The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.
Interrogation of RNA-protein interaction dynamics in bacterial growth
Open accessPublished version of a preprint
Abstract
Characterising RNA–protein interaction dynamics is fundamental to understand how bacteria respond to their environment. In this study, we have analysed the dynamics of 91% of the Escherichia coli expressed proteome and the RNA-interaction properties of 271 RNA-binding proteins (RBPs) at different growth phases. We find that 68% of RBPs differentially bind RNA across growth phases and characterise 17 previously unannotated proteins as bacterial RBPs including YfiF, a ncRNA-binding protein. While these new RBPs are mostly present in Proteobacteria, two of them are orthologs of human mitochondrial proteins associated with rare metabolic disorders. Moreover, we reveal novel RBP functions for proteins such as the chaperone HtpG, a new stationary phase tRNA-binding protein. For the first time, the dynamics of the bacterial RBPome have been interrogated, showcasing how this approach can reveal the function of uncharacterised proteins and identify critical RNA–protein interactions for cell growth which could inform new antimicrobial therapies.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764
Flagged first, then by citations
Research works printed but not linked: 75
- Aiso T, Kamiya S, Yonezawa H, Gamou S (2014) Overexpression of an antisense RNA, ArrS, increases the acid resistance of Escherichia coli. Microbiology 160:954–961 · DOI
- Ajit Bolar N, Vanlander AV, Wilbrecht C, Van der Aa N, Smet J, De Paepe B, Vandeweyer G, Kooy F, Eyskens F, De Latter E et al (2013) Mutation of the iron-sulfur cluster assembly gene IBA57 causes severe myopathy and encephalopathy. Hum Mol Genet 22:2590–2602 · DOI
- Altenhoff AM, Train C-M, Gilbert KJ, Mediratta I, Mendes de Farias T, Moi D, Nevers Y, Radoykova H-S, Rossier V, Warwick Vesztrocy A et al (2021) OMA orthology in 2021: website overhaul, conserved isoforms, ancestral gene order and more. Nucleic Acids Res 49:D373–D379 · DOI · Paper page
- Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2:2006.0008 · DOI · Paper page
- Babitzke P, Romeo T (2007) CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 10:156–163 · DOI
- Bailey TL (2021) STREME: accurate and versatile sequence motif discovery. Bioinformatics 37:2834–2840 · DOI
- Baker CS, Morozov I, Suzuki K, Romeo T, Babitzke P (2002) CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli. Mol Microbiol 44:1599–1610 · DOI
- Baltz AG, Munschauer M, Schwanhäusser B, Vasile A, Murakawa Y, Schueler M, Youngs N, Penfold-Brown D, Drew K, Milek M et al (2012) The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol Cell 46:674–690 · DOI
- Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300 · DOI · Paper page
- Castello A, Fischer B, Eichelbaum K, Horos R, Beckmann BM, Strein C, Davey NE, Humphreys DT, Preiss T, Steinmetz LM et al (2012) Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 149:1393–1406 · DOI · Paper page
- Castello A, Fischer B, Frese CK, Horos R, Alleaume A-M, Foehr S, Curk T, Krijgsveld J, Hentze MW (2016) Comprehensive identification of RNA-binding domains in human cells. Mol Cell 63:696–710 · DOI
- Castello A, Hentze MW, Preiss T (2015) Metabolic enzymes enjoying new partnerships as RNA-binding proteins. Trends Endocrinol Metab 26:746–757 · DOI
- Chakrabarti AM, Capitanchik C, Ule J, Luscombe NM (2023) clipplotr-a comparative visualization and analysis tool for CLIP data. RNA 29:715–723 · DOI
