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, Schlueter J-P, Robledo M, Peregrina A, Giegerich R, Toro N, Becker A, Jimenez-Zurdo JI (2014)
RNA Biology 11(5): 563-579.

Download
No fulltext has been uploaded. References only!
Journal Article | Original Article | Published | English

No fulltext has been uploaded

Author
; ; ; ; ; ; ; ;
Abstract
The RNA chaperone Hfq is a global post-transcriptional regulator in bacteria. Here, we used RNAseq to analyze RNA populations from the legume symbiont Sinorhizobium meliloti that were co-immunoprecipitated (CoIP-RNA) with a FLAG-tagged Hfq in five growth/stress conditions. Hfq-bound transcripts (1315) were largely identified in stressed bacteria and derived from small RNAs (sRNAs), both trans-encoded (6.4%) and antisense (asRNAs; 6.3%), and mRNAs (86%). Pull-down with Hfq recovered a small proportion of annotated S. meliloti sRNAs (14% of trans-sRNAs and 2% of asRNAs) suggesting a discrete impact of this protein in sRNA pathways. Nonetheless, Hfq selectively stabilized CoIP-enriched sRNAs, anticipating that these interactions are functionally significant. Transcription of 26 Hfq-bound sRNAs was predicted to occur from promoters recognized by the major stress s factors sigma(E2) or sigma(H1/2). Recovery rates of sRNAs in each of the CoIP-RNA libraries suggest a large impact of Hfq-assisted riboregulation in S. meliloti osmoadaptation. Hfq directly targeted 18% of the predicted S. meliloti mRNAs, which encode functionally diverse proteins involved in transport and metabolism, sigma(E2)-dependent stress responses, quorum sensing, flagella biosynthesis, ribosome, and membrane assembly or symbiotic nitrogen fixation. Canonical targeting of the 5' regions of two of the ABC transporter mRNAs by the homologous Hfq-binding AbcR1 and AbcR2 sRNAs leading to inhibition of protein synthesis was confirmed in vivo. We therefore provide a comprehensive resource for the systems-level deciphering of hitherto unexplored S. meliloti stress and symbiotic post-transcriptional regulons and the identification of Hfq-dependent sRNA-mRNA regulatory pairs.
Publishing Year
ISSN
eISSN
PUB-ID

Cite this

Torres-Quesada O, Reinkensmeier J, Schlueter J-P, et al. Genome-wide profiling of Hfq-binding RNAs uncovers extensive post-transcriptional rewiring of major stress response and symbiotic regulons in Sinorhizobium meliloti. RNA Biology. 2014;11(5):563-579.
Torres-Quesada, O., Reinkensmeier, J., Schlueter, J. - P., Robledo, M., Peregrina, A., Giegerich, R., Toro, N., et al. (2014). Genome-wide profiling of Hfq-binding RNAs uncovers extensive post-transcriptional rewiring of major stress response and symbiotic regulons in Sinorhizobium meliloti. RNA Biology, 11(5), 563-579. doi:10.4161/rna.28239
Torres-Quesada, O., Reinkensmeier, J., Schlueter, J. - P., Robledo, M., Peregrina, A., Giegerich, R., Toro, N., Becker, A., and Jimenez-Zurdo, J. I. (2014). Genome-wide profiling of Hfq-binding RNAs uncovers extensive post-transcriptional rewiring of major stress response and symbiotic regulons in Sinorhizobium meliloti. RNA Biology 11, 563-579.
Torres-Quesada, O., et al., 2014. Genome-wide profiling of Hfq-binding RNAs uncovers extensive post-transcriptional rewiring of major stress response and symbiotic regulons in Sinorhizobium meliloti. RNA Biology, 11(5), p 563-579.
O. Torres-Quesada, et al., “Genome-wide profiling of Hfq-binding RNAs uncovers extensive post-transcriptional rewiring of major stress response and symbiotic regulons in Sinorhizobium meliloti”, RNA Biology, vol. 11, 2014, pp. 563-579.
Torres-Quesada, O., Reinkensmeier, J., Schlueter, J.-P., Robledo, M., Peregrina, A., Giegerich, R., Toro, N., Becker, A., Jimenez-Zurdo, J.I.: Genome-wide profiling of Hfq-binding RNAs uncovers extensive post-transcriptional rewiring of major stress response and symbiotic regulons in Sinorhizobium meliloti. RNA Biology. 11, 563-579 (2014).
Torres-Quesada, Omar, Reinkensmeier, Jan, Schlueter, Jan-Philip, Robledo, Marta, Peregrina, Alexandra, Giegerich, Robert, Toro, Nicolas, Becker, Anke, and Jimenez-Zurdo, Jose I. “Genome-wide profiling of Hfq-binding RNAs uncovers extensive post-transcriptional rewiring of major stress response and symbiotic regulons in Sinorhizobium meliloti”. RNA Biology 11.5 (2014): 563-579.
This data publication is cited in the following publications:
This publication cites the following data publications:

21 Citations in Europe PMC

Data provided by Europe PubMed Central.

