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PMID: 17971083 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Identification of differentially expressed small non-coding RNAs in the legume endosymbiont Sinorhizobium meliloti by comparative genomics.

Molecular microbiology ·Vol. 66 ·No. 5 ·2007-12-00 ·Pages 1080-91

del Val C, Rivas E, Torres-Quesada O, Toro N, Jiménez-Zurdo JI

Abstract

Bacterial small non-coding RNAs (sRNAs) are being recognized as novel widespread regulators of gene expression in response to environmental signals. Here, we present the first search for sRNA-encoding genes in the nitrogen-fixing endosymbiont Sinorhizobium meliloti, performed by a genome-wide computational analysis of its intergenic regions. Comparative sequence data from eight related alpha-proteobacteria were obtained, and the interspecies pairwise alignments were scored with the programs eQRNA and RNAz as complementary predictive tools to identify conserved and stable secondary structures corresponding to putative non-coding RNAs. Northern experiments confirmed that eight of the predicted loci, selected among the original 32 candidates as most probable sRNA genes, expressed small transcripts. This result supports the combined use of eQRNA and RNAz as a robust strategy to identify novel sRNAs in bacteria. Furthermore, seven of the transcripts accumulated differentially in free-living and symbiotic conditions. Experimental mapping of the 5'-ends of the detected transcripts revealed that their encoding genes are organized in autonomous transcription units with recognizable promoter and, in most cases, termination signatures. These findings suggest novel regulatory functions for sRNAs related to the interactions of alpha-proteobacteria with their eukaryotic hosts.