- Chao Y, Papenfort K, Reinhardt R, Sharma CM, Vogel J (2012) An atlas of Hfq-bound transcripts reveals 3’ UTRs as a genomic reservoir of regulatory small RNAs. EMBO J 31:4005–4019 · DOI
- Chu L-C, Arede P, Li W, Urdaneta EC, Ivanova I, McKellar SW, Wills JC, Fröhlich T, von Kriegsheim A, Beckmann BM et al (2022) The RNA-bound proteome of MRSA reveals post-transcriptional roles for helix-turn-helix DNA-binding and Rossmann-fold proteins. Nat Commun 13:2883 · DOI
- Cieśla J (2006) Metabolic enzymes that bind RNA: yet another level of cellular regulatory network? Acta Biochim Pol 53:11–32 · DOI · Paper page
- Corteggiani M, Bossuet-Greif N, Nougayrède J-P, Byrne D, Ilbert M, Dementin S, Giudici-Orticoni M-T, Méjean V, Oswald E, Genest O (2022) Uncoupling the Hsp90 and DnaK chaperone activities revealed the in vivo relevance of their collaboration in bacteria. Proc Natl Acad Sci USA 119:e2201779119 · DOI
- Curtis NJ, Jeffery CJ (2021) The expanding world of metabolic enzymes moonlighting as RNA binding proteins. Biochem Soc Trans 49:1099–1108 · DOI
- Dobrindt U, Piechaczek K, Schierhorn A, Fischer G, Hecker M, Hacker J (2002) Influence of the leuX-encoded tRNA5(Leu) on the regulation of gene expression in pathogenic Escherichia coli. J Mol Microbiol Biotechnol 4:205–209
- Doncheva NT, Morris JH, Gorodkin J, Jensen LJ (2019) Cytoscape StringApp: network analysis and visualization of proteomics data. J Proteome Res 18:623–632 · DOI
- Doncheva NT, Morris JH, Holze H, Kirsch R, Nastou KC, Cuesta-Astroz Y, Rattei T, Szklarczyk D, von Mering C, Jensen LJ (2023) Cytoscape stringApp 2.0: analysis and visualization of heterogeneous biological networks. J Proteome Res 22:637–646 · DOI
- Dorfer V, Pichler P, Stranzl T, Stadlmann J, Taus T, Winkler S, Mechtler K (2014) MS Amanda, a universal identification algorithm optimized for high accuracy tandem mass spectra. J Proteome Res 13:3679–3684 · DOI
- Garcie C, Tronnet S, Garénaux A, McCarthy AJ, Brachmann AO, Pénary M, Houle S, Nougayrède J-P, Piel J, Taylor PW et al (2016) The bacterial stress-responsive Hsp90 chaperone (HtpG) is required for the production of the genotoxin colibactin and the siderophore yersiniabactin in Escherichia coli. J Infect Dis 214:916–924 · DOI
- Gatto L, Breckels LM, Wieczorek S, Burger T, Lilley KS (2014) Mass-spectrometry-based spatial proteomics data analysis using pRoloc and pRolocdata. Bioinformatics 30:1322–1324 · DOI
- Gatto L, Lilley KS (2012) MSnbase-an R/Bioconductor package for isobaric tagged mass spectrometry data visualization, processing and quantitation. Bioinformatics 28:288–289 · DOI
- Gaudet P, Livstone MS, Lewis SE, Thomas PD (2011) Phylogenetic-based propagation of functional annotations within the Gene Ontology consortium. Brief Bioinform 12:449–462 · DOI
- Geertsma ER, Groeneveld M, Slotboom D-J, Poolman B (2008) Quality control of overexpressed membrane proteins. Proc Natl Acad Sci USA 105:5722–5727 · DOI
- GeZi G, Liu R, Du D, Wu N, Bao N, Fan L, Morigen M (2021) YfiF, an unknown protein, affects initiation timing of chromosome replication in Escherichia coli. J Basic Microbiol 61:883–899 · DOI
- Goldstein J, Pollitt NS, Inouye M (1990) Major cold shock protein of Escherichia coli. Proc Natl Acad Sci USA 87:283–287 · DOI
- Hayes ET, Wilks JC, Sanfilippo P, Yohannes E, Tate DP, Jones BD, Radmacher MD, BonDurant SS, Slonczewski JL (2006) Oxygen limitation modulates pH regulation of catabolism and hydrogenases, multidrug transporters, and envelope composition in Escherichia coli K-12. BMC Microbiol 6:89 · DOI