Expression of the small regulatory RNA gene mmgR is regulated negatively by AniA and positively by NtrC in Sinorhizobium meliloti 2011.
Ceizel Borella G, Lagares A Jr, Valverde C., Microbiology (Reading, Engl.) 164(1), 2018
PMID: 29214973
An account of evolutionary specialization: the AbcR small RNAs in the Rhizobiales.
Sheehan LM, Caswell CC., Mol. Microbiol. 107(1), 2018
PMID: 29076560
RNA silencing in plant symbiotic bacteria: Insights from a protein-centric view.
Jimenez-Zurdo JI, Robledo M., RNA Biol 14(12), 2017
PMID: 28805544
Sinorhizobium meliloti YbeY is an endoribonuclease with unprecedented catalytic features, acting as silencing enzyme in riboregulation.
Saramago M, Peregrina A, Robledo M, Matos RG, Hilker R, Serrania J, Becker A, Arraiano CM, Jimenez-Zurdo JI., Nucleic Acids Res. 45(3), 2017
PMID: 28180335
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
Regulation of Polyhydroxybutyrate Accumulation in Sinorhizobium meliloti by the Trans-Encoded Small RNA MmgR.
Lagares A Jr, Ceizel Borella , Linne U, Becker A, Valverde C., J. Bacteriol. 199(8), 2017
PMID: 28167519
Functional analysis of the two cyclophilin isoforms of Sinorhizobium meliloti.
Thomloudi EE, Skagia A, Venieraki A, Katinakis P, Dimou M., World J. Microbiol. Biotechnol. 33(2), 2017
PMID: 28058638
Non-coding RNAs as antibiotic targets.
Colameco S, Elliot MA., Biochem. Pharmacol. 133(), 2017
PMID: 28012959
Several Hfq-dependent alterations in physiology of Yersinia enterocolitica O:3 are mediated by derepression of the transcriptional regulator RovM.
Leskinen K, Pajunen MI, Varjosalo M, Fernandez-Carrasco H, Bengoechea JA, Skurnik M., Mol. Microbiol. 103(6), 2017
PMID: 28010054
Regulation of fixLJ by Hfq Controls Symbiotically Important Genes in Sinorhizobium meliloti.
Gao M, Nguyen H, Salas Gonzalez I, Teplitski M., Mol. Plant Microbe Interact. 29(11), 2016
PMID: 27712144
C-terminal domain of the RNA chaperone Hfq drives sRNA competition and release of target RNA.
Santiago-Frangos A, Kavita K, Schu DJ, Gottesman S, Woodson SA., Proc. Natl. Acad. Sci. U.S.A. 113(41), 2016
PMID: 27681631
The novel regulatory ncRNA, NfiS, optimizes nitrogen fixation via base pairing with the nitrogenase gene nifK mRNA in Pseudomonas stutzeri A1501.
Zhan Y, Yan Y, Deng Z, Chen M, Lu W, Lu C, Shang L, Yang Z, Zhang W, Wang W, Li Y, Ke Q, Lu J, Xu Y, Zhang L, Xie Z, Cheng Q, Elmerich C, Lin M., Proc. Natl. Acad. Sci. U.S.A. 113(30), 2016
PMID: 27407147
Riboregulation of bacterial and archaeal transposition.
Ellis MJ, Haniford DB., Wiley Interdiscip Rev RNA 7(3), 2016
PMID: 26846462
The stress-related, rhizobial small RNA RcsR1 destabilizes the autoinducer synthase encoding mRNA sinI in Sinorhizobium meliloti.
Baumgardt K, Smidova K, Rahn H, Lochnit G, Robledo M, Evguenieva-Hackenberg E., RNA Biol 13(5), 2016
PMID: 26588798
Use of siRNA molecular beacons to detect and attenuate mycobacterial infection in macrophages.
George R, Cavalcante R, Carvalho C Jr, Marques E, Waugh JB, Unlap MT., World J Exp Med 5(3), 2015
PMID: 26309818
Modulation of Sinorhizobium meliloti quorum sensing by Hfq-mediated post-transcriptional regulation of ExpR.
Gao M, Tang M, Guerich L, Salas-Gonzalez I, Teplitski M., Environ Microbiol Rep 7(1), 2015
PMID: 25382642
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
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

84 References

Data provided by Europe PubMed Central.

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

AUTHOR UNKNOWN, 0
A portal for rhizobial genomes: RhizoGATE integrates a Sinorhizobium meliloti genome annotation update with postgenome data.
Becker A, Barnett MJ, Capela D, Dondrup M, Kamp PB, Krol E, Linke B, Ruberg S, Runte K, Schroeder BK, Weidner S, Yurgel SN, Batut J, Long SR, Puhler A, Goesmann A., J. Biotechnol. 140(1-2), 2009
PMID: 19103235
Fast mapping of short sequences with mismatches, insertions and deletions using index structures.
Hoffmann S, Otto C, Kurtz S, Sharma CM, Khaitovich P, Vogel J, Stadler PF, Hackermuller J., PLoS Comput. Biol. 5(9), 2009
PMID: 19750212
Mapping and quantifying mammalian transcriptomes by RNA-Seq.
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B., Nat. Methods 5(7), 2008
PMID: 18516045
Differential expression analysis for sequence count data.
Anders S, Huber W., Genome Biol. 11(10), 2010
PMID: 20979621
Significant speedup of database searches with HMMs by search space reduction with PSSM family models.
Beckstette M, Homann R, Giegerich R, Kurtz S., Bioinformatics 25(24), 2009
PMID: 19828575
Freiburg RNA Tools: a web server integrating INTARNA, EXPARNA and LOCARNA.
Smith C, Heyne S, Richter AS, Will S, Backofen R., Nucleic Acids Res. 38(Web Server issue), 2010
PMID: 20444875

Export

0 Marked Publications

Open Data PUB

Web of Science

View record in Web of Science®

Sources

PMID: 24786641
PubMed | Europe PMC

Search this title in

Google Scholar