The Clostridium small RNome that responds to stress: The paradigm and importance of toxic metabolite stress in C. acetobutylicum

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Venkataramanan, Keerthi P ^a   Jones, Shawn W ^a   McCormick, Kevin P ^a,b   Kunjeti, Sridhara G ^a   Ralston, Matthew T ^a   Meyers, Blake C ^a   Papoutsakis, Eleftherios T ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b University of Delaware   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BUTANOL; BUTYRIC ACID; HFQ PROTEIN; MESSENGER RNA; SMALL UNTRANSLATED RNA; TRANSFER RNA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; AMINO ACID SEQUENCE; ARTICLE; BACILLUS SUBTILIS; BACTERIUM CULTURE; BINDING SITE; CHEMICAL STRESS; CLOSTRIDIUM ACETOBUTYLICUM; DOWN REGULATION; ESCHERICHIA COLI; GENE CLUSTER; GENE MAPPING; METABOLIC STRESS; NONHUMAN; NORTHERN BLOTTING; OPEN READING FRAME; OPERON; PROTEIN EXPRESSION; PROTEIN MOTIF; REAL TIME POLYMERASE CHAIN REACTION; REGULON; RNA ISOLATION; RNA PROCESSING; RNA SEQUENCE; TRANSCRIPTION INITIATION SITE;

CLOSTRIDIUM; CLOSTRIDIUM ACETOBUTYLICUM; PROKARYOTA;

BINDING SITES; BUTANOLS; BUTYRIC ACID; CLOSTRIDIUM ACETOBUTYLICUM; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENOMICS; HEAT-SHOCK PROTEINS; HOST FACTOR 1 PROTEIN; NUCLEIC ACID CONFORMATION; NUCLEOTIDE MOTIFS; PROTEIN BINDING; REPRODUCIBILITY OF RESULTS; RNA, SMALL UNTRANSLATED; SEQUENCE ANALYSIS, RNA; STRESS, PHYSIOLOGICAL;

EID: 84888800671     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-849     Document Type: Article

References (93)

1. Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EGH, Margalit H, Altuvia S. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 2001, 11(12):941-950. 10.1016/S0960-9822(01)00270-6, 11448770.
2. Brownlee GG. Sequence of 6s RNA of E. coli. Nature-New Biol 1971, 229(5):147.
3. Hindley J. Fractionation of 32P-labelled ribonucleic acids on polyacrylamide gels and their characterization by fingerprinting. J Mol Biol 1967, 30(1):125-136. 10.1016/0022-2836(67)90248-3, 4865141.
4. Storz G, Haas D. A guide to small RNAs in microorganisms. Curr Opin Microbiol 2007, 10(2):93-95.
5. Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, Bassler BL. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 2004, 118(1):69-82. 10.1016/j.cell.2004.06.009, 15242645.
6. 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(12):3484-3493. 10.1093/nar/gkl453, 1524904, 16870723.
7. Shinhara A, Matsui M, Hiraoka K, Nomura W, Hirano R, Nakahigashi K, Tomita M, Mori H, Kanai A. Deep sequencing reveals as-yet-undiscovered small RNAs in Escherichia coli. BMC Genomics 2011, 12:428. 10.1186/1471-2164-12-428, 3175480, 21864382.
8. Irnov I, Sharma CM, Vogel J, Winkler WC. Identification of regulatory RNAs in Bacillus subtilis. Nucleic acids research 2010, 38(19):6637-6651. 10.1093/nar/gkq454, 2965217, 20525796.
9. Mraheil MA, Billion A, Mohamed W, Mukherjee K, Kuenne C, Pischimarov J, Krawitz C, Retey J, Hartsch T, Chakraborty T, et al. The intracellular sRNA transcriptome of Listeria monocytogenes during growth in macrophages. Nucleic Acids Res 2011, 39(10):4235-4248. 10.1093/nar/gkr033, 3105390, 21278422.
