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The transcriptionally active regions in the genome of Bacillus subtilis

Simon Rasmussen, Henrik Bjørn Nielsen, Hanne Jarmer

Molecular Microbiology · 2009

doi:10.1111/j.1365-2958.2009.06830.x

Abstract

Summary The majority of all genes have so far been identified and annotated systematically through in silico gene finding. Here we report the finding of 3662 strand‐specific transcriptionally active regions (TARs) in the genome of Bacillus subtilis by the use of tiling arrays. We have measured the genome‐wide expression during mid‐exponential growth on rich (LB) and minimal (M9) medium. The identified TARs account for 77.3% of the genes as they are currently annotated and additionally we find 84 putative non‐coding RNAs (ncRNAs) and 127 antisense transcripts. One ncRNA, ncr22 , is predicted to act as a translational control on cstA and an antisense transcript was observed opposite the housekeeping sigma factor sigA . Through this work we have discovered a long conserved 3′ untranslated region (UTR) in a group of membrane‐associated genes that is predicted to fold into a large and highly stable secondary structure. One of the genes having this tail is efeN , which encodes a target of the twin‐arginine translocase (Tat) protein translocation system.

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References 78

  1. 1.

    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403-410.

    Not in our library10.1016/s0022-2836(05)80360-2

  2. 2.

    Anagnostopoulos C, Spizizen J. Requirements for transformation in Bacillus subtilis. J Bacteriol. 1961;81:741-746.

    Not in our library10.1128/jb.81.5.741-746.1961

  3. 3.

    Ando Y, Asari S, Suzuma S, Yamane K, Nakamura K. Expression of a small RNA, BS203 RNA, from the yocI–yocJ intergenic region of the Bacillus subtilis genome. FEMS Microbiol Lett. 2002;207:29-33.

    Not in our library10.1111/j.1574-6968.2002.tb11023.x

  4. 4.

    Auchtung JM, Lee CA, Grossman AD. Modulation of the ComA-dependent quorum response in Bacillus subtilis by multiple Rap proteins and Phr peptides. J Bacteriol. 2006;188:5273-5285.

    Not in our library10.1128/jb.00300-06

  5. 5.
  6. 6.

    Bertone P, Stolc V, Royce TE, Rozowsky JS, Urban AE, Zhu X, et al. Global identification of human transcribed sequences with genome tiling arrays. Science. 2004;306:2242-2246.

    Not in our library10.1126/science.1103388

  7. 7.

    Burguière P, Auger S, Hullo MF, Danchin A, Martin-Verstraete I. Three different systems participate in l-cystine uptake in Bacillus subtilis. J Bacteriol. 2004;186:4875-4884.

    Not in our library10.1128/jb.186.15.4875-4884.2004

  8. 8.

    Burkholder PR, Giles NH. Induced biochemical mutations in Bacillus subtilis. Am J Bot. 1947;34:345-348.

    Not in our library

  9. 9.

    Cervantes C, Ji G, Ramirez J, Silver S. Resistance to arsenic compounds in microorganisms. FEMS Microbiol Rev. 1994;15:355-367.

    Not in our library10.1111/j.1574-6976.1994.tb00145.x

  10. 10.

    Cohn F. Untersuchungen über Bakterien. Beitr Biol Pflanzen. 1872;1:127-224.

    Not in our library

  11. 11.

    Cohn F. Untersuchungen über Bakterien, IV. Beiträge zur Biologie der Bacillen. Beitr Biol Pflanzen. 1876;2:249-277.

    Not in our library

  12. 12.

    Conn HJ. The identity of Bacillus subtilis. J Infect Dis. 1930;46:341-350.

    Not in our library

  13. 13.

    David L, Huber W, Granovskaia M, Toedling J, Palm CJ, Bofkin L, et al. A high-resolution map of transcription in the yeast genome. Proc Natl Acad Sci USA. 2006;103:5320-5325.

    Not in our library10.1073/pnas.0601091103

  14. 14.

    DeLisa MP, Tullman D, Georgiou G. Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway. Proc Natl Acad Sci USA. 2003;100:6115-6120.

