Applied Microbiology and Biotechnology

, Volume 98, Issue 8, pp 3413–3424 | Cite as

Small RNA regulators in bacteria: powerful tools for metabolic engineering and synthetic biology

Mini-Review

Abstract

Small RNAs, a large class of ancient posttranscriptional regulators, have recently attracted considerable attention. A plethora of small RNAs has been identified and characterized, many of which belong to the major small noncoding RNA (sRNA) or riboswitch families. It has become increasingly clear that most small RNAs play critical regulatory roles in many processes and are, therefore, considered to be powerful tools for metabolic engineering and synthetic biology. In this review, we describe recent achievements in the identification, characterization, and application of small RNAs. We give particular attention to advances in the design and synthesis of novel sRNAs and riboswitches for metabolic engineering. In addition, a novel strategy for hierarchical control of global metabolic pathways is proposed.

Keywords

Small RNA Riboswitch Gene expression Posttranscriptional regulation Metabolic engineering Synthetic biology 

References

  1. Alon U (2007) Network motifs: theory and experimental approaches. Nat Rev Genet 8:450–461PubMedGoogle Scholar
  2. Alper H, Moxley J, Nevoigt E, Fink GR, Stephanopoulos G (2006) Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 314:1565–1568PubMedGoogle Scholar
  3. Alper H, Stephanopoulos G (2007) Global transcription machinery engineering: a new approach for improving cellular phenotype. Metab Eng 9:258–267PubMedGoogle Scholar
  4. Altuvia S (2007) Identification of bacterial small non-coding RNAs: experimental approaches. Curr Opin Microbiol 10:257–261PubMedGoogle Scholar
  5. Altuvia S, Wagner EG (2000) Switching on and off with RNA. Proc Natl Acad Sci U S A 97:9824–9826PubMedCentralPubMedGoogle Scholar
  6. Ames TD, Breaker RR (2011) Bacterial aptamers that selectively bind glutamine. RNA Biol 8:82–89PubMedCentralPubMedGoogle Scholar
  7. Balasubramanian D, Vanderpool CK (2013) Deciphering the interplay between two independent functions of the small RNA regulator SgrS in Salmonella. J Bacteriol 195:4620–4630PubMedCentralPubMedGoogle Scholar
  8. Barrick JE, Breaker RR (2007) The distributions, mechanisms, and structures of metabolite-binding riboswitches. Genome Biol 8:R239PubMedCentralPubMedGoogle Scholar
  9. 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 101:6421–6426PubMedCentralPubMedGoogle Scholar
  10. Bayer TS, Smolke CD (2005) Programmable ligand-controlled riboregulators of eukaryotic gene expression. Nat Biotechnol 23:337–343PubMedGoogle Scholar
  11. Beisel CL, Storz G (2010) Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol Rev 34:866–882PubMedCentralPubMedGoogle Scholar
  12. Benenson Y (2012) Synthetic biology with RNA: progress report. Curr Opin Chem Biol 16:278–284PubMedGoogle Scholar
  13. Blouin S, Mulhbacher J, Penedo JC, Lafontaine DA (2009) Riboswitches: ancient and promising genetic regulators. Chembiochem 10:400–416PubMedGoogle Scholar
  14. Boehm A, Vogel J (2012) The csgD mRNA as a hub for signal integration via multiple small RNAs. Mol Microbiol 84:1–5PubMedGoogle Scholar
  15. Breaker RR (2008) Complex riboswitches. Science 319:1795–1797PubMedGoogle Scholar
  16. Breaker RR (2012) Riboswitches and the RNA world. CSH Perspect Biol 4Google Scholar