10. Patenge N, Billion A, Raasch P, Normann J, Wisniewska-Kucper A, Retey J, Boisguerin V, Hartsch T, Hain T, Kreikemeyer B. Identification of novel growth phase- and media-dependent small non-coding RNAs in Streptococcus pyogenes M49 using intergenic tiling arrays. BMC Genomics 2012, 13:550. 10.1186/1471-2164-13-550, 3542284, 23062031.
11. Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, Binnewies TT, Hinton JCD, Vogel J. Deep Sequencing Analysis of Small Noncoding RNA and mRNA Targets of the Global Post-Transcriptional Regulator, Hfq. PLoS Genet 2008, 4(8). e1000163. doi:10.1371/journal.pgen.1000163.
12. Sittka A, Sharma CM, Rolle K, Vogel J. Deep sequencing of Salmonella RNA associated with heterologous Hfq proteins in vivo reveals small RNAs as a major target class and identifies RNA processing phenotypes. RNA Biol 2009, 6(3):266-275. 10.4161/rna.6.3.8332, 19333007.
13. Wilms I, Overloper A, Nowrousian M, Sharma CM, Narberhaus F. Deep sequencing uncovers numerous small RNAs on all four replicons of the plant pathogen Agrobacterium tumefaciens. RNA Biol 2012, 9(4):446-457. 10.4161/rna.17212, 3384568, 22336765.
14. Livny J, Waldor MK. Identification of small RNAs in diverse bacterial species. Curr Opin Microbiol 2007, 10(2):96-101. 10.1016/j.mib.2007.03.005, 17383222.
15. Livny J, Fogel MA, Davis BM, Waldor MK. sRNAPredict: an integrative computational approach to identify sRNAs in bacterial genomes. Nucleic Acids Res 2005, 33(13):4096-4105. 10.1093/nar/gki715, 1180744, 16049021.
16. Rivas E, Eddy SR. Noncoding RNA gene detection using comparative sequence analysis. BMC Bioinformatics 2001, 2(1):8. 10.1186/1471-2105-2-8, 64605, 11801179.
17. Pichon C, Felden B. Intergenic sequence inspector: searching and identifying bacterial RNAs. Bioinformatics 2003, 19(13):1707-1709. 10.1093/bioinformatics/btg235, 15593399.
18. Sridhar J, Narmada SR, Sabarinathan R, Ou HY, Deng ZX, Sekar K, Rafi ZA, Rajakumar K. sRNAscanner: A Computational Tool for Intergenic Small RNA Detection in Bacterial Genomes. PloS One 2010, 5(8). e11970. doi: 10.1371/journal.pone.0011970.
19. Domenech P, Honore N, Heym B, Cole ST. Role of OxyS of Mycobacterium tuberculosis in oxidative stress: overexpression confers increased sensitivity to organic hydroperoxides. Microbes Infect 2001, 3(9):713-721. 10.1016/S1286-4579(01)01422-8, 11489419.
20. Mey AR, Craig SA, Payne SM. Characterization of Vibrio cholerae RyhB: the RyhB regulon and role of ryhB in biofilm formation. Infect Immun 2005, 73(9):5706-5719. 10.1128/IAI.73.9.5706-5719.2005, 1231101, 16113288.
21. Davis BM, Quinones M, Pratt J, Ding YP, Waldor MK. Characterization of the small untranslated RNA RyhB and its regulon in Vibrio cholerae. J Bacteriol 2005, 187(12):4005-4014. 10.1128/JB.187.12.4005-4014.2005, 1151736, 15937163.
22. Gottesman S, McCullen C, Guillier M, Vanderpool C, Majdalani N, Benhammou J, Thompson K, FitzGerald P, Sowa N, FitzGerald D. Small RNA regulators and the bacterial response to stress. Cold Spring Harb Symp Quant Biol 2006, 71:1-11. 10.1101/sqb.2006.71.016, 10.1101/sqb.2006.71.016, 3592358, 17381274.
