1887

Abstract

The discovery of non-coding RNA (ncRNA) has been mainly limited to laboratory model systems and human pathogenic bacteria. In this study, we begin to explore the ncRNA diversity in four recently sequenced environmental species ( 40B, 1DA3, VM573 and BAA-1116) by performing searches using Infernal and Rfam for the identification of putative ncRNA-encoding genes. This search method resulted in the identification of 31–38 putative ncRNA genes per species and the total ncRNA catalogue spanned an assortment of regulatory mechanisms (riboswitches, -encoded ncRNAs, -encoded ncRNAs, modulators of protein activity, ribonucleoproteins, transcription termination ncRNAs and unknown). We chose to experimentally validate the identifications for BAA-1116 using a microarray-based expression profiling strategy. Transcript hybridization to tiled probes targeting annotated BAA-1116 intergenic regions revealed that 21 of the 38 predicted ncRNA genes were expressed in mid-exponential-phase cultures grown in nutrient-rich medium. The microarray findings were confirmed by testing a subset of three highly expressed (6S, tmRNA and TPP-2) and three moderately expressed (CsrB, GcvB and purine) ncRNAs via reverse transcription PCR. Our findings provide new information on the diversity of ncRNA in environmental vibrios while simultaneously promoting a more accurate annotation of genomic intergenic regions.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.039149-0
2010-08-01
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/8/2452.html?itemId=/content/journal/micro/10.1099/mic.0.039149-0&mimeType=html&fmt=ahah

