An sRNA and Cold Shock Protein Homolog-Based Feedforward Loop Post-transcriptionally Controls Cell Cycle Master Regulator CtrA

Robledo M, Schlueter J-P, Loehr LO, Linne U, Albaum S, Jimenez-Zurdo JI, Becker A (2018)

Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Robledo, Marta; Schlueter, Jan-Philip; Loehr, Lars O.; Linne, Uwe; Albaum, StefanUniBi ; Jimenez-Zurdo, Jose I.; Becker, Anke
Abstract / Bemerkung
Adjustment of cell cycle progression is crucial for bacterial survival and adaptation under adverse conditions. However, the understanding of modulation of cell cycle control in response to environmental changes is rather incomplete. In alpha-proteobacteria, the broadly conserved cell cycle master regulator CtrA underlies multiple levels of control, including coupling of cell cycle and cell differentiation. CtrA levels are known to be tightly controlled through diverse transcriptional and post-translational mechanisms. Here, small RNA (sRNA)-mediated post-transcriptional regulation is uncovered as an additional level of CtrA fine-tuning. Computational predictions as well as transcriptome and proteome studies consistently suggested targeting of ctrA and the putative cold shock chaperone cspA5 mRNAs by the trans-encoded sRNA (trans-sRNA) GspR (formerly SmelC775) in several Sinorhizobium species. GspR strongly accumulated in the stationary growth phase, especially in minimal medium (MM) cultures. Lack of the gspR locus confers a fitness disadvantage in competition with the wild type, while its overproduction hampers cell growth, suggesting that this riboregulator interferes with cell cycle progression. An eGFP-based reporter in vivo assay, involving wild-type and mutant sRNA and mRNA pairs, experimentally confirmed GspR-dependent posttranscriptional down-regulation of ctrA and cspA5 expression, which most likely occurs through base-pairing to the respective mRNA. The energetically favored secondary structure of GspR is predicted to comprise three stem-loop domains, with stem-loop 1 and stem-loop 3 targeting ctrA and cspA5 mRNA, respectively. Moreover, this work reports evidence for post-transcriptional control of ctrA by CspA5. Thus, this regulation and GspR-mediated post-transcriptional repression of ctrA and cspA5 expression constitute a coherent feed-forward loop, which may enhance the negative effect of GspR on CtrA levels. This novel regulatory circuit involving the riboregulator GspR, CtrA, and a cold shock chaperone may contribute to fine-tuning of ctrA expression.
non-coding RNAs; cell cycle; post-transcriptional control; RNA binding; proteins; CtrA; Sinorhizobium meliloti
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Robledo M, Schlueter J-P, Loehr LO, et al. An sRNA and Cold Shock Protein Homolog-Based Feedforward Loop Post-transcriptionally Controls Cell Cycle Master Regulator CtrA. FRONTIERS IN MICROBIOLOGY. 2018;9: 14.
Robledo, M., Schlueter, J. - P., Loehr, L. O., Linne, U., Albaum, S., Jimenez-Zurdo, J. I., & Becker, A. (2018). An sRNA and Cold Shock Protein Homolog-Based Feedforward Loop Post-transcriptionally Controls Cell Cycle Master Regulator CtrA. FRONTIERS IN MICROBIOLOGY, 9, 14. doi:10.3389/fmicb.2018.00763
Robledo, M., Schlueter, J. - P., Loehr, L. O., Linne, U., Albaum, S., Jimenez-Zurdo, J. I., and Becker, A. (2018). An sRNA and Cold Shock Protein Homolog-Based Feedforward Loop Post-transcriptionally Controls Cell Cycle Master Regulator CtrA. FRONTIERS IN MICROBIOLOGY 9:14.
Robledo, M., et al., 2018. An sRNA and Cold Shock Protein Homolog-Based Feedforward Loop Post-transcriptionally Controls Cell Cycle Master Regulator CtrA. FRONTIERS IN MICROBIOLOGY, 9: 14.