23. Negrete A, Ng WI, Shiloach J. Glucose uptake regulation in E. coli by the small RNA SgrS: comparative analysis of E. coli K-12 (JM109 and MG1655) and E. coli B (BL21). Microb Cell Fact 2010, 9:75. 10.1186/1475-2859-9-75, 10.1186/1475-2859-9-75, 2955591, 20920177.
24. Battesti A, Majdalani N, Gottesman S. The RpoS-Mediated General Stress Response in Escherichia coli. Annu Rev Microbiol 2011, 65:189-213. 10.1146/annurev-micro-090110-102946, 21639793.
25. Mandin P, Gottesman S. Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J 2010, 29(18):3094-3107. 10.1038/emboj.2010.179, 2944060, 20683441.
26. Repoila F, Majdalani N, Gottesman S. Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: the RpoS paradigm. Mol Microbiol 2003, 48(4):855-861. 10.1046/j.1365-2958.2003.03454.x, 12753181.
27. Tracy BP, Jones SW, Fast AG, Indurthi DC, Papoutsakis ET. Clostridia: the importance of their exceptional substrate and metabolite diversity for biofuel and biorefinery applications. Curr Opin Biotechnol 2012, 23(3):364-381. 10.1016/j.copbio.2011.10.008, 22079352.
28. Fast AG, Papoutsakis ET. Stoichiometric and energetic analyses of non-photosynthetic CO2-fixation pathways to support synthetic biology strategies for production of fuels and chemicals. Curr Opin Chem Eng 2012, 1(4):380-395.
29. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, Reyes JA, Shah SA, LeLeiko N, Snapper SB, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 2012, 13(9):R79. 10.1186/gb-2012-13-9-r79, 3506950, 23013615.
30. Alvarez-Ordonez A, Mouwen DJM, Lopez M, Prieto M. Fourier transform infrared spectroscopy as a tool to characterize molecular composition and stress response in foodborne pathogenic bacteria. J Microbiol Meth 2011, 84(3):369-378.
31. Chowdhury R, Sahu GK, Das J. Stress response in pathogenic bacteria. J Biosci 1996, 21(2):149-160.
32. Hassett DJ, Cohen MS. Bacterial Adaptation to Oxidative Stress - Implications for Pathogenesis and Interaction with Phagocytic-Cells. FASEB J 1989, 3(14):2574-2582.
33. Nicolaou SA, Gaida SM, Papoutsakis ET. A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: From biofuels and chemicals, to biocatalysis and bioremediation. Metab Eng 2010, 12(4):307-331. 10.1016/j.ymben.2010.03.004, 20346409.
34. Borden JR, Jones SW, Indurthi D, Chen Y, Papoutsakis ET. A genomic-library based discovery of a novel, possibly synthetic, acid-tolerance mechanism in Clostridium acetobutylicum involving non-coding RNAs and ribosomal RNA processing. Metab Eng 2010, 12(3):268-281. 10.1016/j.ymben.2009.12.004, 2857598, 20060060.
35. Alsaker KV, Paredes C, Papoutsakis ET. Metabolite stress and tolerance in the production of biofuels and chemicals: gene-expression-based systems analysis of butanol, butyrate, and acetate stresses in the anaerobe Clostridium acetobutylicum. Biotechnol Bioeng 2010, 105(6):1131-1147.
36. Gaida SM, Al-Hinai MA, Indurthi D, Nicolaou SA, Papoutsakis ET. Synthetic tolerance: three noncoding small RNAs, DsrA, ArcZ and RprA, acting supra-additively against acid stress. Nucleic Acids Res 2013, 41. 10.1093/nar/gkt1651.
37. Janssen H, Grimmler C, Ehrenreich A, Bahl H, Fischer RJ. A transcriptional study of acidogenic chemostat cells of Clostridium acetobutylicum-Solvent stress caused by a transient n-butanol pulse. J Biotechnol 2012, 161(3):354-365. 10.1016/j.jbiotec.2012.03.027, 22537853.