MeSH Terms
Blotting, Northern Computational Biology/methods DNA, Intergenic Fabaceae/microbiology Genome, Bacterial/genetics Nucleic Acid Conformation Promoter Regions, Genetic RNA, Bacterial/biosynthesis,genetics RNA, Double-Stranded/genetics RNA, Untranslated/biosynthesis,genetics Sinorhizobium meliloti/chemistry,genetics,physiology Transcription, Genetic
Chemicals
DNA, Intergenic RNA, Bacterial RNA, Double-Stranded RNA, Untranslated
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
del Val Coral
Department of Computer Science and Artificial Intelligence, E.T.S.I. Informatics, Universidad de Granada, Daniel Saucedo s/n, 18071 Granada, Spain.
Rivas Elena
Torres-Quesada Omar
Toro Nicolás
Jiménez-Zurdo José I
References (51)
51 references, click to expand
  1. Noncoding RNA gene detection using comparative sequence analysis.
    BMC Bioinformatics. 2001;2:8 PMID: 11801179
  2. RegulonDB (version 4.0): transcriptional regulation, operon organization and growth conditions in Escherichia coli K-12.
    Nucleic Acids Res. 2004 Jan 1;32(Database issue):D303-6 PMID: 14681419
  3. A computational approach to identify genes for functional RNAs in genomic sequences.
    Nucleic Acids Res. 2001 Oct 1;29(19):3928-38 PMID: 11574674
  4. Global analysis of small RNA and mRNA targets of Hfq.
    Mol Microbiol. 2003 Nov;50(4):1111-24 PMID: 14622403
  5. The composite genome of the legume symbiont Sinorhizobium meliloti.
    Science. 2001 Jul 27;293(5530):668-72 PMID: 11474104
  6. A survey of small RNA-encoding genes in Escherichia coli.
    Nucleic Acids Res. 2003 Apr 1;31(7):1813-20 PMID: 12654996
  7. Noncoding RNA genes identified in AT-rich hyperthermophiles.
    Proc Natl Acad Sci U S A. 2002 May 28;99(11):7542-7 PMID: 12032319
  8. An abundance of RNA regulators.
    Annu Rev Biochem. 2005;74:199-217 PMID: 15952886
  9. A global analysis of protein expression profiles in Sinorhizobium meliloti: discovery of new genes for nodule occupancy and stress adaptation.
    Mol Plant Microbe Interact. 2003 Jun;16(6):508-24 PMID: 12795377
  10. Fast and reliable prediction of noncoding RNAs.
    Proc Natl Acad Sci U S A. 2005 Feb 15;102(7):2454-9 PMID: 15665081
  11. Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions.
    Mol Plant Microbe Interact. 2004 Mar;17(3):292-303 PMID: 15000396
  12. Controlling mRNA stability and translation with small, noncoding RNAs.
    Curr Opin Microbiol. 2004 Apr;7(2):140-4 PMID: 15063850
  13. DNA binding sites: representation and discovery.
    Bioinformatics. 2000 Jan;16(1):16-23 PMID: 10812473
  14. Ethylene-mediated phenotypic plasticity in root nodule development on Sesbania rostrata.
    Proc Natl Acad Sci U S A. 1998 Oct 13;95(21):12724-8 PMID: 9770553
  15. Identification of small RNAs in diverse bacterial species.
    Curr Opin Microbiol. 2007 Apr;10(2):96-101 PMID: 17383222
  16. Genes for small, noncoding RNAs under sporulation control in Bacillus subtilis.
    J Bacteriol. 2006 Jan;188(2):532-41 PMID: 16385044
  17. A dual-genome Symbiosis Chip for coordinate study of signal exchange and development in a prokaryote-host interaction.
    Proc Natl Acad Sci U S A. 2004 Nov 23;101(47):16636-41 PMID: 15542588
  18. An expanding universe of noncoding RNAs.
    Science. 2002 May 17;296(5571):1260-3 PMID: 12016301
  19. The evolution of chronic infection strategies in the alpha-proteobacteria.
    Nat Rev Microbiol. 2004 Dec;2(12):933-45 PMID: 15550939
  20. Evolutionary models for insertions and deletions in a probabilistic modeling framework.
    BMC Bioinformatics. 2005 Mar 21;6:63 PMID: 15780137
  21. Query-dependent banding (QDB) for faster RNA similarity searches.
    PLoS Comput Biol. 2007 Mar 30;3(3):e56 PMID: 17397253
  22. Small RNAs in bacteria: diverse regulators of gene expression in response to environmental changes.
    Cell. 2002 Apr 19;109(2):141-4 PMID: 12007399
  23. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli.
    Curr Biol. 2001 Jun 26;11(12):941-50 PMID: 11448770
  24. Identification of new noncoding RNAs in Listeria monocytogenes and prediction of mRNA targets.
    Nucleic Acids Res. 2007;35(3):962-74 PMID: 17259222
  25. R factor transfer in Rhizobium leguminosarum.
    J Gen Microbiol. 1974 Sep;84(1):188-98 PMID: 4612098
  26. RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria.
    Nucleic Acids Res. 2003 Nov 15;31(22):6435-43 PMID: 14602901
  27. Regulation and function of rhizobial nodulation genes.
    FEMS Microbiol Rev. 1993 Jan;10(1-2):39-63 PMID: 8431309
  28. Small RNAs in Escherichia coli.
    Trends Microbiol. 1999 Jan;7(1):37-45 PMID: 10068996
  29. WU-Blast2 server at the European Bioinformatics Institute.
    Nucleic Acids Res. 2003 Jul 1;31(13):3795-8 PMID: 12824421
  30. NONCODE: an integrated knowledge database of non-coding RNAs.
    Nucleic Acids Res. 2005 Jan 1;33(Database issue):D112-5 PMID: 15608158
  31. sRNAPredict: an integrative computational approach to identify sRNAs in bacterial genomes.
    Nucleic Acids Res. 2005 Jul 26;33(13):4096-105 PMID: 16049021
  32. Small RNA genes expressed from Staphylococcus aureus genomic and pathogenicity islands with specific expression among pathogenic strains.
    Proc Natl Acad Sci U S A. 2005 Oct 4;102(40):14249-54 PMID: 16183745
  33. Conserved motifs in a divergent nod box of Azorhizobium caulinodans ORS571 reveal a common structure in promoters regulated by LysR-type proteins.
    Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1646-50 PMID: 1542656
  34. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae.
    Cell. 2004 Jul 9;118(1):69-82 PMID: 15242645
  35. Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake.
    Genome Biol. 2007;8(2):R22 PMID: 17313685
  36. Identification of cyanobacterial non-coding RNAs by comparative genome analysis.
    Genome Biol. 2005;6(9):R73 PMID: 16168080
  37. Small noncoding RNAs controlling pathogenesis.
    Curr Opin Microbiol. 2007 Apr;10(2):182-8 PMID: 17383223
  38. Identification of Sinorhizobium meliloti genes regulated during symbiosis.
    J Bacteriol. 2000 Jul;182(13):3632-7 PMID: 10850975
  39. Antisense RNAs in bacteria and their genetic elements.
    Adv Genet. 2002;46:361-98 PMID: 11931231
  40. Host-Symbiont Interactions : V. THE STRUCTURE OF ACIDIC EXTRACELLULAR POLYSACCHARIDES SECRETED BY RHIZOBIUM LEGUMINOSARUM AND RHIZOBIUM TRIFOLII.
    Plant Physiol. 1981 Mar;67(3):389-400 PMID: 16661681
  41. Organogenesis of legume root nodules.
    Int Rev Cytol. 2004;234:201-62 PMID: 15066376
  42. Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: the RpoS paradigm.
    Mol Microbiol. 2003 May;48(4):855-61 PMID: 12753181
  43. The expression of a novel antisense gene mediates incompatibility within the large repABC family of alpha-proteobacterial plasmids.
    Mol Microbiol. 2005 Jan;55(2):611-23 PMID: 15659174
  44. Intergenic sequence inspector: searching and identifying bacterial RNAs.
    Bioinformatics. 2003 Sep 1;19(13):1707-9 PMID: 15593399
  45. Identification of 17 Pseudomonas aeruginosa sRNAs and prediction of sRNA-encoding genes in 10 diverse pathogens using the bioinformatic tool sRNAPredict2.
    Nucleic Acids Res. 2006;34(12):3484-93 PMID: 16870723
  46. Computational identification of noncoding RNAs in E. coli by comparative genomics.
    Curr Biol. 2001 Sep 4;11(17):1369-73 PMID: 11553332
  47. Characterization and expression patterns of Sinorhizobium meliloti tmRNA (ssrA).
    FEMS Microbiol Lett. 2007 Apr;269(1):117-23 PMID: 17241239
  48. Hfq: a bacterial Sm-like protein that mediates RNA-RNA interaction.
    Mol Cell. 2002 Jan;9(1):23-30 PMID: 11804583
  49. Method for Testing Degree of Infectivity of Rhizobium meliloti Strains.
    Appl Environ Microbiol. 1980 May;39(5):967-70 PMID: 16345574
  50. Identification of novel small RNAs using comparative genomics and microarrays.
    Genes Dev. 2001 Jul 1;15(13):1637-51 PMID: 11445539
  51. A bioinformatics based approach to discover small RNA genes in the Escherichia coli genome.
    Biosystems. 2002 Mar-May;65(2-3):157-77 PMID: 12069726
Article Info
Journal
Molecular microbiology
Abbr.
Mol Microbiol
ISSN
0950-382X
Published
2007-12-00
Epub
2007-00-25
Pages
1080-91
Language
English
Region
England
NLM ID
8712028
PMCID
PMC2780559
Subset
IM
Grants
NIGMS NIH HHS · R01 GM070538 · United States
NIGMS NIH HHS · R01GM070538-02 · United States
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