M. Robledo, et al., “An sRNA and Cold Shock Protein Homolog-Based Feedforward Loop Post-transcriptionally Controls Cell Cycle Master Regulator CtrA”, FRONTIERS IN MICROBIOLOGY, vol. 9, 2018, : 14.
Robledo, M., Schlueter, J.-P., Loehr, L.O., Linne, U., Albaum, S., Jimenez-Zurdo, J.I., Becker, A.: An sRNA and Cold Shock Protein Homolog-Based Feedforward Loop Post-transcriptionally Controls Cell Cycle Master Regulator CtrA. FRONTIERS IN MICROBIOLOGY. 9, : 14 (2018).
Robledo, Marta, Schlueter, Jan-Philip, Loehr, Lars O., Linne, Uwe, Albaum, Stefan, Jimenez-Zurdo, Jose I., and Becker, Anke. “An sRNA and Cold Shock Protein Homolog-Based Feedforward Loop Post-transcriptionally Controls Cell Cycle Master Regulator CtrA”. FRONTIERS IN MICROBIOLOGY 9 (2018): 14.

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Transcription attenuation-derived small RNA rnTrpL regulates tryptophan biosynthesis gene expression in trans.
Melior H, Li S, Madhugiri R, Stötzel M, Azarderakhsh S, Barth-Weber S, Baumgardt K, Ziebuhr J, Evguenieva-Hackenberg E., Nucleic Acids Res 47(12), 2019
PMID: 30993322

62 References

Daten bereitgestellt von Europe PubMed Central.

A guide through the computational analysis of isotope-labeled mass spectrometry-based quantitative proteomics data: an application study.
Albaum SP, Hahne H, Otto A, Haußmann U, Becher D, Poetsch A, Goesmann A, Nattkemper TW., Proteome Sci 9(), 2011
PMID: 21663690
Qupe--a Rich Internet Application to take a step forward in the analysis of mass spectrometry-based quantitative proteomics experiments.
Albaum SP, Neuweger H, Franzel B, Lange S, Mertens D, Trotschel C, Wolters D, Kalinowski J, Nattkemper TW, Goesmann A., Bioinformatics 25(23), 2009
PMID: 19808875
Sinorhizobium meliloti regulator MucR couples exopolysaccharide synthesis and motility.
Bahlawane C, McIntosh M, Krol E, Becker A., Mol. Plant Microbe Interact. 21(11), 2008
PMID: 18842098
Recognition of heptameric seed sequence underlies multi-target regulation by RybB small RNA in Salmonella enterica.
Balbontin R, Fiorini F, Figueroa-Bossi N, Casadesus J, Bossi L., Mol. Microbiol. 78(2), 2010
PMID: 20979336
Bacterial adaptation to cold.
Barria C, Malecki M, Arraiano CM., Microbiology (Reading, Engl.) 159(Pt 12), 2013
PMID: 24068238
RNase E affects the expression of the acyl-homoserine lactone synthase gene sinI in Sinorhizobium meliloti.
Baumgardt K, Charoenpanich P, McIntosh M, Schikora A, Stein E, Thalmann S, Kogel KH, Klug G, Becker A, Evguenieva-Hackenberg E., J. Bacteriol. 196(7), 2014
PMID: 24488310
Riboregulation in plant-associated α-proteobacteria.
Becker A, Overloper A, Schluter JP, Reinkensmeier J, Robledo M, Giegerich R, Narberhaus F, Evguenieva-Hackenberg E., RNA Biol 11(5), 2014
PMID: 25003187
Base pairing small RNAs and their roles in global regulatory networks.
Beisel CL, Storz G., FEMS Microbiol. Rev. 34(5), 2010
PMID: 20662934
R factor transfer in Rhizobium leguminosarum.
Beringer JE., J. Gen. Microbiol. 84(1), 1974
PMID: 4612098
Regulation of the bacterial cell cycle by an integrated genetic circuit.