  17. Ceres P, Garst AD, Marcano-Velazquez JG, Batey RT (2013) Modularity of select riboswitch expression platforms enables facile engineering of novel genetic regulatory devices. ACS Synth Biol 2:463–472PubMedGoogle Scholar
  18. Chappell J, Takahashi MK, Meyer S, Loughrey D, Watters KE, Lucks J (2013) The centrality of RNA for engineering gene expression. Biotechnol J 8:1379–1395PubMedGoogle Scholar
  19. Chen Y, Nielsen J (2013) Advances in metabolic pathway and strain engineering paving the way for sustainable production of chemical building blocks. Curr Opin Biotechnol 24:965–972PubMedGoogle Scholar
  20. Chen Z, Wilmanns M, Zeng AP (2010) Structural synthetic biotechnology: from molecular structure to predictable design for industrial strain development. Trends Biotechnol 28:534–542PubMedGoogle Scholar
  21. Christiansen JK, Nielsen JS, Ebersbach T, Valentin-Hansen P, Sogaard-Andersen L, Kallipolitis BH (2006) Identification of small Hfq-binding RNAs in Listeria monocytogenes. RNA 12:1383–1396PubMedCentralPubMedGoogle Scholar
  22. Coleman J, Green PJ, Inouye M (1984) The use of RNAs complementary to specific mRNAs to regulate the expression of individual bacterial genes. Cell 37:429–436PubMedGoogle Scholar
  23. Cook H, Ussery DW (2013) Sigma factors in a thousand E. coli genomes. Environ Microbiol 15:3121–3129PubMedGoogle Scholar
  24. Coornaert A, Lu A, Mandin P, Springer M, Gottesman S, Guillier M (2010) MicA sRNA links the PhoP regulon to cell envelope stress. Mol Microbiol 76:467–479PubMedCentralPubMedGoogle Scholar
  25. Coppins RL, Hall KB, Groisman EA (2007) The intricate world of riboswitches. Curr Opin Microbiol 10:176–181PubMedCentralPubMedGoogle Scholar
  26. Dahl RH, Zhang F, Alonso-Gutierrez J, Baidoo E, Batth TS, Redding-Johanson AM, Petzold CJ, Mukhopadhyay A, Lee TS, Adams PD, Keasling JD (2013) Engineering dynamic pathway regulation using stress-response promoters. Nat Biotechnol 31:1039–1046PubMedGoogle Scholar
  27. Dambach MD, Winkler WC (2009) Expanding roles for metabolite-sensing regulatory RNAs. Curr Opin Microbiol 12:161–169PubMedCentralPubMedGoogle Scholar
  28. Davidson ME, Harbaugh SV, Chushak YG, Stone MO, Kelley-Loughnane N (2013) Development of a 2,4-dinitrotoluene-responsive synthetic riboswitch in E. coli cells. ACS Chem Biol 8:234–241PubMedGoogle Scholar
  29. Decker KB, Hinton DM (2009) The secret to 6S: regulating RNA polymerase by ribo-sequestration. Mol Microbiol 73:137–140PubMedCentralPubMedGoogle Scholar
  30. Desai RP, Papoutsakis ET (1999) Antisense RNA strategies for metabolic engineering of Clostridium acetobutylicum. Appl Environ Microbiol 65:936–945PubMedCentralPubMedGoogle Scholar
  31. Desai SK, Gallivan JP (2004) Genetic screens and selections for small molecules based on a synthetic riboswitch that activates protein translation. J Am Chem Soc 126:13247–13254PubMedGoogle Scholar
  32. Dietrich JA, McKee AE, Keasling JD (2010) High-throughput metabolic engineering: advances in small-molecule screening and selection. Annu Rev Biochem 79:563–590PubMedGoogle Scholar
  33. Ellington AD (2007) What's so great about RNA? ACS Chem Biol 2:445–448PubMedGoogle Scholar
  34. Fowler CC, Brown ED, Li YF (2010) Using a riboswitch sensor to examine coenzyme B-12 metabolism and transport in E. coli. Chem Biol 17:756–765PubMedGoogle Scholar