- Hentze MW, Castello A, Schwarzl T, Preiss T (2018) A brave new world of RNA-binding proteins. Nat Rev Mol Cell Biol 19:327–341 · DOI · Paper page
- Holmqvist E, Vogel J (2018) RNA-binding proteins in bacteria. Nat Rev Microbiol 16:601–615 · DOI
- Hu W, Yuan B, Lodish HF (2014) Cpeb4-mediated translational regulatory circuitry controls terminal erythroid differentiation. Dev Cell 30:660–672 · DOI
- Huppertz I, Attig J, D’Ambrogio A, Easton LE, Sibley CR, Sugimoto Y, Tajnik M, König J, Ule J (2014) iCLIP: protein-RNA interactions at nucleotide resolution. Methods San Diego Calif 65:274–287 · DOI
- Jiang M, Sullivan SM, Walker AK, Strahler JR, Andrews PC, Maddock JR (2007) Identification of novel Escherichia coli ribosome-associated proteins using isobaric tags and multidimensional protein identification techniques. J Bacteriol 189:3434–3444 · DOI
- Jones PG, VanBogelen RA, Neidhardt FC (1987) Induction of proteins in response to low temperature in Escherichia coli. J Bacteriol 169:2092–2095 · DOI
- Kuret K, Amalietti AG, Jones DM, Capitanchik C, Ule J (2022) Positional motif analysis reveals the extent of specificity of protein-RNA interactions observed by CLIP. Genome Biol 23:191 · DOI
- Lee FCY, Chakrabarti AM, Hänel H, Monzón-Casanova E, Hallegger M, Militti C, Capraro F, Sadée C, Toolan-Kerr P, Wilkins O et al (2021) An improved iCLIP protocol. bioRxiv. https://doi.org/10.1101/2021.08.27.457890 · DOI
- Leone S, Srivastava A, Hummel B, Tittel L, Aprile-Garcia F, Herrero-Ruiz A, Rawat P, Willis AE, Sawarkar R (2024) HSP70 binds to specific non-coding RNA and regulates human RNA Polymerase III. Mol Cell 84:687–701.e7 · DOI
- Letunic I, Bork P (2021) Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49:W293–W296 · DOI
- Liepelt A, Naarmann-de Vries IS, Simons N, Eichelbaum K, Föhr S, Archer SK, Castello A, Usadel B, Krijgsveld J, Preiss T et al (2016) Identification of RNA-binding Proteins in macrophages by interactome capture. Mol Cell Proteomics 15:2699–2714 · DOI
- Lossos A, Stumpfig C, Stevanin G, Gaussen M, Zimmerman B-E, Mundwiller E, Asulin M, Chamma L, Sheffer R, Misk A et al (2015) Fe/S protein assembly gene IBA57 mutation causes hereditary spastic paraplegia. Neurology 84:659–667 · DOI
- McAlister GC, Nusinow DP, Jedrychowski MP, Wühr M, Huttlin EL, Erickson BK, Rad R, Haas W, Gygi SP (2014) MultiNotch MS3 enables accurate, sensitive, and multiplexed detection of differential expression across cancer cell line proteomes. Anal Chem 86:7150–7158 · DOI · Paper page
- Milek M, Imami K, Mukherjee N, Bortoli FD, Zinnall U, Hazapis O, Trahan C, Oeffinger M, Heyd F, Ohler U et al (2017) DDX54 regulates transcriptome dynamics during DNA damage response. Genome Res 27:1344–1359 · DOI
- Nomura T, Fujita N, Ishihama A (1987) Expression of the leuX gene in Escherichia coli. Regulation at transcription and tRNA processing steps. J Mol Biol 197:659–670 · DOI
- Osorio D, Rondón-Villarreal P, Torres R (2015) Peptides: a package for data mining of antimicrobial peptides. The R Journal 7:4–14 · DOI
- Perez-Perri JI, Ferring-Appel D, Huppertz I, Schwarzl T, Sahadevan S, Stein F, Rettel M, Galy B, Hentze MW (2023) The RNA-binding protein landscapes differ between mammalian organs and cultured cells. Nat Commun 14:2074 · DOI
- Potts AH, Vakulskas CA, Pannuri A, Yakhnin H, Babitzke P, Romeo T (2017) Global role of the bacterial post-transcriptional regulator CsrA revealed by integrated transcriptomics. Nat Commun 8:1596 · DOI
- Prickett MD, Page M, Douglas AE, Thomas GH (2006) Buchnera BASE: a post-genomic resource for Buchnera sp. APS. Bioinformatics 22:641–642 · DOI
