Regulatory RNAs in bacillus subtilis: A gram-positive perspective on bacterial RNA-mediated regulation of gene expression

Microbiology and Molecular Biology Reviews

Volumn 80, Issue 4, 2016, Pages 1029-1057

  Mars, Ruben A T ^a   Nicolas, Pierre ^a   Denham, Emma L ^a   Van Dijl, Jan Maarten ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; CHAPERONE; COMPLEMENTARY RNA; MESSENGER RNA; SIGMA FACTOR; SPACER DNA; TRANSFER RNA; 3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; REGULATORY RNA SEQUENCE; RIBOSWITCH; SMALL UNTRANSLATED RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; BACILLUS SUBTILIS; BINDING SITE; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; NONHUMAN; PROTEIN RNA BINDING; RIBOSWITCH; SALMONELLA; GENETICS; METABOLISM; REGULATORY RNA SEQUENCE;

3' UNTRANSLATED REGIONS; 5' UNTRANSLATED REGIONS; BACILLUS SUBTILIS; GENE EXPRESSION REGULATION, BACTERIAL; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RIBOSWITCH; RNA, ANTISENSE; RNA, BACTERIAL; RNA, SMALL UNTRANSLATED; RNA, TRANSFER;

EID: 84995553782     PISSN: 10922172     EISSN: 10985557     Source Type: Journal    
DOI: 10.1128/MMBR.00026-16     Document Type: Article

References (143)

1. Cech TR, Steitz JA. 2014. The noncoding RNA revolution-Trashing old rules to forge new ones. Cell 157:77-94. http://dx.doi.org/10.1016/j.cell.2014.03.008.
2. Waters LS, Storz G. 2009. Regulatory RNAs in bacteria. Cell 136:615- 628. http://dx.doi.org/10.1016/j.cell.2009.01.043.
3. Wang K, Chang H. 2011. Molecular mechanisms of long noncoding RNAs. Mol Cell 43:904-914. http://dx.doi.org/10.1016/j.molcel.2011.08.018.
4. Marraffini LA, Sontheimer EJ. 2010. CRISPR interference: RNAdirected adaptive immunity in bacteria and archaea. Nat Rev Genet 11: 181-190. http://dx.doi.org/10.1038/nrg2749.
5. Schroeder R, Barta A, Semrad K. 2004. Strategies for RNA folding andassembly. Nat Rev Mol Cell Biol 5:908-919. http://dx.doi.org/10.1038/nrm1497.
6. Wan Y, Kertesz M, Spitale RC, Segal E, Chang HY. 2011. Understanding the transcriptome through RNA structure. Nat Rev Genet 12:641- 655. http://dx.doi.org/10.1038/nrg3049.
7. Peer A, Margalit H. 2011. Accessibility and evolutionary conservation mark bacterial small-RNA target-binding regions. J Bacteriol 193:1690- 1701. http://dx.doi.org/10.1128/JB.01419-10.
8. Busch A, Richter AS, Backofen R. 2008. IntaRNA: Efficient prediction of bacterial sRNA targets incorporating target site accessibility and seed regions. Bioinformatics 24:2849 -2856. http://dx.doi.org/10.1093/bioinformatics/btn544.
9. Freyhult E, Gardner PP, Moulton V. 2005. A comparison of RNA folding measures. BMC Bioinformatics 6:241. http://dx.doi.org/10.1186/1471-2105-6-241.
10. Livny J, Waldor MK. 2007. Identification of small RNAs in diverse bacterial species. Curr Opin Microbiol 10:96-101. http://dx.doi.org/10.1016/j.mib.2007.03.005.
11. Silvaggi JM, Perkins JB, Losick R. 2006. Genes for small, noncoding RNAs under sporulation control in Bacillus subtilis. J Bacteriol 188:532- 541. http://dx.doi.org/10.1128/JB.188.2.532-541.2006.
12. Saito S, Kakeshita H, Nakamura K. 2009. Novel small RNA-encoding genes in the intergenic regions of Bacillus subtilis. Gene 428:2-8. http://dx.doi.org/10.1016/j.gene.2008.09.024.
13. Sharma CM, Vogel J. 2014. Differential RNA-seq: The approach behind and the biological insight gained. Curr Opin Microbiol 19:97-105. http://dx.doi.org/10.1016/j.mib.2014.06.010.
14. Irnov I, Sharma CM, Vogel J, Winkler WC. 2010. Identification of regulatory RNAs in Bacillus subtilis. Nucleic Acids Res 38:6637-6651. http://dx.doi.org/10.1093/nar/gkq454.
15. Nicolas P, Mader U, Dervyn E, Rochat T, Leduc A, Pigeonneau N, Bidnenko E, Marchadier E, Hoebeke M, Aymerich S, Becher D, Bisicchia P, Botella E, Delumeau O, Doherty G, Denham EL, Fogg MJ, Fromion V, Goelzer A, Hansen A, Hartig E, Harwood CR, Homuth G, Jarmer H, Jules M, Klipp E, Le Chat L, Lecointe F, Lewis P, Liebermeister W, March A, Mars RA, Nannapaneni P, Noone D, Pohl S, Rinn B, Rugheimer F, Sappa PK, Samson F, Schaffer M, Schwikowski B, Steil L, Stulke J, Wiegert T, Devine KM, Wilkinson AJ, van Dijl JM, Hecker M, Volker U, Bessieres P, Noirot P. 2012. Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 335:1103-1106. http://dx.doi.org/10.1126/science.1206848.