  35. Gaida SM, Al-Hinai MA, Indurthi DC, Nicolaou SA, Papoutsakis ET (2013) Synthetic tolerance: three noncoding small RNAs, DsrA, ArcZ and RprA, acting supra-additively against acid stress. Nucleic Acids Res 41:8726–8737PubMedCentralPubMedGoogle Scholar
  36. Geissen R, Steuten B, Polen T, Wagner R (2010) E. coli 6S RNA a universal transcriptional regulator within the centre of growth adaptation. RNA Biol 7:564–568PubMedGoogle Scholar
  37. 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 37:7239–7257PubMedCentralPubMedGoogle Scholar
  38. Gottesman S (2005) Micros for microbes: non-coding regulatory RNAs in bacteria. Trends Genet 21:399–404PubMedGoogle Scholar
  39. Gottesman S, Storz G (2011) Bacterial small RNA regulators: versatile roles and rapidly evolving variations. CSH Perspect Biol 3Google Scholar
  40. Grosshans H, Filipowicz W (2008) Molecular biology: the expanding world of small RNAs. Nature 451:414–416PubMedGoogle Scholar
  41. Grundy FJ, Henkin TM (1998) The S box regulon: a new global transcription termination control system for methionine and cysteine biosynthesis genes in gram-positive bacteria. Mol Microbiol 30:737–749PubMedGoogle Scholar
  42. Heinemann M, Sauer U (2010) Systems biology of microbial metabolism. Curr Opin Microbiol 13:337–343PubMedGoogle Scholar
  43. Henkin TM (2008) Riboswitch RNAs: using RNA to sense cellular metabolism. Genes Dev 22:3383–3390PubMedCentralPubMedGoogle Scholar
  44. Hindley J (1967) Fractionation of 32P-labelled ribonucleic acids on polyacrylamide gels and their characterization by fingerprinting. J Mol Biol 30:125–136PubMedGoogle Scholar
  45. Hoe CH, Raabe CA, Rozhdestvensky TS, Tang TH (2013) Bacterial sRNAs: regulation in stress. Int J Med Microbiol 303:217–229PubMedGoogle Scholar
  46. Huttenhofer A, Vogel J (2006) Experimental approaches to identify non-coding RNAs. Nucleic Acids Res 34:635–646PubMedCentralPubMedGoogle Scholar
  47. Irnov I, Sharma CM, Vogel J, Winkler WC (2010) Identification of regulatory RNAs in Bacillus subtilis. Nucleic Acids Res 38:6637–6651PubMedCentralPubMedGoogle Scholar
  48. Isaacs FJ, Carr PA, Wang HH, Lajoie MJ, Sterling B, Kraal L, Tolonen AC, Gianoulis TA, Goodman DB, Reppas NB, Emig CJ, Bang D, Hwang SJ, Jewett MC, Jacobson JM, Church GM (2011) Precise manipulation of chromosomes in vivo enables genome-wide codon replacement. Science 333:348–353PubMedGoogle Scholar
  49. Jorgensen MG, Thomason MK, Havelund J, Valentin-Hansen P, Storz G (2013) Dual function of the McaS small RNA in controlling biofilm formation. Genes Dev 27:1132–1145PubMedCentralPubMedGoogle Scholar
  50. Joyce GF (2007) Forty years of in vitro evolution. Angew Chem Int Ed Engl 46:6420–6436PubMedGoogle Scholar
  51. Kang Z, Geng YP, Xia YZ, Kang JH, Qi QS (2009) Engineering Escherichia coli for an efficient aerobic fermentation platform. J Biotechnol 144:58–63PubMedGoogle Scholar
  52. Kang Z, Wang Q, Zhang HJ, Qi QS (2008) Construction of a stress-induced system in Escherichia coli for efficient polyhydroxyalkanoates production. Appl Microbiol Biotechnol 79:203–208PubMedGoogle Scholar
  53. Kang Z, Wang XR, Li YK, Wang Q, Qi QS (2012) Small RNA RyhB as a potential tool used for metabolic engineering in Escherichia coli. Biotechnol Lett 34:527–531PubMedGoogle Scholar