- Queiroz RML, Smith T, Villanueva E, Marti-Solano M, Monti M, Pizzinga M, Mirea D-M, Ramakrishna M, Harvey RF, Dezi V et al (2019) Comprehensive identification of RNA-protein interactions in any organism using orthogonal organic phase separation (OOPS). Nat Biotechnol 37:169–178 · DOI
- Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK (2015) limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43:e47 · DOI · Paper page
- Romeo T, Gong M, Liu MY, Brun-Zinkernagel AM (1993) Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J Bacteriol 175:4744–4755 · DOI
- Shchepachev V, Bresson S, Spanos C, Petfalski E, Fischer L, Rappsilber J, Tollervey D (2019) Defining the RNA interactome by total RNA-associated protein purification. Mol Syst Biol 15:e8689 · DOI
- Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J et al (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539 · DOI
- Skunca N, Bošnjak M, Kriško A, Panov P, Džeroski S, Smuc T, Supek F (2013) Phyletic profiling with cliques of orthologs is enhanced by signatures of paralogy relationships. PLoS Comput Biol 9:e1002852 · DOI
- Smirnov A, Förstner KU, Holmqvist E, Otto A, Günster R, Becher D, Reinhardt R, Vogel J (2016) Grad-seq guides the discovery of ProQ as a major small RNA-binding protein. Proc Natl Acad Sci USA 113:11591–11596 · DOI
- Sonnhammer ELL, Östlund G (2015) InParanoid 8: orthology analysis between 273 proteomes, mostly eukaryotic. Nucleic Acids Res 43:D234–D239 · DOI
- Soufi B, Krug K, Harst A, Macek B (2015) Characterization of the E. coli proteome and its modifications during growth and ethanol stress. Front Microbiol 6:103 · DOI · Paper page
- Stenum TS, Kumar AD, Sandbaumhüter FA, Kjellin J, Jerlström-Hultqvist J, Andrén PE, Koskiniemi S, Jansson ET, Holmqvist E (2023) RNA interactome capture in Escherichia coli globally identifies RNA-binding proteins. Nucleic Acids Res 51:4572–4587 · DOI
- Stylianidou S, Brennan C, Nissen SB, Kuwada NJ, Wiggins PA (2016) SuperSegger: robust image segmentation, analysis and lineage tracking of bacterial cells. Mol Microbiol 102:690–700 · DOI
- Sysoev VO, Fischer B, Frese CK, Gupta I, Krijgsveld J, Hentze MW, Castello A, Ephrussi A (2016) Global changes of the RNA-bound proteome during the maternal-to-zygotic transition in Drosophila. Nat Commun 7:12128 · DOI
- Szklarczyk D, Gable AL, Nastou KC, Lyon D, Kirsch R, Pyysalo S, Doncheva NT, Legeay M, Fang T, Bork P et al (2021) The STRING database in 2021: customizable protein-protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res 49:D605–D612 · DOI · Paper page
- Varadi M, Anyango S, Deshpande M, Nair S, Natassia C, Yordanova G, Yuan D, Stroe O, Wood G, Laydon A et al (2022) AlphaFold Protein Structure Database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res 50:D439–D444 · DOI · Paper page
- Vercruysse M, Köhrer C, Shen Y, Proulx S, Ghosal A, Davies BW, RajBhandary UL, Walker GC (2016) Identification of YbeY-protein interactions involved in 16S rRNA maturation and stress regulation in Escherichia coli. mBio 7:e01785–16 · DOI
- Villanueva E, Smith T, Queiroz RML, Monti M, Pizzinga M, Elzek M, Dezi V, Harvey RF, Ramakrishna M, Willis AE et al (2020) Efficient recovery of the RNA-bound proteome and protein-bound transcriptome using phase separation (OOPS). Nat Protoc 15:2568–2588 · DOI
- Vizcaíno JA, Csordas A, del-Toro N, Dianes JA, Griss J, Lavidas I, Mayer G, Perez-Riverol Y, Reisinger F, Ternent T et al (2016) 2016 update of the PRIDE database and its related tools. Nucleic Acids Res 44:D447–D456 · DOI