References

  1. Almeida L. G., Paixão R., Souza R. C., da Costa G. C., Barrientos F. A., Santos M. T., de Almeida D. F., Vasconcelos A. T. R. 2004; A system for automated bacterial (genome) integrated annotation – SABIA. Bioinformatics 20:2832–2833
    [Google Scholar]
  2. Altuvia S. 2007; Identification of bacterial small non-coding RNAs: experimental approaches. Curr Opin Microbiol 10:257–261
    [Google Scholar]
  3. Altuvia S., Weinstein-Fischer D., Zhang A., Postow L., Storz G. 1997; A small stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell 90:43–53
    [Google Scholar]
  4. Argaman L., Altuvia S. 2000; fhlA repression by OxyS RNA: kissing complex formation at two sites results in a stable antisense–target RNA complex. J Mol Biol 300:1101–1112
    [Google Scholar]
  5. Bartel D. P. 2004; MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297
    [Google Scholar]
  6. Bouché F., Bouché J. P. 1989; Genetic evidence that DicF, a second division inhibitor encoded by the Escherichia coli dicB operon, is probably RNA. Mol Microbiol 3:991–994
    [Google Scholar]
  7. Boysen A., Moller-Jensen J., Kallipolitis B. H., Valentin-Hansen P., Overgaard M. 2010; Translational regulation of gene expression by an anaerobically induced small non-coding RNA in Escherichia coli. J Biol Chem 285:10690–10702
    [Google Scholar]
  8. Chimetto L. A., Cleenwerck I., Alves N. Jr, Silva B. S., Brocchi M., Willems A., De Vos P., Thompson F. L. 2010; Vibrio communis sp. nov. isolated from marine animals ( Mussismilia hispida, Phyllogorgia dilatata, Palythoa caribaeorum, Palythoa variabilis and Litopenaeus vannamei. Int J Syst Evol Microbiol Mar 19Epub ahead of print]
    [Google Scholar]
  9. Davis B. M., Quinones M., Pratt J., Ding Y., Waldor M. K. 2005; Characterization of the small untranslated RNA RyhB and its regulon in Vibrio cholerae. J Bacteriol 187:4005–4014
    [Google Scholar]
  10. Dennis P. P., Omer A. 2005; Small non-coding RNAs in Archaea. Curr Opin Microbiol 8:685–694
    [Google Scholar]
  11. Eddy S. R. 2001; Non-coding RNA genes and the modern RNA world. Nat Rev Genet 2:919–929
    [Google Scholar]
  12. Eddy S. R., Durbin R. 1994; RNA sequence analysis using covariance models. Nucleic Acids Res 22:2079–2088
    [Google Scholar]
  13. Gottesman S., McCullen C. A., Guillier M., Vanderpool C. K., Majdalani N., Benhammou J., Thompson K. M., FitzGerald P. C., Sowa N. A., FitzGerald D. J. 2006; Small RNA regulators and the bacterial response to stress. Cold Spring Harb Symp Quant Biol 71:1–11
    [Google Scholar]
  14. Griffiths-Jones S., Bateman A., Khanna A., Marshall M., Eddy S. R. (2003; Rfam: an RNA family database. Nucleic Acids Res 31:439–441
    [Google Scholar]
  15. Griffiths-Jones S., Moxon S., Marshall M., Khanna A., Eddy S. R., Bateman A. 2005; Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res 33:D121–D124
    [Google Scholar]
  16. Huttenhofer A., Vogel J. 2006; Experimental approaches to identify non-coding RNAs. Nucleic Acids Res 34:635–646
    [Google Scholar]
  17. Jin Y., Watt R. M., Danchin A., Huang J. D. 2009; Small noncoding RNA GcvB is a novel regulator of acid resistance in Escherichia coli. BMC Genomics 10:165
    [Google Scholar]
  18. Karzai A. W., Susskind M. M., Sauer R. T. 1999; SmpB, a unique RNA-binding protein essential for the peptide-tagging activity of SsrA (tmRNA. EMBO J 18:3793–3799
    [Google Scholar]
  19. Kubodera T., Watanabe M., Yoshiuchi K., Yamashita N., Nishimura A., Nakai S., Gomi K., Hanamoto H. 2003; Thiamine-regulated gene expression of Aspergillus oryzae thiA requires splicing of the intron containing a riboswitch-like domain in the 5′-UTR. FEBS Lett 555:516–520
    [Google Scholar]
  20. Kulkarni P. R., Cui X., Williams J. W., Stevens A. M., Kulkarni R. V. 2006; Prediction of CsrA-regulating small RNAs in bacteria and their experimental verification in Vibrio fischeri. Nucleic Acids Res 34:3361–3369
    [Google Scholar]
  21. Lease R. A., Cusick M., Belfort M. 1998; Riboregulation in Escherichia coli: DsrA RNA acts by RNA : RNA interactions at multiple loci. Proc Natl Acad Sci U S A 95:12456–12461
    [Google Scholar]
  22. Lenz D. H., Mok K. C., Lilley B. N., Kulkarni R. V., Wingreen N. S., Bassler B. L. 2004; The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118:69–82
    [Google Scholar]
  23. Lin B., Wang Z., Malanoski A. P., O'Grady E. A., Wimpee C. F., Vuddhakul V., Alves A. Jr, Thompson F. L., Gomez-Gil B., Vora G. J. 2010; Comparative genomic analyses identify the Vibrio harveyi genome sequenced strains BAA-1116 and HY01 as Vibrio campbellii. Environ Microbiol Rep 2:81–89
    [Google Scholar]
  24. Liu J. M., Livny J., Lawrence M. S., Kimball M. D., Waldor M. K., Camilli A. 2009; Experimental discovery of ncRNAs in Vibrio cholerae by direct cloning, 5S/tRNA depletion and parallel sequencing. Nucleic Acids Res 37:e46
    [Google Scholar]