    Not in our library10.1073/pnas.0937838100

  15. 15.

    Deutscher J, Galinier A, Martin-Verstraete I, Sonenshein AL, Hoch JA, Losick R. Carbohydrate uptake and metabolism. Bacillus subtilis and its closest relatives. 2002;129-150.

    Not in our library

  16. 16.

    Dubey AK, Baker CS, Suzuki K, Jones AD, Pandit P, Romeo T, Babitzke P. CsrA regulates translation of the Escherichia coli carbon starvation gene, cstA, by blocking ribosome access to the cstA transcript. J Bacteriol. 2003;185:4450-4460.

    Not in our library10.1128/jb.185.15.4450-4460.2003

  17. 17.

    Ehrenberg CG. Dritter Beitrag zur Erkenntniss grosser Organisation in der Richtung des kleinsten Raumes. Physikalische Abhandlungen der Koeniglichen Akademie der Wissenschaften zu Berlin aus den Jahren 1833–1835. 1835;145-336.

    Not in our library

  18. 18.

    Eiamphungporn W, Helmann JD. Extracytoplasmic function sigma factors regulate expression of the Bacillus subtilis yabE gene via a cis-acting antisense RNA. J Bacteriol. 2009;191:1101-1105.

    Not in our library10.1128/jb.01530-08

  19. 19.

    Fillinger S, Boschi-Muller S, Azza S, Dervyn E, Branlant G, Aymerich S. Two glyceraldehyde-3-phosphate dehydrogenases with opposite physiological roles in a nonphotosynthetic bacterium. J Biol Chem. 2000;275:14031-14037.

    Not in our library10.1074/jbc.275.19.14031

  20. 20.

    Gaballa A, Antelmann H, Aguilar C, Khakh SK, Kyung-Bok S, Smaldone GT, Helmann JD. The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small basic proteins. Proc Natl Acad Sci USA. 2008;105:11927-11932.

    Not in our library10.1073/pnas.0711752105

  21. 21.

    Gaidenko TA, Kim TJ, Weigel AL, Brody MS, Price CW. The blue-light receptor YtvA acts in the environmental stress signaling pathway of Bacillus subtilis. J Bacteriol. 2006;188:6387-6395.

    Not in our library10.1128/jb.00691-06

  22. 22.

    Gardan R, Rapoport G, Débarbouille M. Expression of the rocDEF operon involved in arginine catabolism in Bacillus subtilis. J Mol Biol. 1995;249:843-856.

    Not in our library10.1006/jmbi.1995.0342

  23. 23.

    Gollnick P, Babitzke P, Antson A, Yanofsky C. Complexity in regulation of tryptophan biosynthesis in Bacillus subtilis. Annu Rev Genet. 2005;39:47-68.

    Not in our library10.1146/annurev.genet.39.073003.093745

  24. 24.

    Gruber AR, Lorenz R, Bernhart SH, Neuböck R, Hofacker IL. The Vienna RNA Web suite. Nucleic Acids Res. 2008;36:W70-W74.

    Not in our library10.1093/nar/gkn188

  25. 25.

    Grundy FJ, Henkin TM. The S box regulon: a new global transcription termination control system for methionine and cysteine biosynthesis genes in Gram-positive bacteria. Mol Microbiol. 1998;30:737-774.

    Not in our library10.1046/j.1365-2958.1998.01105.x

  26. 26.

    Haldenwang WG. The sigma factors of Bacillus subtilis. Microbiol Mol Biol Rev. 1995;59:1-30.

    Not in our library10.1128/mr.59.1.1-30.1995

  27. 27.

    Hallin PF, Ussery DW. CBS Genome Atlas Database: a dynamic storage for bioinformatic results and sequence data. Bioinformatics. 2004;20:3682-3686.

    Not in our library10.1093/bioinformatics/bth423

  28. 28.

    Helmann JD, Wu MF, Kobel PA, Gamo FJ, Wilson M, Morshedi MM, et al. Global transcriptional response of Bacillus subtilis to heat shock. J Bacteriol. 2001;183:7318-7328.

    Not in our library10.1128/jb.183.24.7318-7328.2001

  29. 29.
  30. 30.