  54. Kang Z, Wang Y, Gu PF, Wang Q, Qi QS (2011) Engineering Escherichia coli for efficient production of 5-aminolevulinic acid from glucose. Metab Eng 13:492–498PubMedGoogle Scholar
  55. Keasling JD (2012) Synthetic biology and the development of tools for metabolic engineering. Metab Eng 14:189–195PubMedGoogle Scholar
  56. Kiga D, Futamura Y, Sakamoto K, Yokoyama S (1998) An RNA aptamer to the xanthine/guanine base with a distinctive mode of purine recognition. Nucleic Acids Res 26:1755–1760PubMedCentralPubMedGoogle Scholar
  57. Kim JY, Cha HJ (2003) Down-regulation of acetate pathway through antisense strategy in Escherichia coli: improved foreign protein production. Biotechnol Bioeng 83:841–853PubMedGoogle Scholar
  58. Klein DJ, Ferre-D'Amare AR (2006) Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 313:1752–1756PubMedGoogle Scholar
  59. Klocko AD, Wassarman KM (2009) 6S RNA binding to Esigma(70) requires a positively charged surface of sigma(70) region 4.2. Mol Microbiol 73:152–164PubMedCentralPubMedGoogle Scholar
  60. Kohlstedt M, Becker J, Wittmann C (2010) Metabolic fluxes and beyond-systems biology understanding and engineering of microbial metabolism. Appl Microbiol Biotechnol 88:1065–1075PubMedGoogle Scholar
  61. Lease RA, Smith D, McDonough K, Belfort M (2004) The small noncoding DsrA RNA is an acid resistance regulator in Escherichia coli. J Bacteriol 186:6179–6185PubMedCentralPubMedGoogle Scholar
  62. Lee SY (2011) Metabolic engineering, systems biology and synthetic biology. Microb Biotechnol 4:120–121Google Scholar
  63. Levin A, Lis M, Ponty Y, O'Donnell CW, Devadas S, Berger B, Waldispuhl J (2012) A global sampling approach to designing and reengineering RNA secondary structures. Nucleic Acids Res 40:10041–10052PubMedCentralPubMedGoogle Scholar
  64. Li FF, Wang Y, Gong K, Wang Q, Liang QF, Qi QS (2013a) Constitutive expression of RyhB regulates the heme biosynthesis pathway and increases the 5-aminolevulinic acid accumulation in Escherichia coli. FEMS Microbiol Lett. doi:10.1111/1574-6968.12322 Google Scholar
  65. Li L, Huang DD, Cheung MK, Nong WY, Huang QL, Kwan HS (2013b) BSRD: a repository for bacterial small regulatory RNA. Nucleic Acids Res 41:233–238Google Scholar
  66. Liang JC, Bloom RJ, Smolke CD (2011a) Engineering biological systems with synthetic RNA molecules. Mol Cell 43:915–926PubMedCentralPubMedGoogle Scholar
  67. Liang QF, Zhang HJ, Li SN, Qi QS (2011b) Construction of stress-induced metabolic pathway from glucose to 1,3-propanediol in Escherichia coli. Appl Microbiol Biotechnol 89:57–62PubMedGoogle Scholar
  68. Lipfert J, Das R, Chu VB, Kudaravalli M, Boyd N, Herschlag D, Doniach S (2007) Structural transitions and thermodynamics of a glycine-dependent riboswitch from Vibrio cholerae. J Mol Biol 365:1393–1406PubMedCentralPubMedGoogle Scholar
  69. Livny J, Waldor MK (2007) Identification of small RNAs in diverse bacterial species. Curr Opin Microbiol 10:96–101PubMedGoogle Scholar
  70. Mahmood R, Ali I, Husnain T, Riazuddin S (2008) RNA interference: the story of gene silencing in plants and humans. Biotechnol Adv 26:202–209Google Scholar
  71. 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 95:12462–12467PubMedCentralPubMedGoogle Scholar
  72. Majdalani N, Hernandez D, Gottesman S (2002) Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 46:813–826PubMedGoogle Scholar