Biondi EG, Reisinger SJ, Skerker JM, Arif M, Perchuk BS, Ryan KR, Laub MT., Nature 444(7121), 2006
PMID: 17136100
The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis.
Brilli M, Fondi M, Fani R, Mengoni A, Ferri L, Bazzicalupo M, Biondi EG., BMC Syst Biol 4(), 2010
PMID: 20426835
A Sinorhizobium meliloti minE mutant has an altered morphology and exhibits defects in legume symbiosis.
Cheng J, Sibley CD, Zaheer R, Finan TM., Microbiology (Reading, Engl.) 153(Pt 2), 2007
PMID: 17259609
VARNA: Interactive drawing and editing of the RNA secondary structure.
Darty K, Denise A, Ponty Y., Bioinformatics 25(15), 2009
PMID: 19398448
EMMA 2--a MAGE-compliant system for the collaborative analysis and integration of microarray data.
Dondrup M, Albaum SP, Griebel T, Henckel K, Junemann S, Kahlke T, Kleindt CK, Kuster H, Linke B, Mertens D, Mittard-Runte V, Neuweger H, Runte KJ, Tauch A, Tille F, Puhler A, Goesmann A., BMC Bioinformatics 10(), 2009
PMID: 19200358
A qrr noncoding RNA deploys four different regulatory mechanisms to optimize quorum-sensing dynamics.
Feng L, Rutherford ST, Papenfort K, Bagert JD, van Kessel JC, Tirrell DA, Wingreen NS, Bassler BL., Cell 160(1-2), 2015
PMID: 25579683
Spatiotemporal choreography of chromosome and megaplasmids in the Sinorhizobium meliloti cell cycle.
Frage B, Dohlemann J, Robledo M, Lucena D, Sobetzko P, Graumann PL, Becker A., Mol. Microbiol. 100(5), 2016
PMID: 26853523
The composite genome of the legume symbiont Sinorhizobium meliloti.
Galibert F, Finan TM, Long SR, Puhler A, Abola P, Ampe F, Barloy-Hubler F, Barnett MJ, Becker A, Boistard P, Bothe G, Boutry M, Bowser L, Buhrmester J, Cadieu E, Capela D, Chain P, Cowie A, Davis RW, Dreano S, Federspiel NA, Fisher RF, Gloux S, Godrie T, Goffeau A, Golding B, Gouzy J, Gurjal M, Hernandez-Lucas I, Hong A, Huizar L, Hyman RW, Jones T, Kahn D, Kahn ML, Kalman S, Keating DH, Kiss E, Komp C, Lelaure V, Masuy D, Palm C, Peck MC, Pohl TM, Portetelle D, Purnelle B, Ramsperger U, Surzycki R, Thebault P, Vandenbol M, Vorholter FJ, Weidner S, Wells DH, Wong K, Yeh KC, Batut J., Science 293(5530), 2001
PMID: 11474104
Bacterial small RNA regulators: versatile roles and rapidly evolving variations.
Gottesman S, Storz G., Cold Spring Harb Perspect Biol 3(12), 2011
PMID: 20980440
The Vienna RNA websuite.
Gruber AR, Lorenz R, Bernhart SH, Neubock R, Hofacker IL., Nucleic Acids Res. 36(Web Server issue), 2008
PMID: 18424795
Oscillating global regulators control the genetic circuit driving a bacterial cell cycle.
Holtzendorff J, Hung D, Brende P, Reisenauer A, Viollier PH, McAdams HH, Shapiro L., Science 304(5673), 2004
PMID: 15087506
A phospho-signaling pathway controls the localization and activity of a protease complex critical for bacterial cell cycle progression.
Iniesta AA, McGrath PT, Reisenauer A, McAdams HH, Shapiro L., Proc. Natl. Acad. Sci. U.S.A. 103(29), 2006
PMID: 16829582
Unraveling the universe of small RNA regulators in the legume symbiont Sinorhizobium meliloti.