    Huang JM, La Ragione RM, Nunez A, Cutting SM. Immunostimulatory activity of Bacillus spores. FEMS Immunol Med Microbiol. 2008;53:195-203.

    Not in our library10.1111/j.1574-695x.2008.00415.x

  31. 31.

    Huber W, Toedling J, Steinmetz LM. Transcript mapping with high-density oligonucleotide tiling arrays. Bioinformatics. 2006;22:1963-1970.

    Not in our library10.1093/bioinformatics/btl289

  32. 32.

    Jarmer H, Larsen TS, Krogh A, Saxild HH, Brunak S, Knudsen S. Sigma A recognition sites in the Bacillus subtilis genome. Microbiology. 2001;147:2417-2424.

    Not in our library10.1099/00221287-147-9-2417

  33. 33.

    Jerga A, Lu YJ, Schujman GE, de Mendoza D, Rock CO. Identification of a soluble diacylglycerol kinase required for lipoteichoic acid production in Bacillus subtilis. J Biol Chem. 2007;282:21738-21745.

    Not in our library10.1074/jbc.m703536200

  34. 34.

    Jongbloed JDH, Grieger U, Antelmann H, Hecker M, Nijland R, Bron S, van Dijl JM. Two minimal Tat translocases in Bacillus. Mol Microbiol. 2004;54:1319-1325.

    Not in our library10.1111/j.1365-2958.2004.04341.x

  35. 35.

    Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, et al. KEGG for linking genomes to life and the environment. Nucleic Acids Res. 2008;36:D480-D484.

    Not in our library10.1093/nar/gkm882

  36. 36.

    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.

    Not in our library10.1093/nar/gki256

  37. 37.

    Kent WJ. blat– the blast-like alignment tool. Genome Res. 2002;12:656-664.

    Not in our library10.1101/gr.229202

  38. 38.
  39. 39.

    Krogh S, O'Reailly M, Nolan N, Devine KM. The phage-like element PBSX and part of the skin element, which are resident at different locations on the Bacillus subtilis chromosome are highly homologous. Microbiology. 1996;142:2031-2040.

    Not in our library10.1099/13500872-142-8-2031

  40. 40.

    Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, et al. The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature. 1997;390:249-256.

    Not in our library10.1038/36786

  41. 41.

    Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, et al. ClustalW and ClustalX version 2. Bioinformatics. 2007;23:2647-2648.

    Not in our library10.1093/bioinformatics/btm404

  42. 42.

    Lazarevic V, Düsterhöft A, Soldo B, Hilbert H, Maeuël C, Karamata D. Nucleotide sequence of the Bacillus subtilis temperate bacteriophage SPβc2. Microbiology. 1999;145:1055-1067.

    Not in our library10.1099/13500872-145-5-1055

  43. 43.

    Li L, Wang X, Stolc V, Li X, Zhang D, Su N, et al. Genome-wide transcription analyses in rice using tiling microarrays. Nat Genet. 2006;38:124-129.

    Not in our library10.1038/ng1704

  44. 44.

    Licht A, Preis S, Brantl S. Implication of CcpN in the regulation of a novel untranslated RNA (SR1) in B. subtilis. Mol Microbiol. 2005;58:189-206.

    Not in our library10.1111/j.1365-2958.2005.04810.x

  45. 45.

    Mäder U, Henning S, Hecker M, Homuth G. Transcriptional organization and posttranscriptional regulation of the Bacillus subtilis branched-chain amino acid biosynthesis genes. J Bacteriol. 2004;186:2240-2252.

    Not in our library10.1128/jb.186.8.2240-2252.2004

  46. 46.

    Maillard J, Spronk CAEM, Buchanan G, Lyall V, Richardson DJ, Palmer T, et al. Structural diversity in twin-arginine signal peptide-binding proteins. Proc Natl Acad Sci USA. 2007;104:15641-15646.

    Not in our library10.1073/pnas.0703967104

  47. 47.

    Mazumder B, Seshadri V, Fox PL. Translational control by the 3′-UTR: the ends specify the means. Trends Biochem Sci. 2003;28:91-98.