16. Chao Y, Papenfort K, Reinhardt R, Sharma CM, Vogel J. 2012. An atlas of Hfq-bound transcripts reveals 3= UTRs as a genomic reservoir of regulatory small RNAs. EMBO J 31:4005-4019. http://dx.doi.org/10.1038/emboj.2012.229.
17. Wade JT, Grainger DC. 2014. Pervasive transcription: illuminating the dark matter of bacterial transcriptomes. Nat Rev Microbiol 12:647-653. http://dx.doi.org/10.1038/nrmicro3316.
18. Earl AM, Losick R, Kolter R. 2008. Ecology and genomics of Bacillus subtilis. Trends Microbiol 16:269-275. http://dx.doi.org/10.1016/j.tim.2008.03.004.
19. Michna RH, Commichau FM, Todter D, Zschiedrich CP, Stulke J. 2014. SubtiWiki-A database for the model organism Bacillus subtilis that links pathway, interaction and expression information. Nucleic Acids Res 42:D692-D698. http://dx.doi.org/10.1093/nar/gkt1002.
20. Harwood CR. 1992. Bacillus subtilis and its relatives: molecular biological and industrial workhorses. Trends Biotechnol 10:247-256. http://dx.doi.org/10.1016/0167-7799(92)90233-L.
21. van Dijl JM, Hecker M. 2013. Bacillus subtilis: from soil bacterium to super-secreting cell factory. Microb Cell Fact 12:3. http://dx.doi.org/10.1186/1475-2859-12-3.
22. Jousselin A, Metzinger L, Felden B. 2009. On the facultative requirement of the bacterial RNA chaperone, Hfq. Trends Microbiol 17:399- 405. http://dx.doi.org/10.1016/j.tim.2009.06.003.
23. Hammerle H, Amman F, Vecerek B, Stulke J, Hofacker I, Blasi U. 2014. Impact of Hfq on the Bacillus subtilis transcriptome. PLoS One 9:e98661. http://dx.doi.org/10.1371/journal.pone.0098661.
24. Mars RA, Nicolas P, Ciccolini M, Reilman E, Reder A, Schaffer M, Mader U, Volker U, van Dijl JM, Denham EL. 2015. Small regulatory RNA-induced growth rate heterogeneity of Bacillus subtilis. PLoS Genet 11:e1005046. http://dx.doi.org/10.1371/journal.pgen.1005046.
25. Tjalsma H, Antelmann H, Jongbloed JD, Braun PG, Darmon E, Dorenbos R, Dubois JY, Westers H, Zanen G, Quax WJ, Kuipers OP, Bron S, Hecker M, van Dijl JM. 2004. Proteomics of protein secretion by Bacillus subtilis: separating the "secrets" of the secretome. Microbiol Mol Biol Rev 68:207-233. http://dx.doi.org/10.1128/MMBR.68.2.207-233.2004.
26. Tjalsma H, Bolhuis A, Jongbloed JD, Bron S, van Dijl JM. 2000. Signal peptide-dependent protein transport in Bacillus subtilis: A genome-based survey of the secretome. Microbiol Mol Biol Rev 64:515-547. http://dx.doi.org/10.1128/MMBR.64.3.515-547.2000.
27. Brantl S, Brückner R. 2014. Small regulatory RNAs from low-GC Grampositive bacteria. RNA Biol 11:443-456. http://dx.doi.org/10.4161/rna.28036.
28. Wassarman KM. 2007. 6S RNA: A small RNA regulator of transcription. Curr Opin Microbiol 10:164-168. http://dx.doi.org/10.1016/j.mib.2007.03.008.
29. Breaker RR. 2012. Riboswitches and the RNA world. Cold Spring Harb Perspect Biol 4:a003566. http://dx.doi.org/10.1101/cshperspect.a003566.
30. Hubner S, Declerck N, Diethmaier C, Le Coq D, Aymerich S, Stulke J. 2011. Prevention of cross-Talk in conserved regulatory systems: identification of specificity determinants in RNA-binding anti-Termination proteins of the BglG family. Nucleic Acids Res 39:4360-4372. http://dx.doi.org/10.1093/nar/gkr021.
31. Gutierrez-Preciado A, Henkin TM, Grundy FJ, Yanofsky C, Merino E. 2009. Biochemical features and functional implications of the RNAbased T-box regulatory mechanism. Microbiol Mol Biol Rev 73:36-61. http://dx.doi.org/10.1128/MMBR.00026-08.
32. Deiorio-Haggar K, Anthony J, Meyer MM. 2013. RNA structures regulating ribosomal protein biosynthesis in bacilli. RNA Biol 10:1180- 1184. http://dx.doi.org/10.4161/rna.24151.
