Transcription factors and genetic circuits orchestrating the complex, multilayered response of Clostridium acetobutylicum to butanol and butyrate stress

BMC Systems Biology

Volumn 7, Issue , 2013, Pages

  Wang, Qinghua ^a,b   Venkataramanan, Keerthi P ^a   Huang, Hongzhan ^a,b   Papoutsakis, Eleftherios T ^a   Wu, Cathy H ^a,b  

^a UNIVERSITY OF DELAWARE   (United States)

^b University of Delaware   (United States)

Author keywords

Gene expression; Protein protein interaction; TF binding site (TFBS); Transcription factor (TF); Transcriptional regulator (TR); Transcriptional regulatory network (TRN)

Indexed keywords

CLOSTRIDIUM; CLOSTRIDIUM ACETOBUTYLICUM; POSIBACTERIA;

AMINO ACID; BACTERIAL DNA; BUTANOL; BUTYRIC ACID DERIVATIVE; TRANSCRIPTION FACTOR;

ARTICLE; BIOSYNTHESIS; CLOSTRIDIUM ACETOBUTYLICUM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GENOMICS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; REGULON;

AMINO ACIDS; BUTANOLS; BUTYRATES; CLOSTRIDIUM ACETOBUTYLICUM; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; GENOMICS; REGULON; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

EID: 84887028426     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-7-120     Document Type: Article

References (80)