    Not in our library10.1016/s0968-0004(03)00002-1

  48. 48.

    Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science. 2008;320:1344-1349.

    Not in our library10.1126/science.1158441

  49. 49.

    Nicolas P, Bize L, Muri F, Hoebeke M, Rodolphe F, Ehrlic SD, et al. Mining Bacillus subtilis chromosome heterogeneities using hidden Markov models. Nucleic Acids Res. 2002;30:1418-1426.

    Not in our library10.1093/nar/30.6.1418

  50. 50.

    Nielsen P, Krogh A. Large-scale prokaryotic gene prediction and comparison to genome annotation. Bioinformatics. 2005;21:4322-4329.

    Not in our library10.1093/bioinformatics/bti701

  51. 51.

    Ogura M, Shimane K, Asai K, Ogasawara N, Tanaka T. Binding of response regulator DegU to the aprE promoter is inhibited by RapG, which is counteracted by extracellular PhrG in Bacillus subtilis. Mol Microbiol. 2003;49:1685-1697.

    Not in our library10.1046/j.1365-2958.2003.03665.x

  52. 52.

    Ollinger J, Song KB, Antelmann H, Hecker M, Helmann JD. Role of the Fur regulon in iron transport in Bacillus subtilis. J Bacteriol. 2006;188:3664-3673.

    Not in our library10.1128/jb.188.10.3664-3673.2006

  53. 53.

    Oussenko IA, Abe T, Ujiie H, Muto A, Bechhofer DH. Participation of 3′- to 5′-exoribonucleases in the turnover of Bacillus subtilis mRNA. J Bacteriol. 2005;187:2758-2767.

    Not in our library10.1128/jb.187.8.2758-2767.2005

  54. 54.

    Perocchi F, Xu Z, Clauder-Münster S, Steinmetz LM. Antisense artifacts in transcriptome microarray experiments are resolved by actinomycin D. Nucleic Acids Res. 2007;35:1-7.

    Not in our library10.1093/nar/gkm683

  55. 55.

    Ratushna VG, Weller JW, Gibas CJ. Secondary structure in the target as a confounding factor in synthetic oligomer microarray design. BMC Genomics. 2005;6:31.

    Not in our library10.1186/1471-2164-6-31

  56. 56.

    Reppas NB, Wade JT, Church GM, Struhl K. The transition between transcriptional initiation and elongation in E. coli is highly variable and often rate limiting. Mol Cell. 2006;24:747-757.

    Not in our library10.1016/j.molcel.2006.10.030

  57. 57.

    Saito S, Kakeshita H, Nakamura K. Novel small RNA-encoding genes in the intergenic regions of Bacillus subtilis. Gene. 2009;428:2-8.

    Not in our library10.1016/j.gene.2008.09.024

  58. 58.

    Shivers RP, Sonenshein AL. Bacillus subtilis ilvB operon: an intersection of global regulons. Mol Microbiol. 2005;56:1549-1559.

    Not in our library10.1111/j.1365-2958.2005.04634.x

  59. 59.

    Sierro N, Makita Y, de Hoon M, Nakai K. DBTBS: a database of transcriptional regulation in Bacillus subtilis containing upstream intergenic conservation information. Nucleic Acids Res. 2008;36:D93-D96.

    Not in our library10.1093/nar/gkm910

  60. 60.

    Silvaggi JM, Perkins JB, Losick R. Small untranslated RNA antitoxin in Bacillus subtilis. J Bacteriol. 2005;187:6641-6650.

    Not in our library10.1128/jb.187.19.6641-6650.2005

  61. 61.

    Silvaggi JM, Perkins JB, Losick R. Genes for small, noncoding RNAs under sporulation control in Bacillus subtilis. J Bacteriol. 2006;188:532-541.

    Not in our library10.1128/jb.188.2.532-541.2006

  62. 62.

    Spizizen J. Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc Natl Acad Sci USA. 1958;44:1072-1078.

    Not in our library10.1073/pnas.44.10.1072

  63. 63.

    Spizizen J. Citation classic – Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Curr Contents Life Sci. 1984;19:15.

    Not in our library10.1073/pnas.44.10.1072

  64. 64.

