Genome-wide detection of predicted non-coding RNAs in Rhizobium etli expressed during free-living and host-associated growth using a high-resolution tiling array

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Vercruysse, Maarten ^a   Fauvart, Maarten ^a   Cloots, Lore ^a   Engelen, Kristof ^a   Thijs, Inge M ^a   Marchal, Kathleen ^a   Michiels, Jan ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSFER RNA; UNTRANSLATED RNA; BACTERIAL RNA;

ALPHAPROTEOBACTERIA; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENETICS; BACTERIAL GROWTH; EVOLUTIONARY ADAPTATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC ANALYSIS; HOST; HOST PATHOGEN INTERACTION; MICROARRAY ANALYSIS; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PHASEOLUS VULGARIS; PLASMID; PREDICTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHIZOBIUM ETLI; ALGORITHM; BACTERIAL GENOME; BIOLOGY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; METHODOLOGY; SEQUENCE ANALYSIS;

ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); EUKARYOTA; GAMMAPROTEOBACTERIA; PROTEOBACTERIA; RHIZOBIUM; RHIZOBIUM ETLI;

ALGORITHMS; COMPUTATIONAL BIOLOGY; GENE EXPRESSION PROFILING; GENOME, BACTERIAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RHIZOBIUM ETLI; RNA, BACTERIAL; RNA, UNTRANSLATED; SEQUENCE ANALYSIS, RNA;

EID: 76949103628     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-53     Document Type: Article

References (64)