  25. Livny J., Fogel M. A., Davis B. M., Waldor M. K. 2005; ncRNAPredict: an integrative computational approach to identify ncRNAs in bacterial genomes. Nucleic Acids Res 33:4096–4105
    [Google Scholar]
  26. Majdalani N., Cunning C., Sledjeski D., Elliott T., Gottesman S. 1998; DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription. Proc Natl Acad Sci U S A 95:12462–12467
    [Google Scholar]
  27. Mandal M., Boese B., Barrick J. E., Breaker R. R. 2003; Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113:577–586
    [Google Scholar]
  28. Mata J., Marguerat S., Bahler J. 2005; Post-transcriptional control of gene expression: a genome-wide perspective. Trends Biochem Sci 30:506–514
    [Google Scholar]
  29. Mizuno T., Chou M. Y., Inouye M. 1984; A unique mechanism regulating gene expression: translational inhibition by a complementary RNA transcript (micRNA. Proc Natl Acad Sci U S A 81:1966–1970
    [Google Scholar]
  30. Moller T., Franch T., Udesen C., Gerdes K., Valentin-Hansen P. 2002; Spot 42 RNA mediates discoordinate expression of the E. coli galactose operon. Genes Dev 16:1696–1706
    [Google Scholar]
  31. Murphy E. R., Payne S. M. 2007; RyhB, an iron-responsive small RNA molecule, regulates Shigella dysenteriae virulence. Infect Immun 75:3470–3477
    [Google Scholar]
  32. Nawrocki E. P., Kolbe D. L., Eddy S. R. 2009; Infernal 1.0: inference of RNA alignments. Bioinformatics 25:1335–1337
    [Google Scholar]
  33. Oh B. K., Chauhan A. K., Isono K., Apirion D. 1990; Location of a gene ( ssrA) for a small, stable RNA (10Sa RNA) in the Escherichia coli chromosome. J Bacteriol 172:4708–4709
    [Google Scholar]
  34. Pedersen K., Gerdes K. 1999; Multiple hok genes on the chromosome of Escherichia coli. Mol Microbiol 32:1090–1102
    [Google Scholar]
  35. Romby P., Vandenesch F., Wagner E. G. 2006; The role of RNAs in the regulation of virulence-gene expression. Curr Opin Microbiol 9:229–236
    [Google Scholar]
  36. Romeo T. 1998; Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol Microbiol 29:1321–1330
    [Google Scholar]
  37. Sledjeski D., Gottesman S. 1995; A small RNA acts as an antisilencer of the H-NS-silenced rcsA gene of Escherichia coli. Proc Natl Acad Sci U S A 92:2003–2007
    [Google Scholar]
  38. Song T., Mika F., Lindmark B., Liu Z., Schild S., Bishop A., Zhu J., Camilli A., Johansson J. other authors 2008; A new Vibrio cholerae ncRNA modulates colonization and affects release of outer membrane vesicles. Mol Microbiol 70:100–111
    [Google Scholar]
  39. Sudarsan N., Barrick J. E., Breaker R. R. 2003; Metabolite-binding RNA domains are present in the genes of eukaryotes. RNA 9:644–647
    [Google Scholar]
  40. Tetart F., Bouche J. P. 1992; Regulation of the expression of the cell-cycle gene ftsZ by DicF antisense RNA. Division does not require a fixed number of FtsZ molecules. Mol Microbiol 6:615–620
    [Google Scholar]
  41. Thompson C. C., Vicente A. C., Souza R. C., Vasconcelos A. T., Vesth T., Alves N. Jr, Ussery D. W., Iida T., Thompson F. L. 2009; Genomic taxonomy of vibrios. BMC Evol Biol 9:258
    [Google Scholar]
  42. Tu K. C., Bassler B. L. 2007; Multiple small RNAs act additively to integrate sensory information and control quorum sensing in Vibrio harveyi. Genes Dev 21:221–233
    [Google Scholar]
  43. Urbanowski M. L., Stauffer L. T., Stauffer G. V. 2000; The gcvB gene encodes a small untranslated RNA involved in expression of the dipeptide and oligopeptide transport systems in Escherichia coli. Mol Microbiol 37:856–868
    [Google Scholar]
  44. Vogel J., Sharma C. M. 2005; How to find small non-coding RNAs in bacteria. Biol Chem 386:1219–1238
    [Google Scholar]
  45. Wagner E. G., Brantl S. 1998; Kissing and RNA stability in antisense control of plasmid replication. Trends Biochem Sci 23:451–454
    [Google Scholar]
  46. Wagner E. G., Altuvia S., Romby P. 2002; Antisense RNAs in bacteria and their genetic elements. Adv Genet 46:361–398
    [Google Scholar]
  47. Wassarman K. M., Storz G. 2000; 6S RNA regulates E. coli RNA polymerase activity. Cell 101:613–623
    [Google Scholar]
  48. Wassarman K. M., Zhang A., Storz G. 1999; Small RNAs in Escherichia coli. Trends Microbiol 7:37–45
    [Google Scholar]
  49. Waters L. S., Storz G. 2009; Regulatory RNAs in bacteria. Cell 136:615–628
    [Google Scholar]
  50. Winkler W., Nahvi A., Breaker R. R. 2002; Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419:952–956
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.039149-0
Loading
/content/journal/micro/10.1099/mic.0.039149-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

PDF

Supplementary material 3

PDF

Supplementary material 4

PDF

Supplementary material 5

PDF

Supplementary material 6

PDF

Supplementary material 7

PDF

Supplementary material 8

PDF

Supplementary material 9

PDF

Supplementary material 10

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error