33. Mader U, Nicolas P, Depke M, Pane-Farre J, Debarbouille M, van der Kooi-Pol MM, Guerin C, Derozier S, Hiron A, Jarmer H, Leduc A, Michalik S, Reilman E, Schaffer M, Schmidt F, Bessieres P, Noirot P, Hecker M, Msadek T, Volker U, van Dijl JM. 2016. Staphylococcus aureus transcriptome architecture: from laboratory to infectionmimicking conditions. PLoS Genet 12:e1005962. http://dx.doi.org/10.1371/journal.pgen.1005962.
34. Mader U, Nicolas P, Richard H, Bessieres P, Aymerich S. 2011. Comprehensive identification and quantification of microbial transcriptomes by genome-wide unbiased methods. Curr Opin Biotechnol 22:32- 41. http://dx.doi.org/10.1016/j.copbio.2010.10.003.
35. Rasmussen S, Nielsen HB, Jarmer H. 2009. The transcriptionally active regions in the genome of Bacillus subtilis. Mol Microbiol 73:1043-1057. http://dx.doi.org/10.1111/j.1365-2958.2009.06830.x.
36. Mirauta B, Nicolas P, Richard H. 2014. Parseq: Reconstruction of microbial transcription landscape from RNA-Seq read counts using statespace models. Bioinformatics 30:1409-1416. http://dx.doi.org/10.1093/bioinformatics/btu042.
37. Burge SW, Daub J, Eberhardt R, Tate J, Barquist L, Nawrocki EP, Eddy SR, Gardner PP, Bateman A. 2013. Rfam 11.0: 10 years of RNA families. Nucleic Acids Res 41:D226-D232. http://dx.doi.org/10.1093/nar/gks1005.
38. Abreu-Goodger C, Merino E. 2005. RibEx: A web server for locating riboswitches and other conserved bacterial regulatory elements. Nucleic Acids Res 33:W690-W692. http://dx.doi.org/10.1093/nar/gki445.
39. Barbe V, Cruveiller S, Kunst F, Lenoble P, Meurice G, Sekowska A, Vallenet D, Wang T, Moszer I, Medigue C, Danchin A. 2009. From a consortium sequence to a unified sequence: The Bacillus subtilis 168 reference genome a decade later. Microbiology 155:1758-1775. http://dx.doi.org/10.1099/mic.0.027839-0.
40. Sierro N, Makita Y, de Hoon M, Nakai K. 2008. DBTBS: A database of transcriptional regulation in Bacillus subtilis containing upstream intergenic conservation information. Nucleic Acids Res 36:D93-D96.
41. de Jong A, Pietersma H, Cordes M, Kuipers OP, Kok J. 2012. PePPER: A webserver for prediction of prokaryote promoter elements and regulons. BMC Genomics 13:299. http://dx.doi.org/10.1186/1471-2164-13-299.
42. Campbell EA, Westblade LF, Darst SA. 2008. Regulation of bacterial RNA polymerase sigma factor activity: A structural perspective. Curr Opin Microbiol 11:121-127. http://dx.doi.org/10.1016/j.mib.2008.02.016.
43. Gaballa A, Antelmann H, Aguilar C, Khakh SK, Song KB, Smaldone GT, Helmann JD. 2008. The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small, basic proteins. Proc Natl Acad Sci U S A 105:11927-11932. http://dx.doi.org/10.1073/pnas.0711752105.
44. Licht A, Preis S, Brantl S. 2005. Implication of CcpN in the regulation of a novel untranslated RNA (SR1) in Bacillus subtilis. Mol Microbiol 58:189-206. http://dx.doi.org/10.1111/j.1365-2958.2005.04810.x.
45. Haugen SP, Ross W, Gourse RL. 2008. Advances in bacterial promoter recognition and its control by factors that do not bind DNA. Nat Rev Microbiol 6:507-519. http://dx.doi.org/10.1038/nrmicro1912.
46. Hofacker IL, Stadler PF. 2006. Memory efficient folding algorithms for circular RNA secondary structures. Bioinformatics 22:1172-1176. http://dx.doi.org/10.1093/bioinformatics/btl023.
47. Kertesz M, Wan Y, Mazor E, Rinn JL, Nutter RC, Chang HY, Segal E. 2010. Genome-wide measurement of RNA secondary structure in yeast. Nature 467:103-107. http://dx.doi.org/10.1038/nature09322.
48. Smolke CD, Keasling JD. 2002. Effect of gene location, mRNA secondary structures, and RNase sites on expression of two genes in an engineered operon. Biotechnol Bioeng 80:762-776. http://dx.doi.org/10.1002/bit.10434.
49. Sharp JS, Bechhofer DH. 2005. Effect of 5=-proximal elements on decay of a model mRNA in Bacillus subtilis. Mol Microbiol 57:484-495. http://dx.doi.org/10.1111/j.1365-2958.2005.04683.x.
50. Reilman E, Mars RA, van Dijl JM, Denham EL. 2014. The multidrug ABC transporter BmrC/BmrD of Bacillus subtilis is regulated via a ribosome- mediated transcriptional attenuation mechanism. Nucleic Acids Res 42:11393-11407. http://dx.doi.org/10.1093/nar/gku832.
51. Lehnik-Habrink M, Pfortner H, Rempeters L, Pietack N, Herzberg C, Stulke J. 2010. The RNA degradosome in Bacillus subtilis: identification of CshA as the major RNA helicase in the multiprotein complex. Mol Microbiol 77:958-971. http://dx.doi.org/10.1111/j.1365-2958.2010.07264.x.