1. Brownlee GG. Sequence of 6S RNA of E. coli. Nat New Biol 1971, 229:147-149.
2. Stougaard P, Molin S, Nordstrom K. RNAs involved in copy-number control and incompatibility of plasmid R1. Proc Natl Acad Sci USA 1981, 78:6008-6012. 348966, 6171808.
3. Gottesman S. Micros for microbes: non-coding regulatory RNAs in bacteria. Trends Genet 2005, 21:399-404.
4. Storz G, Altuvia S, Wassarman KM. An abundance of RNA regulators. Annu Rev Biochem 2005, 74:199-217.
5. Vogel J, Sharma CM. How to find small non-coding RNAs in bacteria. Biol Chem 2005, 386:1219-1238.
6. Wassarman KM. Small RNAs in bacteria: diverse regulators of gene expression in response to environmental changes. Cell 2002, 109:141-144.
7. Waters LS, Storz G. Regulatory RNAs in bacteria. Cell 2009, 136:615-628.
8. Brantl S. Regulatory mechanisms employed by cis-encoded antisense RNAs. Curr Opin Microbiol 2007, 10:102-109.
9. Babitzke P, Romeo T. CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 2007, 10:156-163.
10. Winkler WC. Riboswitches and the role of noncoding RNAs in bacterial metabolic control. Curr Opin Chem Biol 2005, 9:594-602.
11. Johansson J. RNA thermosensors in bacterial pathogens. Contrib Microbiol 2009, 16:150-160.
12. Sorek R, Kunin V, Hugenholtz P. CRISPR--a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 2008, 6:181-186.
13. Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EG, Margalit H, Altuvia S. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 2001, 11:941-950.
14. Chen S, Lesnik EA, Hall TA, Sampath R, Griffey RH, Ecker DJ, Blyn LB. A bioinformatics based approach to discover small RNA genes in the Escherichia coli genome. Biosystems 2002, 65:157-177.
15. Rivas E, Klein RJ, Jones TA, Eddy SR. Computational identification of noncoding RNAs in E. coli by comparative genomics. Curr Biol 2001, 11:1369-1373.
16. Wassarman KM, Repoila F, Rosenow C, Storz G, Gottesman S. Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev 2001, 15:1637-1651. 312727, 11445539.
17. Saito S, Kakeshita H, Nakamura K. Novel small RNA-encoding genes in the intergenic regions of Bacillus subtilis. Gene 2009, 428:2-8.
18. Livny J, Brencic A, Lory S, Waldor MK. 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, 34:3484-3493. 1524904, 16870723.
19. Pichon C, Felden B. Small RNA genes expressed from Staphylococcus aureus genomic and pathogenicity islands with specific expression among pathogenic strains. Proc Natl Acad Sci USA 2005, 102:14249-14254. 1242290, 16183745.
20. Swiercz JP, Hindra, Bobek J, Haiser HJ, Di Berardo C, Tjaden B, Elliot MA. Small non-coding RNAs in Streptomyces coelicolor. Nucleic Acids Res 2008, 36:7240-7251. 2602773, 19008244.
21. Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, Binnewies TT, Hinton JC, Vogel J. Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet 2008, 4:e1000163. 2515195, 18725932.
22. Mandin P, Repoila F, Vergassola M, Geissmann T, Cossart P. Identification of new noncoding RNAs in Listeria monocytogenes and prediction of mRNA targets. Nucleic Acids Res 2007, 35:962-974. 1807966, 17259222.
23. Arnvig KB, Young DB. Identification of small RNAs in Mycobacterium tuberculosis. Mol Microbiol 2009, 73:397-408. 2764107, 19555452.
24. Livny J, Waldor MK. Identification of small RNAs in diverse bacterial species. Curr Opin Microbiol 2007, 10:96-101.
25. Altuvia S. Identification of bacterial small non-coding RNAs: experimental approaches. Curr Opin Microbiol 2007, 10:257-261.
26. Landt SG, Abeliuk E, McGrath PT, Lesley JA, McAdams HH, Shapiro L. Small non-coding RNAs in Caulobacter crescentus. Mol Microbiol 2008, 68:600-614.
27. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, Balestrino D, Loh E, Gripenland J, Tiensuu T, Vaitkevicius K, Barthelemy M, Vergassola M, Nahori MA, Soubigou G, Regnault B, Coppee JY, Lecuit M, Johansson J, Cossart P. The Listeria transcriptional landscape from saprophytism to virulence. Nature 2009, 459:950-956.
28. Braeken K, Fauvart M, Vercruysse M, Beullens S, Lambrichts I, Michiels J. Pleiotropic effects of a rel mutation on stress survival of Rhizobium etli CNPAF512. BMC Microbiol 2008, 8:219. 2631030, 19077212.
29. Fauvart M, Michiels J. Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis. FEMS Microbiol Lett 2008, 285:1-9.
30. Moris M, Braeken K, Schoeters E, Verreth C, Beullens S, Vanderleyden J, Michiels J. Effective symbiosis between Rhizobium etli and Phaseolus vulgaris requires the alarmone ppGpp. J Bacteriol 2005, 187:5460-5469. 1196010, 16030240.
31. D'Hooghe I, Michiels J, Vlassak K, Verreth C, Waelkens F, Vanderleyden J. Structural and functional analysis of the fixLJ genes of Rhizobium leguminosarum biovar phaseoli CNPAF512. Mol Gen Genet 1995, 249:117-126.
32. D'Hooghe I, Wauven C, Michiels J, Tricot C, de Wilde P, Vanderleyden J, Stalon V. The arginine deiminase pathway in Rhizobium etli: DNA sequence analysis and functional study of the arcABC genes. J Bacteriol 1997, 179:7403-7409. 179691, 9393705.
33. Bhagwat AA, Phadke RP, Wheeler D, Kalantre S, Gudipati M, Bhagwat M. Computational methods and evaluation of RNA stabilization reagents for genome-wide expression studies. J Microbiol Methods 2003, 55:399-409.
34. Becker A, Berges H, Krol E, Bruand C, Ruberg S, Capela D, Lauber E, Meilhoc E, Ampe F, de Bruijn FJ, Fourment J, Francez-Charlot A, Kahn D, Kuster H, Liebe C, Puhler A, Weidner S, Batut J. Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions. Mol Plant Microbe Interact 2004, 17:292-303.
35. Capela D, Filipe C, Bobik C, Batut J, Bruand C. Sinorhizobium meliloti differentiation during symbiosis with Alfalfa: a transcriptomic dissection. Mol Plant Microbe Interact 2006, 19:363-372.
