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      Grad‐seq in a Gram‐positive bacterium reveals exonucleolytic sRNA activation in competence control

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          Abstract

          RNA–protein interactions are the crucial basis for many steps of bacterial gene expression, including post‐transcriptional control by small regulatory RNAs ( sRNAs). In stark contrast to recent progress in the analysis of Gram‐negative bacteria, knowledge about RNA–protein complexes in Gram‐positive species remains scarce. Here, we used the Grad‐seq approach to draft a comprehensive landscape of such complexes in Streptococcus pneumoniae, in total determining the sedimentation profiles of ~ 88% of the transcripts and ~ 62% of the proteins of this important human pathogen. Analysis of in‐gradient distributions and subsequent tag‐based protein capture identified interactions of the exoribonuclease Cbf1/YhaM with sRNAs that control bacterial competence for DNA uptake. Unexpectedly, the nucleolytic activity of Cbf1 stabilizes these sRNAs, thereby promoting their function as repressors of competence. Overall, these results provide the first RNA/protein complexome resource of a Gram‐positive species and illustrate how this can be utilized to identify new molecular factors with functions in RNA‐based regulation of virulence‐relevant pathways.

          Abstract

          Comprehensive assessment of protein‐ RNA complexes in Streptococcus pneumoniae via Grad‐seq uncovers an unexpected role for the exoribonuclease Cbf1 in stabilizing sRNAs that control bacterial competence for DNA uptake.

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          Small RNAs in bacteria and archaea: who they are, what they do, and how they do it.

          Small RNAs are ubiquitously present regulators in all kingdoms of life. Most bacterial and archaeal small RNAs (sRNAs) act by antisense mechanisms on multiple target mRNAs, thereby globally affecting essentially any conceivable trait-stress responses, adaptive metabolic changes, virulence etc. The sRNAs display many distinct mechanisms of action, most of them through effects on target mRNA translation and/or stability, and helper proteins like Hfq often play key roles. Recent data highlight the interplay between posttranscriptional control by sRNAs and transcription factor-mediated transcriptional control, and cross talk through mutual regulation of regulators. Based on the properties that distinguish sRNA-type from transcription factors-type control, we begin to glimpse why sRNAs have evolved as a second, essential layer of gene regulation. This review will discuss the prevalence of sRNAs, who they are, what biological roles they play, and how they carry out their functions.
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            Assembly of bacterial ribosomes.

            The assembly of ribosomes from a discrete set of components is a key aspect of the highly coordinated process of ribosome biogenesis. In this review, we present a brief history of the early work on ribosome assembly in Escherichia coli, including a description of in vivo and in vitro intermediates. The assembly process is believed to progress through an alternating series of RNA conformational changes and protein-binding events; we explore the effects of ribosomal proteins in driving these events. Ribosome assembly in vivo proceeds much faster than in vitro, and we outline the contributions of several of the assembly cofactors involved, including Era, RbfA, RimJ, RimM, RimP, and RsgA, which associate with the 30S subunit, and CsdA, DbpA, Der, and SrmB, which associate with the 50S subunit.
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              Signal recognition particle: an essential protein-targeting machine.

              The signal recognition particle (SRP) and its receptor compose a universally conserved and essential cellular machinery that couples the synthesis of nascent proteins to their proper membrane localization. The past decade has witnessed an explosion in in-depth mechanistic investigations of this targeting machine at increasingly higher resolutions. In this review, we summarize recent work that elucidates how the SRP and SRP receptor interact with the cargo protein and the target membrane, respectively, and how these interactions are coupled to a novel GTPase cycle in the SRP·SRP receptor complex to provide the driving force and enhance the fidelity of this fundamental cellular pathway. We also discuss emerging frontiers in which important questions remain to be addressed.
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                Author and article information

                Contributors
                Birgitta.Henriques@ki.se
                joerg.vogel@uni-wuerzburg.de
                Journal
                EMBO J
                EMBO J
                10.1002/(ISSN)1460-2075
                EMBJ
                embojnl
                The EMBO Journal
                John Wiley and Sons Inc. (Hoboken )
                0261-4189
                1460-2075
                30 March 2020
                04 May 2020
                30 March 2020
                : 39
                : 9 ( doiID: 10.1002/embj.v39.9 )
                : e103852
                Affiliations
                [ 1 ] Institute of Molecular Infection Biology University of Würzburg Würzburg Germany
                [ 2 ] Department of Microbiology, Tumor & Cell Biology Karolinska Institutet Stockholm Sweden
                [ 3 ] ZB MED—Information Centre for Life Sciences Cologne Germany
                [ 4 ] Helmholtz Institute for RNA‐based Infection Research (HIRI) Helmholtz Centre for Infection Research (HZI) Würzburg Germany
                [ 5 ] Rudolf Virchow Center for Experimental Biomedicine University of Würzburg Würzburg Germany
                [ 6 ] Faculty of Information Science and Communication Studies TH Köln Cologne Germany
                [ 7 ] Department of Clinical Microbiology Karolinska University Hospital Stockholm Sweden
                [ 8 ] SCELSE and LKC Nanyang Technological University, NTU Singapore Singapore
                Author notes
                [*] [* ] Corresponding author. Tel: +46 852 480 000; E‐mail: Birgitta.Henriques@ 123456ki.se

                Corresponding author. Tel: +49 931 3182 575; E‐mail: joerg.vogel@ 123456uni-wuerzburg.de

                Author information
                https://orcid.org/0000-0003-3052-4430
                https://orcid.org/0000-0002-5361-0975
                https://orcid.org/0000-0002-8565-1421
                https://orcid.org/0000-0001-8900-8209
                https://orcid.org/0000-0002-1481-2996
                https://orcid.org/0000-0003-0612-9932
                https://orcid.org/0000-0002-5429-4759
                https://orcid.org/0000-0003-2220-1404
                Article
                EMBJ2019103852
                10.15252/embj.2019103852
                7196914
                32227509
                8fa0a7ab-3046-4c22-a05a-c6d9ec552013
                © 2020 The Authors. Published under the terms of the CC BY 4.0 license

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 28 October 2019
                : 03 March 2020
                : 06 March 2020
                Page count
                Figures: 12, Tables: 0, Pages: 19, Words: 16017
                Funding
                Funded by: Deutsche Forschungsgemeinschaft (DFG) , open-funder-registry 10.13039/501100001659;
                Award ID: Vo875-18
                Funded by: IZKF at the University of Würzburg
                Award ID: Project Z-6
                Funded by: Knut and Wallenberg Foundation
                Funded by: Swedish Research Council , open-funder-registry 10.13039/501100004359;
                Funded by: Swedish Foundation for Strategic Research (SSF) , open-funder-registry 10.13039/501100001729;
                Funded by: Stockholm County Council , open-funder-registry 10.13039/501100004348;
                Categories
                Resource
                Resource
                Custom metadata
                2.0
                04 May 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.1 mode:remove_FC converted:04.05.2020

                Molecular biology
                cbf1,competence,grad‐seq,rna–protein complex,streptococcus pneumoniae,microbiology, virology & host pathogen interaction,rna biology

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