  73. Man SA, Cheng RB, Miao CC, Gong QH, Gu YC, Lu XZ, Han F, Yu WG (2011) Artificial trans-encoded small non-coding RNAs specifically silence the selected gene expression in bacteria. Nucleic Acids Res 39:e50Google Scholar
  74. Mandal M, Boese B, Barrick JE, Winkler WC, Breaker RR (2003) Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113:577–586PubMedGoogle Scholar
  75. Masse E, Majdalani N, Gottesman S (2003) Regulatory roles for small RNAs in bacteria. Curr Opin Microbiol 6:120–124PubMedGoogle Scholar
  76. Mehta A, Sonam S, Gouri I, Loharch S, Sharma DK, Parkesh R (2013) SMMRNA: a database of small molecule modulators of RNA. Nucleic Acids Res. doi:10.1093/nar/gkt976 Google Scholar
  77. Miranda-Rios J, Navarro M, Soberon M (2001) A conserved RNA structure (thi box) is involved in regulation of thiamin biosynthetic gene expression in bacteria. Proc Natl Acad Sci U S A 98:9736–9741PubMedCentralPubMedGoogle Scholar
  78. Mizuno T, Chou MY, Inouye M (1984) A unique mechanism regulating gene expression: translational inhibition by a complementary RNA transcript (micRNA). Proc Natl Acad Sci U S A 81:1966–1970PubMedCentralPubMedGoogle Scholar
  79. Muranaka N, Sharma V, Nomura Y, Yokobayashi Y (2009) An efficient platform for genetic selection and screening of gene switches in Escherichia coli. Nucleic Acids Res 37:e39Google Scholar
  80. Na D, Yoo SM, Chung H, Park H, Park JH, Lee SY (2013) Metabolic engineering of Escherichia coli using synthetic small regulatory RNAs. Nat Biotechnol 31:170–174PubMedGoogle Scholar
  81. Nakashima N, Tamura T (2009) Conditional gene silencing of multiple genes with antisense RNAs and generation of a mutator strain of Escherichia coli. Nucleic Acids Res 37:e103Google Scholar
  82. Nakashima N, Tamura T, Good L (2006) Paired termini stabilize antisense RNAs and enhance conditional gene silencing in Escherichia coli. Nucleic Acids Res 34:e138Google Scholar
  83. Negrete A, Majdalani N, Phue JN, Shiloach J (2013) Reducing acetate excretion from E. coli K-12 by over-expressing the small RNA SgrS. N Biotechnol 30:269–273PubMedCentralPubMedGoogle Scholar
  84. Neusser T, Polen T, Geissen R, Wagner R (2010) Depletion of the non-coding regulatory 6S RNA in E. coli causes a surprising reduction in the expression of the translation machinery. BMC Genomics 11:165PubMedCentralPubMedGoogle Scholar
  85. Nielsen J, Pronk JT (2012) Metabolic engineering, synthetic biology and systems biology. FEMS Yeast Res 12:103–103PubMedGoogle Scholar
  86. Nou X, Kadner RJ (2000) Adenosylcobalamin inhibits ribosome binding to btuB RNA. Proc Natl Acad Sci U S A 97:7190–7195PubMedCentralPubMedGoogle Scholar
  87. Ogawa A (2011) Rational design of artificial riboswitches based on ligand-dependent modulation of internal ribosome entry in wheat germ extract and their applications as label-free biosensors. RNA 17:478–488PubMedCentralPubMedGoogle Scholar
  88. Papenfort K, Said N, Welsink T, Lucchini S, Hinton JC, Vogel J (2009) Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol Microbiol 74:139–158PubMedGoogle Scholar
  89. Pfleger BF, Pitera DJ, Smolke CD, Keasling JD (2006) Combinatorial engineering of intergenic regions in operons tunes expression of multiple genes. Nat Biotechnol 24:1027–1032PubMedGoogle Scholar
  90. Pichon C, Felden B (2008) Small RNA gene identification and mRNA target predictions in bacteria. Bioinformatics 24:2807–2813PubMedGoogle Scholar