38. Alsaker KV, Spitzer TR, Papoutsakis ET. Transcriptional analysis of spo0A overexpression in Clostridium acetobutylicum and its effect on the cell's response to butanol stress. J Bacteriol 2004, 186(7):1959-1971. 10.1128/JB.186.7.1959-1971.2004, 374416, 15028679.
39. Tomas CA, Beamish J, Papoutsakis ET. Transcriptional analysis of butanol stress and tolerance in Clostridium acetobutylicum. J Bacteriol 2004, 186(7):2006-2018. 10.1128/JB.186.7.2006-2018.2004, 374415, 15028684.
40. Chen Y, Indurthi DC, Jones SW, Papoutsakis ET. Small RNAs in the genus Clostridium. Ambio 2011, 2(1):e00340-00310. 10.1128/mBio.00340-10.
41. Nicolaou SA, Gaida SM, Papoutsakis ET. Coexisting/Coexpressing Genomic Libraries (CoGeL) identify interactions among distantly located genetic loci for developing complex microbial phenotypes. Nucleic Acids Res 2011, 39(22):e152. 10.1093/nar/gkr817, 3239195, 21976725.
42. Alsaker KV, Papoutsakis ET. Transcriptional program of early sporulation and stationary-phase events in Clostridium acetobutylicum. J Bacteriol 2005, 187(20):7103-7118. 10.1128/JB.187.20.7103-7118.2005, 1251621, 16199581.
43. Paredes CJ, Rigoutsos I, Papoutsakis ET. Transcriptional organization of the Clostridium acetobutylicum genome. Nucleic Acids Res 2004, 32(6):1973-1981. 10.1093/nar/gkh509, 390361, 15060177.
44. Komine Y, Kitabatake M, Yokogawa T, Nishikawa K, Inokuchi H. A Transfer-Rna-Like Structure Is Present in 10sa Rna, a Small Stable Rna from Escherichia coli. Proc Natl Acad Sci USA 1994, 91(20):9223-9227. 10.1073/pnas.91.20.9223, 44784, 7524073.
45. Jones SW, Paredes CJ, Tracy B, Cheng N, Sillers R, Senger RS, Papoutsakis ET. The transcriptional program underlying the physiology of clostridial sporulation. Genome Biol 2008, 9(7):R114. 10.1186/gb-2008-9-7-r114, 2530871, 18631379.
46. Zomer AL, Buist G, Larsen R, Kok J, Kuipers OP. Time-resolved determination of the CcpA regulon of Lactococcus lactis subsp cremoris MG1363. J Bacteriol 2007, 189(4):1366-1381. 10.1128/JB.01013-06, 1797362, 17028270.
47. Paredes CJ, Alsaker KV, Papoutsakis ET. A comparative genomic view of clostridial sporulation and physiology. Nat Rev Microbiol 2005, 3(12):969-978. 10.1038/nrmicro1288, 16261177.
48. Akhter Y, Tundup S, Hasnain SE. Novel biochemical properties of a CRP/FNR family transcription factor from Mycobacterium tuberculosis. Int J Med Microbiol 2007, 297(6):451-457. 10.1016/j.ijmm.2007.04.009, 17702648.
49. Kazakov AE, Rodionov DA, Price MN, Arkin AP, Dubchak I, Novichkov PS. Transcription Factor Family-Based Reconstruction of Singleton Regulons and Study of the Crp/Fnr, ArsR, and GntR Families in Desulfovibrionales Genomes. J Bacteriol 2013, 195(1):29-38. 10.1128/JB.01977-12, 3536172, 23086211.
50. Wietzke M, Bahl H. The redox-sensing protein Rex, a transcriptional regulator of solventogenesis in Clostridium acetobutylicum. Appl Microbiol Biotechnol 2012, 96(3):749-761. 10.1007/s00253-012-4112-2, 22576944.