Jiménez-Zurdo J., Robledo M.., 2015
Insights into the noncoding RNome of nitrogen-fixing endosymbiotic α-proteobacteria.
Jimenez-Zurdo JI, Valverde C, Becker A., Mol. Plant Microbe Interact. 26(2), 2013
PMID: 22991999
Cold Shock Proteins: A Minireview with Special Emphasis on Csp-family of Enteropathogenic Yersinia.
Keto-Timonen R, Hietala N, Palonen E, Hakakorpi A, Lindstrom M, Korkeala H., Front Microbiol 7(), 2016
PMID: 27499753
System-level design of bacterial cell cycle control.
McAdams HH, Shapiro L., FEBS Lett. 583(24), 2009
PMID: 19766635
Bacteroid formation in the Rhizobium-legume symbiosis.
Oke V, Long SR., Curr. Opin. Microbiol. 2(6), 1999
PMID: 10607628
The rules of engagement in the legume-rhizobial symbiosis.
Oldroyd GE, Murray JD, Poole PS, Downie JA., Annu. Rev. Genet. 45(), 2011
PMID: 21838550
Two separate modules of the conserved regulatory RNA AbcR1 address multiple target mRNAs in and outside of the translation initiation region.
Overloper A, Kraus A, Gurski R, Wright PR, Georg J, Hess WR, Narberhaus F., RNA Biol 11(5), 2014
PMID: 24921646
Small RNA-based feedforward loop with AND-gate logic regulates extrachromosomal DNA transfer in Salmonella.
Papenfort K, Espinosa E, Casadesus J, Vogel J., Proc. Natl. Acad. Sci. U.S.A. 112(34), 2015
PMID: 26307765
Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis.
Penterman J, Abo RP, De Nisco NJ, Arnold MF, Longhi R, Zanda M, Walker GC., Proc. Natl. Acad. Sci. U.S.A. 111(9), 2014
PMID: 24501120
Probability-based protein identification by searching sequence databases using mass spectrometry data.
Perkins DN, Pappin DJ, Creasy DM, Cottrell JS., Electrophoresis 20(18), 1999
PMID: 10612281
Cell Cycle Control by the Master Regulator CtrA in Sinorhizobium meliloti.
Pini F, De Nisco NJ, Ferri L, Penterman J, Fioravanti A, Brilli M, Mengoni A, Bazzicalupo M, Viollier PH, Walker GC, Biondi EG., PLoS Genet. 11(5), 2015
PMID: 25978424
Construction of a large signature-tagged mini-Tn5 transposon library and its application to mutagenesis of Sinorhizobium meliloti.
Pobigaylo N, Wetter D, Szymczak S, Schiller U, Kurtz S, Meyer F, Nattkemper TW, Becker A., Appl. Environ. Microbiol. 72(6), 2006
PMID: 16751548
An easy-to-use Decoy Database Builder software tool, implementing different decoy strategies for false discovery rate calculation in automated MS/MS protein identifications.
Reidegeld KA, Eisenacher M, Kohl M, Chamrad D, Korting G, Bluggel M, Meyer HE, Stephan C., Proteomics 8(6), 2008
PMID: 18338823
Conservation and Occurrence of Trans-Encoded sRNAs in the Rhizobiales.
Reinkensmeier J, Schluter JP, Giegerich R, Becker A., Genes (Basel) 2(4), 2011
PMID: 24710299
A stress-induced small RNA modulates alpha-rhizobial cell cycle progression.
Robledo M, Frage B, Wright PR, Becker A., PLoS Genet. 11(4), 2015
PMID: 25923724
Primary Characterization of Small RNAs in Symbiotic Nitrogen-Fixing Bacteria.
Robledo M, Garcia-Tomsig NI, Jimenez-Zurdo JI., Methods Mol. Biol. 1734(), 2018
PMID: 29288462
A conserved α-proteobacterial small RNA contributes to osmoadaptation and symbiotic efficiency of rhizobia on legume roots.