1. Van den Abbeele P, et al. Butyrate-producing Clostridium cluster XIVa species specifically colonize mucins in an in vitro gut model. Isme Journal 2013, 7(5):949-961.
2. Tracy BP, et al. Clostridia: the importance of their exceptional substrate and metabolite diversity for biofuel and biorefinery applications. Curr Opin Biotechnol 2012, 23(3):364-381.
3. 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.
4. Papoutsakis ET. Engineering solventogenic clostridia. Curr Opin Biotechnol 2008, 19(5):420-429.
5. Jones SW, et al. The transcriptional program underlying the physiology of clostridial sporulation. Genome Biol 2008, 9(7):R114.
6. Alsaker K, Papoutsakis ET. Microarray-based analysis of the stress response in clostridium acetobutylicum cultures. Abstr Pap Am Chem Soc 2004, 227:U245-U245.
7. 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.
8. 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.
9. Honicke D, et al. Global transcriptional changes of Clostridium acetobutylicum cultures with increased butanol: acetone ratios. N Biotechnol 2012, 29(4):485-493.
10. Tomas CA, Beamish J, Papoutsakis ET. Transcriptional analysis of butanol stress and tolerance in Clostridium acetobutylicum. J Bacteriol 2004, 186(7):2006-2018.
11. Janssen H, et al. A proteomic and transcriptional view of acidogenic and solventogenic steady-state cells of Clostridium acetobutylicum in a chemostat culture. Appl Microbiol Biotechnol 2010, 87(6):2209-2226.
12. Hou S, et al. Workflow for quantitative proteomic analysis of Clostridium acetobutylicum ATCC 824 using iTRAQ tags. Methods 2013, 61(3):269-276.
13. Emerson JE, et al. Microarray analysis of the transcriptional responses of Clostridium difficile to environmental and antibiotic stress. J Med Microbiol 2008, 57(6):757-764.
14. Yang SH, et al. Clostridium thermocellum ATCC27405 transcriptomic, metabolomic and proteomic profiles after ethanol stress. BMC Genomics 2012, 13:336.
15. Baer SH, Blaschek HP, Smith TL. Effect of butanol challenge and temperature on lipid-composition and membrane fluidity of butanol-tolerant clostridium-acetobutylicum. Appl Environ Microbiol 1987, 53(12):2854-2861.
16. Baut F, et al. Investigation of acetone-butanol-ethanol fermentation by fluorescence. Appl Microbiol Biotechnol 1994, 41(5):551-555.
17. Isar J, Rangaswamy V. Improved n-butanol production by solvent tolerant Clostridium beijerinckii. Biomass & Bioenergy 2012, 37:9-15.
18. Brochado AR, Typas A. High-throughput approaches to understanding gene function and mapping network architecture in bacteria. Curr Opin Microbiol 2013, 16(2):199-206.
19. Cho B-K, Palsson B, Zengler K. Deciphering the regulatory codes in bacterial genomes. Biotechnol J 2011, 6(9):1052-1063.
20. Thomas-Chollier M, et al. RSAT 2011: regulatory sequence analysis tools. Nucleic Acids Res 2011, 39(Web Server):W86-W91.
21. Janky R, van Helden J. Evaluation of phylogenetic footprint discovery for predicting bacterial cis-regulatory elements and revealing their evolution. BMC Bioinforma 2008, 9(1):37.
22. Novichkov PS, et al. RegPrecise: a database of curated genomic inferences of transcriptional regulatory interactions in prokaryotes. Nucleic Acids Res 2009, 38(Database):D111-D118.
23. Kazakov AE, et al. RegTransBase--a database of regulatory sequences and interactions in a wide range of prokaryotic genomes. Nucleic Acids Res 2007, 35(Database issue):D407-D412.
24. Munch R, et al. Virtual Footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 2005, 21(22):4187-4189.
25. Bailey TL, et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 2009, 37:W202-W208.
26. Altenhoff AM, et al. OMA 2011: orthology inference among 1000 complete genomes. Nucleic Acids Res 2011, 39:D289-D294.
27. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001, 98(9):5116-5121.
28. Paredes CJ, et al. A general framework for designing and validating oligomer-based DNA microarrays and its application to Clostridium acetobutylicum. Appl Environ Microbiol 2007, 73(14):4631-4638.
29. Blom EJ, et al. FIVA: Functional Information Viewer and Analyzer extracting biological knowledge from transcriptome data of prokaryotes. Bioinformatics 2007, 23(9):1161-1163.
30. Kanehisa M, et al. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 2011, 40(D1):D109-D114.
31. Uniprot C. Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res 2012, 41(D1):D43-D47.
32. Janssen H, et al. 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.
33. Schwarz KM, et al. A transcriptional study of acidogenic chemostat cells of Clostridium acetobutylicum - Cellular behavior in adaptation to n-butanol. J Biotechnol 2012, 161(3):366-377.
34. Paredes CJ, Alsaker KV, Papoutsakis ET. A comparative genomic view of clostridial sporulation and physiology. Nat Rev Microbiol 2005, 3(12):969-978.
35. Paredes CJ, Rigoutsos I, Papoutsakis ET. Transcriptional organization of the Clostridium acetobutylicum genome. Nucleic Acids Res 2004, 32(6):1973-1981.
36. Paredes CJ, et al. A general framework for designing and validating oligomer-based DNA microarrays and its application to Clostridium acetobutylicum. Appl Environ Microbiol 2007, 73(14):4631-4638.
37. Schneider TD, Stephens RM. Sequence logos - a New Way to display consensus sequences. Nucleic Acids Res 1990, 18(20):6097-6100.
38. Crooks GE, et al. WebLogo: a sequence logo generator. Genome Res 2004, 14(6):1188-1190.
39. Bahl H, et al. Expression of heat shock genes in Clostridium acetobutylicum. FEMS Microbiol Rev 1995, 17(3):341-348.
40. Chastanet A, Fert J, Msadek T. Comparative genomics reveal novel heat shock regulatory mechanisms in Staphylococcus aureus and other Gram-positive bacteria. Mol Microbiol 2003, 47(4):1061-1073.