51. Vogel J, Luisi BF. Hfq and its constellation of RNA. Nat Rev Microbiol 2011, 9(8):578-589. 10.1038/nrmicro2615, 21760622.
52. Otaka H, Ishikawa H, Morita T, Aiba H. PolyU tail of rho-independent terminator of bacterial small RNAs is essential for Hfq action. Proc Natl Acad Sci USA 2011, 108(32):13059-13064. 10.1073/pnas.1107050108, 3156202, 21788484.
53. Papenfort K, Bouvier M, Mika F, Sharma CM, Vogel J. Evidence for an autonomous 5 ' target recognition domain in an Hfq-associated small RNA. Proc Natl Acad Sci U S A 2010, 107(47):20435-20440. 10.1073/pnas.1009784107, 2996696, 21059903.
54. Schumacher MA, Pearson RF, Moller T, Valentin-Hansen P, Brennan RG. Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: a bacterial Sm-like protein. EMBO J 2002, 21(13):3546-3556. 10.1093/emboj/cdf322, 126077, 12093755.
55. Ishikawa H, Otaka H, Maki K, Morita T, Aiba H. The functional Hfq-binding module of bacterial sRNAs consists of a double or single hairpin preceded by a U-rich sequence and followed by a 3 ' poly(U) tail. RNA 2012, 18(5):1062-1074. 10.1261/rna.031575.111, 3334693, 22454537.
56. Ikeda Y, Yagi M, Morita T, Aiba H. Hfq binding at RhlB-recognition region of RNase E is crucial for the rapid degradation of target mRNAs mediated by sRNAs in Escherichia coli. Mol Microbiol 2011, 79(2):419-432. 10.1111/j.1365-2958.2010.07454.x, 21219461.
57. Brennan RG, Link TM. Hfq structure, function and ligand binding. Curr Opin Microbiol 2007, 10(2):125-133. 10.1016/j.mib.2007.03.015, 17395525.
58. Link TM, Valentin-Hansen P, Brennan RG. Structure of Escherichia coli Hfq bound to polyriboadenylate RNA. Proc Natl Acad Sci USA 2009, 106(46):19286-19291. 10.1073/pnas.0905469106, 2780808, 19880750.
59. Beisel CL, Updegrove TB, Janson B, Storz G. Multiple factors dictate target selection by Hfq-binding small RNAs. EMBO J 2012, 31(8):1961-1974. 10.1038/emboj.2012.52, 3343335, 22388518.
60. Schwarz KM, Kuit W, Grimmler C, Ehrenreich A, Kengen SWM. A transcriptional study of acidogenic chemostat cells of Clostridium acetobutylicum - Cellular behavior in adaptation to n-butanol. J Biotechnol 2012, 161(3):366-377. 10.1016/j.jbiotec.2012.03.018, 22484128.
61. Hou S, Jones SW, Choe LH, Papoutsakis ET, Lee KH. Workflow for quantitative proteomic analysis of Clostridia acetobutylicum ATCC 824 using iTRAQ tags. Methods 2013, 61(3):269-276. 10.1016/j.ymeth.2013.03.013, 10.1016/j.ymeth.2013.03.013, 23523702.
62. Wang FQ, Kashket S, Kashket ER. Maintenance of Delta pH by a butanol-tolerant mutant of Clostridium beijerinckii. Microbiol-Sgm 2005, 151:607-613.
63. Heipieper HJ, Weber FJ, Sikkema J, Keweloh H, Debont JAM. Mechanisms of Resistance of Whole Cells to Toxic Organic-Solvents. Trends Biotechnol 1994, 12(10):409-415.
64. Poritz MA, Bernstein HD, Strub K, Zopf D, Wilhelm H, Walter P. An Escherichia coli Ribonucleoprotein Containing 4.5s Rna Resembles Mammalian Signal Recognition Particle. Science 1990, 250(4984):1111-1117. 10.1126/science.1701272, 1701272.