52. Lehnik-Habrink M, Lewis RJ, Mader U, Stulke J. 2012. RNA degradation in Bacillus subtilis: An interplay of essential endo-And exoribonucleases. Mol Microbiol 84:1005-1017. http://dx.doi.org/10.1111/j.1365-2958.2012.08072.x.
53. Durand S, Gilet L, Bessieres P, Nicolas P, Condon C. 2012. Three essential ribonucleases-RNase Y, J1, and III-control the abundance of a majority of Bacillus subtilis mRNAs. PLoS Genet 8:e1002520. http://dx.doi.org/10.1371/journal.pgen.1002520.
54. Mathy N, Benard L, Pellegrini O, Daou R, Wen T, Condon C. 2007. 5=-To-3= exoribonuclease activity in bacteria: Role of RNase J1 in rRNA maturation and 5= stability of mRNA. Cell 129:681-692. http://dx.doi.org/10.1016/j.cell.2007.02.051.
55. Durand S, Tomasini A, Braun F, Condon C, Romby P. 2015. sRNA and mRNA turnover in Gram-positive bacteria. FEMS Microbiol Rev 39: 316-330. http://dx.doi.org/10.1093/femsre/fuv007.
56. Naville M, Gautheret D. 2010. Transcription attenuation in bacteria: Theme and variations. Brief Funct Genomics 9:178-189. http://dx.doi.org/10.1093/bfgp/elq008.
57. Dar D, Shamir M, Mellin JR, Koutero M, Stern-Ginossar N, Cossart P, Sorek R. 2016. Term-seq reveals abundant ribo-regulation of antibiotics resistance in bacteria. Science 352:aad9822. http://dx.doi.org/10.1126/science.aad9822.
58. Ohki R, Tateno K, Takizawa T, Aiso T, Murata M. 2005. Transcriptional termination control of a novel ABC transporter gene involved in antibiotic resistance in Bacillus subtilis. J Bacteriol 187:5946-5954. http://dx.doi.org/10.1128/JB.187.17.5946-5954.2005.
59. Saito H, Inoue T. 2009. Synthetic biology with RNA motifs. Int J Biochem Cell Biol 41:398-404. http://dx.doi.org/10.1016/j.biocel.2008.08.017.
60. Qi LS, Arkin AP. 2014. A versatile framework for microbial engineering using synthetic non-coding RNAs. Nat Rev Microbiol 12:341-354. http://dx.doi.org/10.1038/nrmicro3244.
61. Mandal M, Boese B, Barrick JE, Winkler WC, Breaker RR. 2003. Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113:577-586. http://dx.doi.org/10.1016/S0092-8674(03)00391-X.
62. Barrick JE, Corbino KA, Winkler WC, Nahvi A, Mandal M, Collins J, Lee M, Roth A, Sudarsan N, Jona I, Wickiser JK, Breaker RR. 2004. New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. Proc Natl Acad Sci U S A 101:6421-6426. http://dx.doi.org/10.1073/pnas.0308014101.
63. Mehne FM, Gunka K, Eilers H, Herzberg C, Kaever V, Stulke J. 2013. Cyclic di-AMP homeostasis in Bacillus subtilis: both lack and high level accumulation of the nucleotide are detrimental for cell growth. J Biol Chem 288:2004-2017. http://dx.doi.org/10.1074/jbc.M112.395491.
64. Nelson JW, Sudarsan N, Furukawa K, Weinberg Z, Wang JX, Breaker RR. 2013. Riboswitches in eubacteria sense the second messenger c-di- AMP. Nat Chem Biol 9:834-839. http://dx.doi.org/10.1038/nchembio.1363.
65. Winkler WC, Cohen-Chalamish S, Breaker RR. 2002. An mRNA structure that controls gene expression by binding FMN. Proc Natl Acad Sci U S A 99:15908-15913. http://dx.doi.org/10.1073/pnas.212628899.
66. Weinberg Z, Wang JX, Bogue J, Yang J, Corbino K, Moy RH, Breaker RR. 2010. Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes. Genome Biol 11:R31. http://dx.doi.org/10.1186/gb-2010-11-3-r31.
67. Henkin TM, Glass BL, Grundy FJ. 1992. Analysis of the Bacillus subtilis tyrS gene: conservation of a regulatory sequence in multiple tRNA synthetase genes. J Bacteriol 174:1299-1306.
68. Yakhnin H, Yakhnin AV, Babitzke P. 2015. Ribosomal protein L10(L12)4 autoregulates expression of the Bacillus subtilis rplJL operon by a transcription attenuation mechanism. Nucleic Acids Res 43:7032- 7043. http://dx.doi.org/10.1093/nar/gkv628.
69. Shajani Z, Sykes MT, Williamson JR. 2011. Assembly of bacterial ribosomes. Annu Rev Biochem 80:501-526. http://dx.doi.org/10.1146/annurev-biochem-062608-160432.
70. Mars RA, Mendonca K, Denham EL, van Dijl JM. 2015. The reduction in small ribosomal subunit abundance in ethanol-stressed cells of Bacillus subtilis is mediated by a SigB-dependent antisense RNA. Biochim Biophys Acta 1853:2553-2559. http://dx.doi.org/10.1016/j.bbamcr.2015.06.009.
