharide utilization loci (PULs) to forage diverse dietary and host-derived glycans. The expression of the multi-protein PUL complexes is tightly regulated at the transcriptional level. However, how PULs are orchestrated at translational level in response to the fluctuating levels of their cognate substrates is unknown. Here, we identify the RNA-binding protein RbpB and a family of noncoding RNAs as key players in post-transcriptional PUL regulation. We demonstrate that RbpB interacts with numerous cellular transcripts, including a paralogous noncoding RNA family comprised of 14 members, the FopS (family of paralogous sRNAs). Through a series of in-vitro and in-vivo assays, we reveal that FopS sRNAs repress the translation of SusC-like glycan transporters when substrates are limited—an effect antagonized by RbpB. Ablation of RbpB in Bacteroides thetaiotaomicron compromises colonization in the mouse gut in a diet-dependent manner. Together, this study adds to our understanding of RNA-coordinated metabolic control as an important factor contributing to the in-vivo fitness of predominant microbiota species in dynamic nutrient landscapes.https://doi.org/10.1038/s41467-024-55383-8 |
| spellingShingle | Ann-Sophie Rüttiger Daniel Ryan Luisella Spiga Vanessa Lamm-Schmidt Gianluca Prezza Sarah Reichardt Madison Langford Lars Barquist Franziska Faber Wenhan Zhu Alexander J. Westermann The global RNA-binding protein RbpB is a regulator of polysaccharide utilization in Bacteroides thetaiotaomicron Nature Communications |
| title | The global RNA-binding protein RbpB is a regulator of polysaccharide utilization in Bacteroides thetaiotaomicron |
| title_full | The global RNA-binding protein RbpB is a regulator of polysaccharide utilization in Bacteroides thetaiotaomicron |
| title_fullStr | The global RNA-binding protein RbpB is a regulator of polysaccharide utilization in Bacteroides thetaiotaomicron |
| title_full_unstemmed | The global RNA-binding protein RbpB is a regulator of polysaccharide utilization in Bacteroides thetaiotaomicron |
| title_short | The global RNA-binding protein RbpB is a regulator of polysaccharide utilization in Bacteroides thetaiotaomicron |
| title_sort | global rna binding protein rbpb is a regulator of polysaccharide utilization in bacteroides thetaiotaomicron |
| url | https://doi.org/10.1038/s41467-024-55383-8 |
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