65. Honicke D, Janssen H, Grimmler C, Ehrenreich A, Lutke-Eversloh T. Global transcriptional changes of Clostridium acetobutylicum cultures with increased butanol:acetone ratios. N Biotechnol 2012, 29(4):485-493. 10.1016/j.nbt.2012.01.001, 22285530.
66. Cavanagh AT, Sperger JM, Wassarman KM. Regulation of 6S RNA by pRNA synthesis is required for efficient recovery from stationary phase in E. coli and B. subtilis. Nucleic Acids Res 2012, 40(5):2234-2246. 10.1093/nar/gkr1003, 3299989, 22102588.
67. Geissen R, Steuten B, Polen T, Wagner R. E. coli 6S RNA A universal transcriptional regulator within the centre of growth adaptation. RNA Biol 2010, 7(5):564-568. 10.4161/rna.7.5.12969, 20930516.
68. Sharma UK, Chatterji D. Transcriptional switching in Escherichia coli during stress and starvation by modulation of Sigma 70 activity. FEMS Microbiol Rev 2010, 34(5):646-657.
69. Soutourina OA, Monot M, Boudry P, Saujet L, Pichon C, Sismeiro O, Semenova E, Severinov K, Le Bouguenec C, Coppée J-Y, et al. Genome-Wide Identification of Regulatory RNAs in the Human Pathogen Clostridium difficile. PLoS Genet 2013, 9(5):e1003493. 10.1371/journal.pgen.1003493, 3649979, 23675309.
70. Chae H, Han K, Kim KS, Park H, Lee J, Lee Y. Rho-dependent Termination of ssrS (6S RNA) Transcription in Escherichia coli: implication for 3' processing of 6S RNA and expression of downstream ygfA (putative 5-formyl-tetrahydrofolate cyclo-ligase). J Biol Chem 2011, 286(1):114-122. 10.1074/jbc.M110.150201, 3012964, 21036909.
71. Kim KS, Lee Y. Regulation of 6S RNA biogenesis by switching utilization of both sigma factors and endoribonucleases. Nucleic Acids Res 2004, 32(20):6057-6068. 10.1093/nar/gkh939, 534622, 15550566.
72. Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, Bateman A. Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res 2005, 33:D121-D124. 540035, 15608160.
73. Faucher SP, Friedlander G, Livny J, Margalit H, Shuman HA. Legionella pneumophila 6S RNA optimizes intracellular multiplication. Proc Natl Acad Sci USA 2010, 107(16):7533-7538. 10.1073/pnas.0911764107, 2867745, 20368425.
74. Keiler KC. Biology of trans-Translation. Annu Rev Microbiol 2008, 62:133-151. 10.1146/annurev.micro.62.081307.162948, 18557701.
75. Tadaki T, Fukushima M, Ushida C, Himeno H, Muto A. Interaction of 10Sa RNA with ribosomes in Escherichia coli. FEBS Lett 1996, 399(3):223-226. 10.1016/S0014-5793(96)01330-0, 8985150.
76. Felden B, Himeno H, Muto A, McCutcheon JP, Atkins JF, Gesteland RF. Probing the structure of the Escherichia coli 10Sa RNA (tmRNA). RNA 1997, 3(1):89-103. 1369465, 8990402.
77. Schönhuber W, Le Bourhis G, Tremblay J, Amann R, Kulakauskas S. Utilization of tmRNA sequences for bacterial identification. BMC Microbiol 2001, 1(1):20.
78. Barends S, Kraal B, van Wezel GP. The tmRNA-tagging mechanism and the control of gene expression: a review. Wires RNA 2011, 2(2):233-246. 10.1002/wrna.48, 21957008.
79. Barends S, Zehl M, Bialek S, de Waal E, Traag BA, Willemse J, Jensen ON, Vijgenboom E, van Wezel GP. Transfer-messenger RNA controls the translation of cell-cycle and stress proteins in Streptomyces. EMBO Rep 2009, 11(2):119-125. 2828758, 20019758.