71. Babitzke P. 2004. Regulation of transcription attenuation and translation initiation by allosteric control of an RNA-binding protein: The Bacillus subtilis TRAP protein. Curr Opin Microbiol 7:132-139. http://dx.doi.org/10.1016/j.mib.2004.02.003.
72. Willimsky G, Bang H, Fischer G, Marahiel MA. 1992. Characterization of cspB, a Bacillus subtilis inducible cold shock gene affecting cell viability at low temperatures. J Bacteriol 174:6326-6335.
73. Graumann P, Wendrich TM, Weber MH, Schroder K, Marahiel MA. 1997. A family of cold shock proteins in Bacillus subtilis is essential for cellular growth and for efficient protein synthesis at optimal and low temperatures. Mol Microbiol 25:741-756. http://dx.doi.org/10.1046/j.1365-2958.1997.5121878.x.
74. Turner RJ, Lu Y, Switzer RL. 1994. Regulation of the Bacillus subtilis pyrimidine biosynthetic (pyr) gene cluster by an autogenous transcriptional attenuation mechanism. J Bacteriol 176:3708-3722.
75. Lu Y, Turner RJ, Switzer RL. 1996. Function of RNA secondary structures in transcriptional attenuation of the Bacillus subtilis pyr operon. Proc Natl Acad Sci U S A 93:14462-14467. http://dx.doi.org/10.1073/pnas.93.25.14462.
76. Glatz E, Nilsson RP, Rutberg L, Rutberg B. 1996. A dual role for the Bacillus subtilis glpD leader and the GlpP protein in the regulated expression of glpD: Antitermination and control of mRNA stability. Mol Microbiol 19:319 -328. http://dx.doi.org/10.1046/j.1365-2958.1996.376903.x.
77. Kumarevel T, Mizuno H, Kumar PK. 2005. Structural basis of HutPmediated anti-Termination and roles of the Mg2- ion and L-histidine ligand. Nature 434:183-191. http://dx.doi.org/10.1038/nature03355.
78. Morinaga T, Kobayashi K, Ashida H, Fujita Y, Yoshida K. 2010. Transcriptional regulation of the Bacillus subtilis asnH operon and role of the 5=-proximal long sequence triplication in RNA stabilization. Microbiology 156:1632-1641. http://dx.doi.org/10.1099/mic.0.036582-0.
79. Hambraeus G, von Wachenfeldt C, Hederstedt L. 2003. Genome-wide survey of mRNA half-lives in Bacillus subtilis identifies extremely stable mRNAs. Mol Genet Genomics 269:706-714. http://dx.doi.org/10.1007/s00438-003-0883-6.
80. Noone D, Salzberg LI, Botella E, Basell K, Becher D, Antelmann H, Devine KM. 2014. A highly unstable transcript makes CwlO D, Lendopeptidase expression responsive to growth conditions in Bacillus subtilis. J Bacteriol 196:237-247. http://dx.doi.org/10.1128/JB.00986-13.
81. Deana A, Belasco JG. 2005. Lost in translation: The influence of ribosomes on bacterialmRNAdecay. Genes Dev 19:2526-2533. http://dx.doi.org/10.1101/gad.1348805.
82. Yao S, Bechhofer DH. 2009. Processing and stability of inducibly expressed rpsOmRNAderivatives in Bacillus subtilis. J Bacteriol 191:5680- 5689. http://dx.doi.org/10.1128/JB.00740-09.
83. Hambraeus G, Karhumaa K, Rutberg B. 2002. A 5= stem-loop and ribosome binding but not translation are important for the stability of Bacillus subtilis aprE leader mRNA. Microbiology 148:1795-1803. http://dx.doi.org/10.1099/00221287-148-6-1795.
84. de Smit MH, van Duin J. 1994. Control of translation by mRNA secondary structure in Escherichia coli. A quantitative analysis of literature data. J Mol Biol 244:144-150.
85. Kruger S, Gertz S, Hecker M. 1996. Transcriptional analysis of bglPH expression in Bacillus subtilis: Evidence for two distinct pathways mediating carbon catabolite repression. J Bacteriol 178:2637-2644.
86. Meng Q, Switzer RL. 2001. Regulation of transcription of the Bacillus subtilis pyrG gene, encoding cytidine triphosphate synthetase. J Bacteriol 183:5513-5522. http://dx.doi.org/10.1128/JB.183.19.5513-5522.2001.
87. Jensen-MacAllister IE, Meng Q, Switzer RL. 2007. Regulation of pyrG expression in Bacillus subtilis: CTP-regulated antitermination and reiterative transcription with pyrG templates in vitro. Mol Microbiol 63: 1440-1452. http://dx.doi.org/10.1111/j.1365-2958.2007.05595.x.
88. Lehnik-Habrink M, Schaffer M, Mader U, Diethmaier C, Herzberg C, Stulke J. 2011. RNA processing in Bacillus subtilis: identification of targets of the essential RNase Y. Mol Microbiol 81:1459-1473. http://dx.doi.org/10.1111/j.1365-2958.2011.07777.x.