  91. Qi L, Lucks JB, Liu CC, Mutalik VK, Arkin AP (2012) Engineering naturally occurring trans-acting non-coding RNAs to sense molecular signals. Nucleic Acids Res 40:5775–5786PubMedCentralPubMedGoogle Scholar
  92. Regulski EE, Moy RH, Weinberg Z, Barrick JE, Yao Z, Ruzzo WL, Breaker RR (2008) A widespread riboswitch candidate that controls bacterial genes involved in molybdenum cofactor and tungsten cofactor metabolism. Mol Microbiol 68:918–932PubMedCentralPubMedGoogle Scholar
  93. Repoila F, Darfeuille F (2009) Small regulatory non-coding RNAs in bacteria: physiology and mechanistic aspects. Biol Cell 101:117–131PubMedGoogle Scholar
  94. Rodrigo G, Landrain TE, Jaramillo A (2012) De novo automated design of small RNA circuits for engineering synthetic riboregulation in living cells. Proc Natl Acad Sci U S A 109:15271–15276PubMedCentralPubMedGoogle Scholar
  95. Rodrigo G, Landrain TE, Shen S, Jaramillo A (2013) A new frontier in synthetic biology: automated design of small RNA devices in bacteria. Trends Genet 29:529–536PubMedGoogle Scholar
  96. Romby P, Charpentier E (2010) An overview of RNAs with regulatory functions in gram-positive bacteria. Cell Mol Life Sci 67:217–237PubMedGoogle Scholar
  97. Roth A, Winkler WC, Regulski EE, Lee BW, Lim J, Jona I, Barrick JE, Ritwik A, Kim JN, Welz R, Iwata-Reuyl D, Breaker RR (2007) A riboswitch selective for the queuosine precursor preQ1 contains an unusually small aptamer domain. Nat Struct Mol Biol 14:308–317PubMedGoogle Scholar
  98. Santos CN, Stephanopoulos G (2008) Combinatorial engineering of microbes for optimizing cellular phenotype. Curr Opin Chem Biol 12:168–176PubMedGoogle Scholar
  99. Scheel M, Lutke-Eversloh T (2013) New options to engineer biofuel microbes: development and application of a high-throughput screening system. Metab Eng 17:51–58PubMedGoogle Scholar
  100. Serganov A (2009) The long and the short of riboswitches. Curr Opin Struct Biol 19:251–259PubMedCentralPubMedGoogle Scholar
  101. Serganov A, Patel DJ (2007) Ribozymes, riboswitches and beyond: regulation of gene expression without proteins. Nat Rev Genet 8:776–790PubMedGoogle Scholar
  102. Serganov A, Patel DJ (2012) Metabolite recognition principles and molecular mechanisms underlying riboswitch function. Annu Rev Biophys 41:343–370PubMedGoogle Scholar
  103. Seshasayee AS, Bertone P, Fraser GM, Luscombe NM (2006) Transcriptional regulatory networks in bacteria: from input signals to output responses. Curr Opin Microbiol 9:511–519PubMedGoogle Scholar
  104. Sharma CM, Vogel J (2009) Experimental approaches for the discovery and characterization of regulatory small RNA. Curr Opin Microbiol 12:536–546PubMedGoogle Scholar
  105. Sharma V, Yamamura A, Yokobayashi Y (2012) Engineering artificial small RNAs for conditional gene silencing in Escherichia coli. ACS Synth Biol 1:6–13PubMedGoogle Scholar
  106. Sinha J, Reyes SJ, Gallivan JP (2010) Reprogramming bacteria to seek and destroy an herbicide. Nat Chem Biol 6:464–470PubMedCentralPubMedGoogle Scholar
  107. Sledjeski DD, Gupta A, Gottesman S (1996) The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J 15:3993–4000PubMedCentralPubMedGoogle Scholar
  108. Sonnleitner E, Romeo A, Blasi U (2012) Small regulatory RNAs in Pseudomonas aeruginosa. RNA Biol 9:364–371PubMedGoogle Scholar