41. Homuth G, Mogk A, Schumann W. Post-transcriptional regulation of the Bacillus subtilis dnaK operon. Mol Microbiol 1999, 32(6):1183-1197.
42. Schumann W. The Bacillus subtilis heat shock stimulon. Cell Stress Chaperones 2003, 8(3):207-217.
43. Hu Y, et al. Transcriptomic and phenotypic analyses suggest a network between the transcriptional regulators HrcA and sigma(B) in Listeria monocytogenes. Appl Environ Microbiol 2007, 73(24):7981-7991.
44. Beam CE, Saveson CJ, Lovett ST. Role for radA/sms in recombination intermediate processing in Escherichia coli. J Bacteriol 2002, 184(24):6836-6844.
45. Bejerano-Sagie M, et al. A checkpoint protein that scans the chromosome for damage at the start of sporulation in Bacillus subtilis. Cell 2006, 125(4):679-690.
46. Tao L, Chattoraj P, Biswas I. CtsR Regulation in mcsAB-Deficient Gram-Positive Bacteria. J Bacteriol 2012, 194(6):1361-1368.
47. Alsaker KV, Papoutsakis ET. Transcriptional program of early sporulation and stationary-phase events in Clostridium acetobutylicum. J Bacteriol 2005, 187(20):7103-7118.
48. Millat T, et al. A shift in the dominant phenotype governs the pH-induced metabolic switch of Clostridium acetobutylicumin phosphate-limited continuous cultures. Appl Microbiol Biotechnol 2013, 97(14):6451-6466.
49. Foster JW. Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol 2004, 2(11):898-907.
50. Borden JR, et al. 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.
51. Broadbent JR, et al. Physiological and transcriptional response of lactobacillus casei ATCC 334 to acid stress. J Bacteriol 2010, 192(9):2445-2458.
52. Trip H, Mulder NL, Lolkema JS. Improved Acid Stress Survival of Lactococcus lactis Expressing the Histidine Decarboxylation Pathway of Streptococcus thermophilus CHCC1524. J Biol Chem 2012, 287(14):11195-11204.
53. Hirasawa T, et al. Identification of target genes conferring ethanol stress tolerance to Saccharomyces cerevisiae based on DNA microarray data analysis. J Biotechnol 2007, 131(1):34-44.
54. Santiago B, et al. The branched-chain amino acid aminotransferase encoded by ilvE is involved in acid tolerance in Streptococcus mutans. J Bacteriol 2012, 194(8):2010-2019.
55. Foster JW. When protons attack: microbial strategies of acid adaptation. Curr Opin Microbiol 1999, 2(2):170-174.
56. Leyn SA, et al. Genomic reconstruction of the transcriptional regulatory network in bacillus subtilis. J Bacteriol 2013, 195(11):2463-2473.
57. Michel B. After 30 years of study, the bacterial SOS response still surprises us. Plos Biology 2005, 3(7):e255.
58. 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.
59. Shiba T, et al. Sos-Inducible DNA-Repair Proteins, Ruva and Ruvb, of Escherichia-Coli - Functional Interactions between Ruva and Ruvb for Atp Hydrolysis and Renaturation of the Cruciform Structure in Supercoiled DNA. Proc Natl Acad Sci USA 1991, 88(19):8445-8449.
60. Sancar GB, et al. The uvrB gene of Escherichia coli has both lexA-repressed and lexA-independent promoters. Cell 1982, 28(3):523-530.
61. Au N, et al. Genetic composition of the Bacillus subtilis SOS system. J Bacteriol 2005, 187(22):7655-7666.
62. Ravcheev DA, et al. Transcriptional regulation of central carbon and energy metabolism in bacteria by redox-responsive repressor Rex. J Bacteriol 2011, 194(5):1145-1157.
63. 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.
64. Hillmann F, et al. PerR acts as a switch for oxygen tolerance in the strict anaerobe Clostridium acetobutylicum. Mol Microbiol 2008, 68(4):848-860.
65. Hillmann F, et al. The role of PerR in O2-affected gene expression of clostridium acetobutylicum. J Bacteriol 2009, 191(19):6082-6093.
66. Makarova KS, Mironov AA, Gelfand MS. Conservation of the binding site for the arginine repressor in all bacterial lineages. Genome Biol 2001, 2(4). RESEARCH0013.
67. Lim D, et al. Nucleotide sequence of the argR gene of Escherichia coli K-12 and isolation of its product, the arginine repressor. Proc Natl Acad Sci 1987, 84(19):6697-6701.
68. Schaumburg CS, Tan M. Arginine-dependent gene regulation via the ArgR repressor is species specific in Chlamydia. J Bacteriol 2006, 188(3):919-927.
69. Blom EJ, et al. MOTIFATOR: detection and characterization of regulatory motifs using prokaryote transcriptome data. Bioinformatics 2009, 25(4):550-551.
70. Schneider A, Dessimoz C, Gonnet GH. OMA Browser - Exploring orthologous relations across 352 complete genomes. Bioinformatics 2007, 23(16):2180-2182.
71. Even S, et al. Global control of cysteine metabolism by CymR in Bacillus subtilis. J Bacteriol 2006, 188(6):2184-2197.
72. Tanous C, et al. The CymR regulator in complex with the enzyme CysK controls cysteine metabolism in Bacillus subtilis. J Biol Chem 2008, 283(51):35551-35560.
73. Franceschini A, et al. STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 2013, 41(D1):D808-D815.
74. Venkataramanan KP, et al. The Clostridium small RNome that responds to stress: the paradigm and importance of toxic metabolite stress in C. acetobutylicum. BMC Genomics In press.
75. Fu Y, Jarboe LR, Dickerson JA. Reconstructing genome-wide regulatory network of E. coli using transcriptome data and predicted transcription factor activities. BMC Bioinforma 2011, 12(1):233.
76. Smyth GK. Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions Using R and Bioconductor 2005, 397-420. New York: Springer.
77. Yang H. A segmental nearest neighbor normalization and gene identification method gives superior results for DNA-array analysis. Proc Natl Acad Sci 2003, 100(3):1122-1127.
78. Saeed AI, et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003, 34(2):374-378.
79. Eisen MB, et al. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998, 95(25):14863-14868.
80. Shannon P, et al. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res 2003, 13(11):2498-2504.