Robledo M, Peregrina A, Millan V, Garcia-Tomsig NI, Torres-Quesada O, Mateos PF, Becker A, Jimenez-Zurdo JI., Environ. Microbiol. 19(7), 2017
PMID: 28401641
An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing.
Roux B, Rodde N, Jardinaud MF, Timmers T, Sauviac L, Cottret L, Carrere S, Sallet E, Courcelle E, Moreau S, Debelle F, Capela D, de Carvalho-Niebel F, Gouzy J, Bruand C, Gamas P., Plant J. 77(6), 2014
PMID: 24483147
Topological control of the Caulobacter cell cycle circuitry by a polarized single-domain PAS protein.
Sanselicio S, Berge M, Theraulaz L, Radhakrishnan SK, Viollier PH., Nat Commun 6(), 2015
PMID: 25952018
Global mapping of transcription start sites and promoter motifs in the symbiotic α-proteobacterium Sinorhizobium meliloti 1021.
Schluter JP, Reinkensmeier J, Barnett MJ, Lang C, Krol E, Giegerich R, Long SR, Becker A., BMC Genomics 14(), 2013
PMID: 23497287
A genome-wide survey of sRNAs in the symbiotic nitrogen-fixing alpha-proteobacterium Sinorhizobium meliloti.
Schluter JP, Reinkensmeier J, Daschkey S, Evguenieva-Hackenberg E, Janssen S, Janicke S, Becker JD, Giegerich R, Becker A., BMC Genomics 11(), 2010
PMID: 20398411
Cell cycle-dependent adaptor complex for ClpXP-mediated proteolysis directly integrates phosphorylation and second messenger signals.
Smith SC, Joshi KK, Zik JJ, Trinh K, Kamajaya A, Chien P, Ryan KR., Proc. Natl. Acad. Sci. U.S.A. 111(39), 2014
PMID: 25197043
Quantitative proteomic analysis of the Hfq-regulon in Sinorhizobium meliloti 2011.
Sobrero P, Schluter JP, Lanner U, Schlosser A, Becker A, Valverde C., PLoS ONE 7(10), 2012
PMID: 23119037
Regulation by small RNAs in bacteria: expanding frontiers.
Storz G, Vogel J, Wassarman KM., Mol. Cell 43(6), 2011
PMID: 21925377
Independent activity of the homologous small regulatory RNAs AbcR1 and AbcR2 in the legume symbiont Sinorhizobium meliloti.
Torres-Quesada O, Millan V, Nisa-Martinez R, Bardou F, Crespi M, Toro N, Jimenez-Zurdo JI., PLoS ONE 8(7), 2013
PMID: 23869210
Genome-wide profiling of Hfq-binding RNAs uncovers extensive post-transcriptional rewiring of major stress response and symbiotic regulons in Sinorhizobium meliloti.
Torres-Quesada O, Reinkensmeier J, Schluter JP, Robledo M, Peregrina A, Giegerich R, Toro N, Becker A, Jimenez-Zurdo JI., RNA Biol 11(5), 2014
PMID: 24786641
Regulatory RNAs in bacteria.
Waters LS, Storz G., Cell 136(4), 2009
PMID: 19239884
CopraRNA and IntaRNA: predicting small RNA targets, networks and interaction domains.
Wright PR, Georg J, Mann M, Sorescu DA, Richter AS, Lott S, Kleinkauf R, Hess WR, Backofen R., Nucleic Acids Res. 42(Web Server issue), 2014
PMID: 24838564
Analysis of serum proteome profiles of non-Hodgkin lymphoma for biomarker identification.
Zhang MZ, Sun ZC, Fu XR, Nan FF, Fan QX, Wu XA, Geng L, Ma W, Wang RL., J Proteomics 72(6), 2009
PMID: 19361584


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