89. Nahvi A, Barrick JE, Breaker RR. 2004. Coenzyme B12 riboswitches are widespread genetic control elements in prokaryotes. Nucleic Acids Res 32:143-150. http://dx.doi.org/10.1093/nar/gkh167.
90. Stark A, Brennecke J, Bushati N, Russell RB, Cohen SM. 2005. Animal microRNAs confer robustness to gene expression and have a significant impact on 3=UTR evolution. Cell 123:1133-1146. http://dx.doi.org/10.1016/j.cell.2005.11.023.
91. Tomecki R, Dziembowski A. 2010. Novel endoribonucleases as central players in various pathways of eukaryotic RNA metabolism. RNA 16: 1692-1724. http://dx.doi.org/10.1261/rna.2237610.
92. Belasco JG. 2010. All things must pass: contrasts and commonalities in eukaryotic and bacterial mRNA decay. Nat Rev Mol Cell Biol 11:467- 478. http://dx.doi.org/10.1038/nrm2917.
93. Gerwig J, Stulke J. 2014. Caught in the act: RNA-Seq provides novel insights into mRNA degradation. Mol Microbiol 94:5-8. http://dx.doi.org/10.1111/mmi.12769.
94. Alen C, Sonenshein AL. 1999. Bacillus subtilis aconitase is an RNAbinding protein. Proc Natl Acad SciUSA 96:10412-10417. http://dx.doi.org/10.1073/pnas.96.18.10412.
95. Miethke M, Monteferrante CG, Marahiel MA, van Dijl JM. 2013. The Bacillus subtilis EfeUOB transporter is essential for high-Affinity acquisition of ferrous and ferric iron. Biochim Biophys Acta 1833:2267-2278. http://dx.doi.org/10.1016/j.bbamcr.2013.05.027.
96. Pfleger BF, Pitera DJ, Smolke CD, Keasling JD. 2006. Combinatorial engineering of intergenic regions in operons tunes expression of multiple genes. Nat Biotechnol 24:1027-1032. http://dx.doi.org/10.1038/nbt1226.
97. Allenby NE, O'Connor N, Pragai Z, Carter NM, Miethke M, Engelmann S, Hecker M, Wipat A, Ward AC, Harwood CR. 2004. Posttranscriptional regulation of the Bacillus subtilis pst operon encoding a phosphate-specific ABC transporter. Microbiology 150:2619-2628. http://dx.doi.org/10.1099/mic.0.27126-0.
98. Irnov I, Winkler WC. 2010. A regulatory RNA required for antitermination of biofilm and capsular polysaccharide operons in Bacillales. Mol Microbiol 76:559-575. http://dx.doi.org/10.1111/j.1365-2958.2010.07131.x.
99. Jerga A, Lu YJ, Schujman GE, de Mendoza D, Rock CO. 2007. Identification of a soluble diacylglycerol kinase required for lipoteichoic acid production in Bacillus subtilis. J Biol Chem 282:21738-21745. http://dx.doi.org/10.1074/jbc.M703536200.
100. Smaldone GT, Antelmann H, Gaballa A, Helmann JD. 2012. The FsrA sRNA and FbpB protein mediate the iron-dependent induction of the Bacillus subtilis lutABC iron-sulfur-containing oxidases. J Bacteriol 194: 2586-2593. http://dx.doi.org/10.1128/JB.05567-11.
101. Updegrove TB, Shabalina SA, Storz G. 2015. How do base-pairing small RNAs evolve? FEMS Microbiol Rev 39:379-391. http://dx.doi.org/10.1093/femsre/fuv014.
102. Smaldone GT, Revelles O, Gaballa A, Sauer U, Antelmann H, Helmann JD. 2012. A global investigation of the Bacillus subtilis iron-sparing response identifies major changes in metabolism. J Bacteriol 194:2594- 2605. http://dx.doi.org/10.1128/JB.05990-11.
103. Beisel CL, Storz G. 2010. Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol Rev 34:866-882. http://dx.doi.org/10.1111/j.1574-6976.2010.00241.x.
104. Heidrich N, Chinali A, Gerth U, Brantl S. 2006. The small untranslated RNA SR1 from the Bacillus subtilis genome is involved in the regulation of arginine catabolism. Mol Microbiol 62:520-536. http://dx.doi.org/10.1111/j.1365-2958.2006.05384.x.
105. Gimpel M, Heidrich N, Mader U, Krugel H, Brantl S. 2010. A dualfunction sRNA from B. subtilis: SR1 acts as a peptide encodingmRNAon the gapA operon. Mol Microbiol 76:990-1009. http://dx.doi.org/10.1111/j.1365-2958.2010.07158.x.
106. Gimpel M, Preis H, Barth E, Gramzow L, Brantl S. 2012. SR1-A small RNA with two remarkably conserved functions. Nucleic Acids Res 40: 11659-11672. http://dx.doi.org/10.1093/nar/gks895.
107. Geissmann T, Chevalier C, Cros MJ, Boisset S, Fechter P, Noirot C, Schrenzel J, Francois P, Vandenesch F, Gaspin C, Romby P. 2009. A search for small noncoding RNAs in Staphylococcus aureus reveals a conserved sequence motif for regulation. Nucleic Acids Res 37:7239- 7257. http://dx.doi.org/10.1093/nar/gkp668.