  109. Srivastava R, Cha HJ, Peterson MS, Bentley WE (2000) Antisense downregulation of sigma(32) as a transient metabolic controller in Escherichia coli: effects on yield of active organophosphorus hydrolase. Appl Environ Microbiol 66:4366–4371PubMedCentralPubMedGoogle Scholar
  110. Steuten B, Setny P, Zacharias M, Wagner R (2013) Mapping the spatial neighborhood of the regulatory 6S RNA bound to Escherichia coli RNA polymerase holoenzyme. J Mol Biol 425:3649–3661PubMedGoogle Scholar
  111. Stevens DC, Conway KR, Pearce N, Villegas-Penaranda LR, Garza AG, Boddy CN (2013) Alternative sigma factor over-expression enables heterologous expression of a type II polyketide biosynthetic pathway in Escherichia coli. PLoS One 8:64858Google Scholar
  112. Storz G, Opdyke JA, Zhang A (2004) Controlling mRNA stability and translation with small, noncoding RNAs. Curr Opin Microbiol 7:140–144PubMedGoogle Scholar
  113. Sudarsan N, Lee ER, Weinberg Z, Moy RH, Kim JN, Link KH, Breaker RR (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321:411–413PubMedGoogle Scholar
  114. Suess B, Weigand JE (2008) Engineered riboswitches—overview, problems and trends. RNA Biol 5:24–29PubMedGoogle Scholar
  115. Tannler S, Zamboni N, Kiraly C, Aymerich S, Sauer U (2008) Screening of Bacillus subtilis transposon mutants with altered riboflavin production. Metab Eng 10:216–226PubMedGoogle Scholar
  116. Tjaden B, Goodwin SS, Opdyke JA, Guillier M, Fu DX, Gottesman S, Storz G (2006) Target prediction for small, noncoding RNAs in bacteria. Nucleic Acids Res 34:2791–2802PubMedCentralPubMedGoogle Scholar
  117. Topp S, Gallivan JP (2007) Guiding bacteria with small molecules and RNA. J Am Chem Soc 129:6807–6811PubMedCentralPubMedGoogle Scholar
  118. Topp S, Reynoso CMK, Seeliger JC, Goldlust IS, Desai SK, Murat D, Shen A, Puri AW, Komeili A, Bertozzi CR, Scott JR, Gallivan JP (2010) Synthetic riboswitches that induce gene expression in diverse bacterial species. Appl Environ Microbiol 76:7881–7884PubMedCentralPubMedGoogle Scholar
  119. Trotochaud AE, Wassarman KM (2004) 6S RNA function enhances long-term cell survival. J Bacteriol 186:4978–4985PubMedCentralPubMedGoogle Scholar
  120. Vanderpool CK, Gottesman S (2004) Involvement of a novel transcriptional activator and small RNA in post-transcriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system. Mol Microbiol 54:1076–1089PubMedGoogle Scholar
  121. Vejnar CE, Blum M, Zdobnov EM (2013) miRmap web: comprehensive microRNA target prediction online. Nucleic Acids Res 41:165–168Google Scholar
  122. Vitreschak AG, Rodionov DA, Mironov AA, Gelfand MS (2004) Riboswitches: the oldest mechanism for the regulation of gene expression? Trends Genet 20:44–50PubMedGoogle Scholar
  123. Vogel J, Papenfort K (2006) Small non-coding RNAs and the bacterial outer membrane. Curr Opin Microbiol 9:605–611PubMedGoogle Scholar
  124. Wachsmuth M, Findeiss S, Weissheimer N, Stadler PF, Morl M (2013) De novo design of a synthetic riboswitch that regulates transcription termination. Nucleic Acids Ress 41:2541–2551Google Scholar
  125. Wadler CS, Vanderpool CK (2007) A dual function for a bacterial small RNA: SgrS performs base pairing-dependent regulation and encodes a functional polypeptide. Proc Natl Acad Sci U S A 104:20454–20459PubMedCentralPubMedGoogle Scholar