80. Andre G, Even S, Putzer H, Burguiere P, Croux C, Danchin A, Martin-Verstraete I, Soutourina O. S-box and T-box riboswitches and antisense RNA control a sulfur metabolic operon of Clostridium acetobutylicum. Nucleic Acids Res 2008, 36(18):5955-5969. 10.1093/nar/gkn601, 2566862, 18812398.
81. Cornillot E, Nair RV, Papoutsakis ET, Soucaille P. The genes for butanol and acetone formation in Clostridium acetobutylicum ATCC 824 reside on a large plasmid whose loss leads to degeneration of the strain. J Bacteriol 1997, 179(17):5442-5447. 179415, 9286999.
82. Nair RV, Bennett GN, Papoutsakis ET. Molecular characterization of an aldehyde/alcohol dehydrogenase gene from Clostridium acetobutylicum ATCC 824. J Bacteriol 1994, 176(3):871-885. 205125, 8300540.
83. Harris LM, Welker NE, Papoutsakis ET. Northern, morphological, and fermentation analysis of spo0A inactivation and overexpression in Clostridium acetobutylicum ATCC 824. J Bacteriol 2002, 184(13):3586-3597. 10.1128/JB.184.13.3586-3597.2002, 135115, 12057953.
84. Fischer RJ, Helms J, Durre P. Cloning, sequencing, and molecular analysis of the Sol operon of Clostridium acetobutylicum, a chromosomal locus involved in solventogenesis. J Bacteriol 1993, 175(21):6959-6969. 206823, 8226639.
85. Nair RV, Green EM, Watson DE, Bennett GN, Papoutsakis ET. Regulation of the sol locus genes for butanol and acetone formation in Clostridium acetobutylicum ATCC 824 by a putative transcriptional repressor. J Bacteriol 1999, 181(1):319-330. 103564, 9864345.
86. Harris LM, Blank L, Desai RP, Welker NE, Papoutsakis ET. Fermentation characterization and flux analysis of recombinant strains of Clostridium acetobutylicum with an inactivated solR gene. J Ind Microbiol Biotechnol 2001, 27(5):322-328. 10.1038/sj.jim.7000191, 11781808.
87. Schiel B, Nold N, Dürre P. Identification of a small noncoding RNA in Clostridium acetobutylicum. Programme for the 3rd Joint Conference of the German Society for Hygiene and Microbiology (Jahrestagung der Deutschen Gesellschaft für Hygiene und Mikorobiologie [DGHM]) and the Association for General and Applied Microbiology (Jahrestagung der Vereinigung für Allgemeine und Angewandte Mikrobiologie [VAAM]), 28 to 31 March 2010 2010, Hannover, Germany: GRV09:135.
88. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25(9):1105-1111. 10.1093/bioinformatics/btp120, 2672628, 19289445.
89. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 2010, 11(10):R106. 10.1186/gb-2010-11-10-r106, 3218662, 20979621.
90. Macke TJ, Ecker DJ, Gutell RR, Gautheret D, Case DA, Sampath R. RNAMotif, an RNA secondary structure definition and search algorithm. Nucleic Acids Res 2001, 29(22):4724-4735. 10.1093/nar/29.22.4724, 92549, 11713323.
91. Lambert A, Fontaine JF, Legendre M, Leclerc F, Permal E, Major F, Putzer H, Delfour O, Michot B, Gautheret D. The ERPIN server: an interface to profile-based RNA motif identification. Nucleic Acids Res 2004, 32:W160-W165. 10.1093/nar/gkh418, 441556, 15215371.
92. Gruber AR, Lorenz R, Bernhart SH, Neuboock R, Hofacker IL. The Vienna RNA Websuite. Nucleic Acids Res 2008, 36:W70-W74. 10.1093/nar/gkn188, 2447809, 18424795.
93. Hofacker IL. Vienna RNA secondary structure server. Nucleic Acids Res 2003, 31(13):3429-3431. 10.1093/nar/gkg599, 169005, 12824340.