108. Durand S, Braun F, Lioliou E, Romilly C, Helfer AC, Kuhn L, Quittot N, Nicolas P, Romby P, Condon C. 2015. A nitric oxide regulated small RNA controls expression of genes involved in redox homeostasis in Bacillus subtilis. PLoS Genet 11:e1004957. http://dx.doi.org/10.1371/journal.pgen.1004957.
109. Schmalisch M, Maiques E, Nikolov L, Camp AH, Chevreux B, Muffler A, Rodriguez S, Perkins J, Losick R. 2010. Small genes under sporulation control in the Bacillus subtilis genome. J Bacteriol 192:5402-5412. http://dx.doi.org/10.1128/JB.00534-10.
110. Silvaggi JM, Perkins JB, Losick R. 2005. Small untranslated RNA antitoxin in Bacillus subtilis. J Bacteriol 187:6641-6650. http://dx.doi.org/10.1128/JB.187.19.6641-6650.2005.
111. Commichau FM, Stulke J. 2012. A mystery unraveled: Essentiality of RNase III in Bacillus subtilis is caused by resident prophages. PLoS Genet 8:e1003199. http://dx.doi.org/10.1371/journal.pgen.1003199.
112. Durand S, Jahn N, Condon C, Brantl S. 2012. Type I toxin-Antitoxin systems in Bacillus subtilis. RNA Biol 9:1491-1497. http://dx.doi.org/10.4161/rna.22358.
113. Jahn N, Preis H, Wiedemann C, Brantl S. 2012. BsrG/SR4 from Bacillus subtilis-The first temperature-dependent type I toxin-Antitoxin system. Mol Microbiol 83:579-598. http://dx.doi.org/10.1111/j.1365-2958.2011.07952.x.
114. Jahn N, Brantl S. 2013. One antitoxin-Two functions: SR4 controls toxin mRNA decay and translation. Nucleic Acids Res 41:9870-9880. http://dx.doi.org/10.1093/nar/gkt735.
115. Meissner C, Jahn N, Brantl S. 2016. In vitro characterization of the type I toxin-Antitoxin system bsrE/SR5 from Bacillus subtilis. J Biol Chem 291:560-571. http://dx.doi.org/10.1074/jbc.M115.697524.
116. Loh E, Dussurget O, Gripenland J, Vaitkevicius K, Tiensuu T, Mandin P, Repoila F, Buchrieser C, Cossart P, Johansson J. 2009. A trans-Acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. Cell 139:770-779. http://dx.doi.org/10.1016/j.cell.2009.08.046.
117. Marchais A, Duperrier S, Durand S, Gautheret D, Stragier P. 2011. CsfG, a sporulation-specific, small non-coding RNA highly conserved in endospore formers. RNA Biol 8:358-364. http://dx.doi.org/10.4161/rna.8.3.14998.
118. Georg J, Hess WR. 2011. cis-Antisense RNA, another level of gene regulation in bacteria. Microbiol Mol Biol Rev 75:286-300. http://dx.doi.org/10.1128/MMBR.00032-10.
119. Brantl S. 2007. Regulatory mechanisms employed by cis-encoded antisense RNAs. Curr Opin Microbiol 10:102-109. http://dx.doi.org/10.1016/j.mib.2007.03.012.
120. Thomason MK, Storz G. 2010. Bacterial antisense RNAs: how many are there, and what are they doing? Annu Rev Genet 44:167-188. http://dx.doi.org/10.1146/annurev-genet-102209-163523.
121. Eiamphungporn W, Helmann JD. 2009. Extracytoplasmic function sigma factors regulate expression of the Bacillus subtilis yabE gene via a cis-Acting antisense RNA. J Bacteriol 191:1101-1105. http://dx.doi.org/10.1128/JB.01530-08.
122. Luo Y, Helmann JD. 2012. A sigmaD-dependent antisense transcript modulates expression of the cyclic-di-AMP hydrolase GdpP in Bacillus subtilis. Microbiology 158:2732-2741. http://dx.doi.org/10.1099/mic.0.062174-0.
123. Guell M, van Noort V, Yus E, Chen WH, Leigh-Bell J, Michalodimi-Trakis K, Yamada T, Arumugam M, Doerks T, Kuhner S, Rode M, Suyama M, Schmidt S, Gavin AC, Bork P, Serrano L. 2009. Transcriptome complexity in a genome-reduced bacterium. Science 326:1268- 1271. http://dx.doi.org/10.1126/science.1176951.
124. Hecker M, Pane-Farre J, Volker U. 2007. SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu Rev Microbiol 61:215-236. http://dx.doi.org/10.1146/annurev.micro.61.080706.093445.
125. Weng M, Nagy PL, Zalkin H. 1995. Identification of the Bacillus subtilis pur operon repressor. Proc Natl Acad Sci U S A 92:7455-7459. http://dx.doi.org/10.1073/pnas.92.16.7455.
126. Freese E, Heinze JE, Galliers EM. 1979. Partial purine deprivation causes sporulation of Bacillus subtilis in the presence of excess ammonia, glucose and phosphate. J Gen Microbiol 115:193-205. http://dx.doi.org/10.1099/00221287-115-1-193.