- Wada A, Igarashi K, Yoshimura S, Aimoto S, Ishihama A (1995) Ribosome modulation factor: stationary growth phase-specific inhibitor of ribosome functions from Escherichia coli. Biochem Biophys Res Commun 214:410–417 · DOI
- Wada A, Yamazaki Y, Fujita N, Ishihama A (1990) Structure and probable genetic location of a ‘ribosome modulation factor’ associated with 100S ribosomes in stationary-phase Escherichia coli cells. Proc Natl Acad Sci USA 87:2657–2661 · DOI
- Walczak M, Mancini L, Xu J, Raguseo F, Kotar J, Cicuta P, Di Michele L (2023) A synthetic signaling network imitating the action of immune cells in response to bacterial metabolism. Adv Mater 35:2301562 · DOI
- Weraarpachai W, Antonicka H, Sasarman F, Seeger J, Schrank B, Kolesar JE, Lochmüller H, Chevrette M, Kaufman BA, Horvath R et al (2009) Mutation in TACO1, encoding a translational activator of COX I, results in cytochrome c oxidase deficiency and late-onset Leigh syndrome. Nat Genet 41:833–837 · DOI
- Wickham H (2009) Ggplot2: elegant graphics for data analysis. New York, Springer · DOI · Paper page
- Wickham H, Averick M, Bryan J, Chang W, McGowan L, François R, Grolemund G, Hayes A, Henry L, Hester J et al (2019) Welcome to the Tidyverse. J Open Source Softw 4:1686 · DOI · Paper page
- Wolin E, Guo JK, Blanco MR, Perez AA, Goronzy IN, Abdou AA, Gorhe D, Guttman M, Jovanovic M (2023) SPIDR: a highly multiplexed method for mapping RNA-protein interactions uncovers a potential mechanism for selective translational suppression upon cellular stress. bioRxiv · DOI
- Young JC, Hoogenraad NJ, Hartl FU (2003) Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112:41–50 · DOI · Paper page
- Zhu Y, Orre LM, Zhou Tran Y, Mermelekas G, Johansson HJ, Malyutina A, Anders S, Lehtiö J (2020) DEqMS: a method for accurate variance estimation in differential protein expression analysis. Mol Cell Proteomics MCP 19:1047–1057 · DOI
Metadata
- Authors
- Monti, M., Herman, R., Mancini, L., Capitanchik, C., Davey, K., Dawson, C. S., Ule, J., Thomas, G. H., Willis, A. E., Lilley, K. S., & Villanueva, E.
- Affiliations
- University of Cambridge (GB)
- University of York (GB)
- King's College London (GB)
- Corresponding author
- Willis, Anne E
- Lilley, Kathryn S
- Villanueva, Eneko
- ORCID
- Venue
- Molecular Systems Biology
- Published
- 2024-03-26
- Volume
- 20
- Issue
- 5
- Pages
- 573-589
- ISSN
- 1744-4292 (ISSN-L)
- PMC
- PMC11066096
- OpenAlex
- W4393192761
- Cited by
- 16
- References
- 1
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 4
- FWCI
- 3.44
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Molecular Systems Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research Portal (King's College London) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- UKRI | Medical Research Council (5TR00, FC001110)
- Wellcome Trust (110071/Z/15/Z, FC001110)
- Herchel Smith Postoctoral Fellowship
- Herchel Smith PhD Research Studenship
- European Union Horizon 2020 research and innovation programme (835300-RNPdynamics)
- UKRI | Innovate UK) (BB/N01040X/1)
- Cancer Research UK (FC001110)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Keywords
- RNA-protein interactions, RNA-binding proteins, Escherichia coli, bacterial growth phase, HtpG, molecular chaperones, Proteobacteria, antimicrobial drug targets, unannotated proteins
- MeSH terms
- Escherichia coli, Humans, Protein Binding, RNA, Bacterial, Gene Expression Regulation, Bacterial, RNA-Binding Proteins, Proteome, Escherichia coli Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review