36. Spaniolas S, Bazakos C, Awad M, Kalaitzis P. Exploitation of the chloroplast trnL (UAA) intron polymorphisms for the authentication of plant oils by means of a lab-on-a-chip capillary electrophoresis system. J Agric Food Chem 2008, 56:6886-6891.
37. Nuwaysir EF, Huang W, Albert TJ, Singh J, Nuwaysir K, Pitas A, Richmond T, Gorski T, Berg JP, Ballin J, McCormick M, Norton J, Pollock T, Sumwalt T, Butcher L, Porter D, Molla M, Hall C, Blattner F, Sussman MR, Wallace RL, Cerrina F, Green RD. Gene expression analysis using oligonucleotide arrays produced by maskless photolithography. Genome Res 2002, 12:1749-1755. 187555, 12421762.
38. Nelson CM, Herron MJ, Felsheim RF, Schloeder BR, Grindle SM, Chavez AO, Kurtti TJ, Munderloh UG. Whole genome transcription profiling of Anaplasma phagocytophilum in human and tick host cells by tiling array analysis. BMC Genomics 2008, 9:364. 2527338, 18671858.
39. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 2002, 30:e15. 100354, 11842121.
40. Tukey JW. Exploratory Data Analysis. 1977, Addison-Wesley, Menlo Park, First.
41. del Val C, Rivas E, Torres-Quesada O, Toro N, Jimenez-Zurdo JI. Identification of differentially expressed small non-coding RNAs in the legume endosymbiont Sinorhizobium meliloti by comparative genomics. Mol Microbiol 2007, 66:1080-1091. 2780559, 17971083.
42. Ulve VM, Sevin EW, Cheron A, Barloy-Hubler F. Identification of chromosomal alpha-proteobacterial small RNAs by comparative genome analysis and detection in Sinorhizobium meliloti strain 1021. BMC Genomics 2007, 8:467. 2245857, 18093320.
43. Weinberg Z, Barrick JE, Yao Z, Roth A, Kim JN, Gore J, Wang JX, Lee ER, Block KF, Sudarsan N, Neph S, Tompa M, Ruzzo WL, Breaker RR. Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline. Nucleic Acids Res 2007, 35:4809-4819. 1950547, 17621584.
44. Livny J, Teonadi H, Livny M, Waldor MK. High-throughput, kingdom-wide prediction and annotation of bacterial non-coding RNAs. PLoS ONE 2008, 3:e3197. 2527527, 18787707.
45. Valverde C, Livny J, Schluter JP, Reinkensmeier J, Becker A, Parisi G. Prediction of Sinorhizobium meliloti sRNA genes and experimental detection in strain 2011. BMC Genomics 2008, 9:416. 2573895, 18793445.
46. Abreu-Goodger C, Merino E. RibEx: a web server for locating riboswitches and other conserved bacterial regulatory elements. Nucleic Acids Res 2005, 33:W690-692. 1160206, 15980564.
47. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45. 55695, 11328886.
48. Wassarman KM, Storz G. 6S RNA regulates E. coli RNA polymerase activity. Cell 2000, 101:613-623.
49. Wassarman KM. 6S RNA: a regulator of transcription. Mol Microbiol 2007, 65:1425-1431.
50. Regalia M, Rosenblad MA, Samuelsson T. Prediction of signal recognition particle RNA genes. Nucleic Acids Res 2002, 30:3368-3377. 137091, 12140321.
51. Rosenblad MA, Gorodkin J, Knudsen B, Zwieb C, Samuelsson T. SRPDB: Signal Recognition Particle Database. Nucleic Acids Res 2003, 31:363-364. 165554, 12520023.
52. Evans D, Marquez SM, Pace NR. RNase P: interface of the RNA and protein worlds. Trends Biochem Sci 2006, 31:333-341.
53. Gur E, Sauer RT. Evolution of the ssrA degradation tag in Mycoplasma: specificity switch to a different protease. Proc Natl Acad Sci USA 2008, 105:16113-16118. 2570983, 18852454.
54. Nudler E, Mironov AS. The riboswitch control of bacterial metabolism. Trends Biochem Sci 2004, 29:11-17.
55. Miranda-Rios J, Morera C, Taboada H, Davalos A, Encarnacion S, Mora J, Soberon M. Expression of thiamin biosynthetic genes (thiCOGE) and production of symbiotic terminal oxidase cbb3 in Rhizobium etli. J Bacteriol 1997, 179:6887-6893. 179625, 9371431.
56. Miranda-Rios J, Navarro M, Soberon M. A conserved RNA structure (thi box) is involved in regulation of thiamin biosynthetic gene expression in bacteria. Proc Natl Acad Sci USA 2001, 98:9736-9741. 55522, 11470904.
57. MacLellan SR, Smallbone LA, Sibley CD, Finan TM. The expression of a novel antisense gene mediates incompatibility within the large repABC family of alpha-proteobacterial plasmids. Mol Microbiol 2005, 55:611-623.
58. Izquierdo J, Venkova-Canova T, Ramirez-Romero MA, Tellez-Sosa J, Hernandez-Lucas I, Sanjuan J, Cevallos MA. An antisense RNA plays a central role in the replication control of a repC plasmid. Plasmid 2005, 54:259-277.
59. Vogel J, Bartels V, Tang TH, Churakov G, Slagter-Jager JG, Huttenhofer A, Wagner EG. RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res 2003, 31:6435-6443. 275561, 14602901.
60. Kawano M, Reynolds AA, Miranda-Rios J, Storz G. Detection of 5'- and 3'-UTR-derived small RNAs and cis-encoded antisense RNAs in Escherichia coli. Nucleic Acids Res 2005, 33:1040-1050. 549416, 15718303.
61. Guillier M, Gottesman S. The 5' end of two redundant sRNAs is involved in the regulation of multiple targets, including their own regulator. Nucleic Acids Res 2008, 36:6781-6794. 2588501, 18953042.
62. Michiels J, Van Soom T, D'Hooghe I, Dombrecht B, Benhassine T, de Wilde P, Vanderleyden J. The Rhizobium etli rpoN locus: DNA sequence analysis and phenotypical characterization of rpoN, ptsN, and ptsA mutants. J Bacteriol 1998, 180:1729-1740. 107084, 9537369.
63. Kulkarni PR, Cui X, Williams JW, Stevens AM, Kulkarni RV. Prediction of CsrA-regulating small RNAs in bacteria and their experimental verification in Vibrio fischeri. Nucleic Acids Res 2006, 34:3361-3369. 1488887, 16822857.
64. Wilderman PJ, Sowa NA, FitzGerald DJ, FitzGerald PC, Gottesman S, Ochsner UA, Vasil ML. Identification of tandem duplicate regulatory small RNAs in Pseudomonas aeruginosa involved in iron homeostasis. Proc Natl Acad Sci USA 2004, 101:9792-9797. 470753, 15210934.