127. Eijlander RT, de Jong A, Krawczyk AO, Holsappel S, Kuipers OP. 2014. SporeWeb: An interactive journey through the complete sporulation cycle of Bacillus subtilis. Nucleic Acids Res 42:D685-D691. http://dx.doi.org/10.1093/nar/gkt1007.
128. Kobayashi K, Shoji K, Shimizu T, Nakano K, Sato T, Kobayashi Y. 1995. Analysis of a suppressor mutation ssb (kinC) of sur0B20 (spo0A) mutation in Bacillus subtilis reveals that kinC encodes a histidine protein kinase. J Bacteriol 177:176-182.
129. Ingram LO, Vreeland NS. 1980. Differential effects of ethanol and hexanol on the Escherichia coli cell envelope. J Bacteriol 144:481-488.
130. Reichmann NT, Grundling A. 2011. Location, synthesis and function of glycolipids and polyglycerolphosphate lipoteichoic acid in Grampositive bacteria of the phylum Firmicutes. FEMS Microbiol Lett 319:97- 105. http://dx.doi.org/10.1111/j.1574-6968.2011.02260.x.
131. Vogel J, Luisi BF. 2011. Hfq and its constellation of RNA. Nat Rev Microbiol 9:578-589. http://dx.doi.org/10.1038/nrmicro2615.
132. Rochat T, Delumeau O, Figueroa-Bossi N, Noirot P, Bossi L, Dervyn E, Bouloc P. 2015. Tracking the elusive function of Bacillus subtilis Hfq. PLoS One 10:e0124977. http://dx.doi.org/10.1371/journal.pone.0124977.
133. Boisset S, Geissmann T, Huntzinger E, Fechter P, Bendridi N, Possedko M, Chevalier C, Helfer AC, Benito Y, Jacquier A, Gaspin C, Vandenesch F, Romby P. 2007. Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 21:1353-1366. http://dx.doi.org/10.1101/gad.423507.
134. Burke TP, Portnoy DA. 2016. SpoVG is a conserved RNA-binding protein that regulates Listeria monocytogenes lysozyme resistance, virulence, and swarming motility. mBio 7:e00240. http://dx.doi.org/10.1128/mBio.00240-16.
135. Vrentas C, Ghirlando R, Keefer A, Hu Z, Tomczak A, Gittis AG, Murthi A, Garboczi DN, Gottesman S, Leppla SH. 2015. Hfqs in Bacillus anthracis: Role of protein sequence variation in the structure and function of proteins in the Hfq family. Protein Sci 24:1808-1819. http://dx.doi.org/10.1002/pro.2773.
136. Tanay A, Regev A, Shamir R. 2005. Conservation and evolvability in regulatory networks: The evolution of ribosomal regulation in yeast. Proc Natl Acad Sci U S A 102:7203-7208. http://dx.doi.org/10.1073/pnas.0502521102.
137. Goelzer A, Fromion V. 2011. Bacterial growth rate reflects a bottleneck in resource allocation. Biochim Biophys Acta 1810:978-988. http://dx.doi.org/10.1016/j.bbagen.2011.05.014.
138. Kirschner M, Gerhart J. 1998. Evolvability. Proc Natl Acad Sci U S A 95:8420-8427. http://dx.doi.org/10.1073/pnas.95.15.8420.
139. Carvunis AR, Rolland T, Wapinski I, Calderwood MA, Yildirim MA, Simonis N, Charloteaux B, Hidalgo CA, Barbette J, Santhanam B, Brar GA, Weissman JS, Regev A, Thierry-Mieg N, Cusick ME, Vidal M. 2012. Proto-genes and de novo gene birth. Nature 487:370-374. http://dx.doi.org/10.1038/nature11184.
140. Shimoni Y, Friedlander G, Hetzroni G, Niv G, Altuvia S, Biham O, Margalit H. 2007. Regulation of gene expression by small non-coding RNAs: A quantitative view. Mol Syst Biol. 3:138. http://dx.doi.org/10.1038/msb4100181.
141. Arrieta-Ortiz ML, Hafemeister C, Bate AR, Chu T, Greenfield A, Shuster B, Barry SN, Gallitto M, Liu B, Kacmarczyk T, Santoriello F, Chen J, Rodrigues CD, Sato T, Rudner DZ, Driks A, Bonneau R, Eichenberger P. 2015. An experimentally supported model of the Bacillus subtilis global transcriptional regulatory network. Mol Syst Biol 11: 839. http://dx.doi.org/10.15252/msb.20156236.
142. Barquist L, Vogel J. 2015. Accelerating discovery and functional analysis of small RNAs with new technologies. Annu Rev Genet 49:367-394. http://dx.doi.org/10.1146/annurev-genet-112414-054804.
143. Peters JM, Colavin A, Shi H, Czarny TL, Larson MH, Wong S, Hawkins JS, Lu CH, Koo BM, Marta E, Shiver AL, Whitehead EH, Weissman JS, Brown ED, Qi LS, Huang KC, Gross CA. 2016. A comprehensive, CRISPR-based functional analysis of essential genes in bacteria. Cell 165:1493-1506. http://dx.doi.org/10.1016/j.cell.2016.05.003.