  126. Wadler CS, Vanderpool CK (2009) Characterization of homologs of the small RNA SgrS reveals diversity in function. Nucleic Acids Res 37:5477–5485PubMedCentralPubMedGoogle Scholar
  127. Wang HH, Isaacs FJ, Carr PA, Sun ZZ, Xu G, Forest CR, Church GM (2009) Programming cells by multiplex genome engineering and accelerated evolution. Nature 460:894–898PubMedGoogle Scholar
  128. Wang JX, Lee ER, Morales DR, Lim J, Breaker RR (2008) Riboswitches that sense S-adenosylhomocysteine and activate genes involved in coenzyme recycling. Mol Cell 29:691–702PubMedCentralPubMedGoogle Scholar
  129. Wassarman KM (2007) 6S RNA: a small RNA regulator of transcription. Curr Opin Microbiol 10:164–168PubMedGoogle Scholar
  130. Wassarman KM, Repoila F, Rosenow C, Storz G, Gottesman S (2001) Identification of novel small RNAs using comparative genomics and microarrays. Gene Dev 15:1637–1651PubMedCentralPubMedGoogle Scholar
  131. Wassarman KM, Storz G (2000) 6S RNA regulates E. coli RNA polymerase activity. Cell 101:613–623PubMedGoogle Scholar
  132. Waters LS, Storz G (2009) Regulatory RNAs in bacteria. Cell 136:615–628PubMedCentralPubMedGoogle Scholar
  133. Win MN, Smolke CD (2007) A modular and extensible RNA-based gene-regulatory platform for engineering cellular function. Proc Natl Acad Sci U S A 104:14283–14288PubMedCentralPubMedGoogle Scholar
  134. Winkler W, Nahvi A, Breaker RR (2002a) Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419:952–956PubMedGoogle Scholar
  135. Winkler WC, Cohen-Chalamish S, Breaker RR (2002b) An mRNA structure that controls gene expression by binding FMN. Proc Natl Acad Sci U S A 99:15908–15913PubMedCentralPubMedGoogle Scholar
  136. Wurm R, Neusser T, Wagner R (2010) 6S RNA-dependent inhibition of RNA polymerase is released by RNA-dependent synthesis of small de novo products. Biol Chem 391:187–196PubMedGoogle Scholar
  137. Yang J, Seo SW, Jang S, Shin SI, Lim CH, Roh TY, Jung GY (2013) Synthetic RNA devices to expedite the evolution of metabolite-producing microbes. Nat Commun 4:1413PubMedGoogle Scholar
  138. Yoo SM, Na D, Lee SY (2013) Design and use of synthetic regulatory small RNAs to control gene expression in Escherichia coli. Nat Protoc 8:1694–1707PubMedGoogle Scholar
  139. Zhang A, Altuvia S, Tiwari A, Argaman L, Hengge-Aronis R, Storz G (1998) The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J 17:6061–6068PubMedCentralPubMedGoogle Scholar
  140. Zhao Y, Huang Y, Gong Z, Wang Y, Man J, Xiao Y (2012) Automated and fast building of three-dimensional RNA structures. Sci Rep 2:734PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Zhen Kang
    • 1
    • 2
    • 4
    • 6
  • Chuanzhi Zhang
    • 2
  • Junli Zhang
    • 2
  • Peng Jin
    • 2
  • Juan Zhang
    • 1
    • 2
    • 4
  • Guocheng Du
    • 1
    • 2
    • 3
    • 4
  • Jian Chen
    • 1
    • 2
    • 4
    • 5
  1. 1.Synergetic Innovation Center of Food Safety and NutritionWuxiChina
  2. 2.The Key Laboratory of Industrial Biotechnology, Ministry of EducationJiangnan UniversityWuxiChina
  3. 3.The Key Laboratory of Carbohydrate Chemistry and Biotechnology, Ministry of EducationJiangnan UniversityWuxiChina
  4. 4.Synergy Innovation Center of Modern Industrial FermentationWuxiChina
  5. 5.National Engineering Laboratory for Cereal Fermentation TechnologyJiangnan UniversityWuxiChina
  6. 6.Yixing Union Biochemical Co., Ltd.WuxiChina

Personalised recommendations