    Steil L, Serrano M, Henriques AO, Völker U. Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis. Microbiology. 2005;151:339-420.

    Not in our library10.1099/mic.0.27493-0

  65. 65.

    Suzuma S, Asari S, Bunai K, Yoshino K, Ando Y, Kakeshita H, et al. Identification and characterization of novel small RNAs in the aspS–yrvM intergenic region of the Bacillus subtilis genome. Microbiology. 2002;148:2591-2598.

    Not in our library10.1099/00221287-148-8-2591

  66. 66.

    Swets JA. Measuring the accuracy of diagnostic systems. Science. 1988;240:1285-1293.

    Not in our library10.1126/science.3287615

  67. 67.

    Takemaru K, Mizuno M, Sato T, Takeuchi M, Kobayashi Y. Complete nucleotide sequence of a skin element excised by DNA rearrangement during sporulation in Bacillus subtilis. Microbiology. 1995;141:323-327.

    Not in our library10.1099/13500872-141-2-323

  68. 68.

    Teas HJ. Mutants of Bacillus subtilis that require threonine or threonine plus methionine. J Bacteriol. 1949;59:93-104.

    Not in our library10.1128/jb.59.1.93-104.1950

  69. 69.

    Tjaden B, Goodwin SS, Opdyke JA, Guillier M, Fu DX, Gottesman S, Storz G. Target prediction for small, noncoding RNAs in bacteria. Nucleic Acids Res. 2006;34:2791-2802.

    Not in our library10.1093/nar/gkl356

  70. 70.

    Tjaden B, Saxena RM, Stolyar S, Haynor DR, Kolker E, Rosenow C. Transcriptome analysis of Escherichia coli using high-density oligonucleotide probe arrays. Nucleic Acids Res. 2002;30:3732-3738.

    Not in our library10.1093/nar/gkf505

  71. 71.

    Vogel J, Wagner EGH. Target identification of small noncoding RNAs in bacteria. Curr Opin Microbiol. 2007;10:262-270.

    Not in our library10.1016/j.mib.2007.06.001

  72. 72.

    Wang L, Park S, Doi RH. A novel Bacillus subtilis gene, antE, temporally regulated and convergent to and overlapping dnaE. J Bacteriol. 1999;181:353-356.

    Not in our library10.1128/jb.181.1.353-356.1999

  73. 73.

    Wernersson R, Nielsen HB. OligoWiz 2.0 – integrating sequence feature annotation into the design of microarray probes. Nucleic Acids Res. 2005;33:W611-W615.

    Not in our library10.1093/nar/gki399

  74. 74.

    Wood HE, Dawson MT, Devine KM, McConnell DJ. Characterization of PBSX, a defective prophage of Bacillus subtilis. J Bacteriol. 1990;172:2667-2674.

    Not in our library10.1128/jb.172.5.2667-2674.1990

  75. 75.

    Xu Z, Wei W, Gagneur J, Perocchi F, Clauder-Münster S, Camblon J, et al. Bidirectional promoters generate pervasive transcription in yeast. Nature. 2009;457:1033-1037.

    Not in our library10.1038/nature07728

  76. 76.

    Yakhnin H, Pandi P, Petty TJ, Baker CS, Romeo T, Babitzke P. CrsA of Bacillus subtilis regulates translation initiation of the gene encoding the flagellin protein (hag) by blocking ribosome binding. Mol Microbiol. 2007;64:1605-1620.

    Not in our library10.1111/j.1365-2958.2007.05765.x

  77. 77.

    Zahler SA, Korman RZ, Rosenthal R, Hemphill HE. Bacillus subtilis bacteriophage SPβ: localization of the prophage attachment site and specialized transduction. J Bacteriol. 1977;129:556-558.

    Not in our library10.1128/jb.129.1.556-558.1977

  78. 78.

    Zeigler DR, Prágai Z, Rodriguez S, Chevreux B, Muffler A, Albert T, et al. The origins of 168, W23, and other Bacillus subtilis legacy strains. J Bacteriol. 2008;190:6983-6995.

    Not in our library10.1128/jb.00722-08

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