Capturing the response of Clostridium acetobutylicum to chemical stressors using a regulated genome-scale metabolic model

Biotechnology for Biofuels

Volumn 7, Issue 1, 2014, Pages

  Dash, Satyakam ^a   Mueller, Thomas J ^a   Venkataramanan, Keerthi P ^b,c   Papoutsakis, Eleftherios T ^b,c   Maranas, Costas D ^a  

^a The Pennsylvania State University   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

^c University of Delaware   (United States)

Author keywords

Clostridium acetobutylicum; CoreReg; Genome scale metabolic model; Regulation

Indexed keywords

ACETONE; ASSOCIATION REACTIONS; BIOMASS; CLOSTRIDIUM; FERMENTATION; GENES; METABOLISM; PHYSIOLOGY; YIELD STRESS;

ACETONE-BUTANOL-ETHANOL FERMENTATION; CLOSTRIDIUM ACETOBUTYLICUM; COREREG; GENOME SCALE METABOLIC MODEL; INDUSTRIAL COMPOUNDS; METABOLIC CAPACITIES; REGULATION; SUBSTRATE UTILIZATION;

METABOLIC ENGINEERING;

BACTERIUM; BIOFUEL; FERMENTATION; GENOME; METABOLISM; MODEL TEST; MODEL VALIDATION; REACTION KINETICS; SUBSTRATE;

CLOSTRIDIA; CLOSTRIDIUM ACETOBUTYLICUM; FIRMICUTES; POSIBACTERIA;

EID: 84988815635     PISSN: 17546834     EISSN: None     Source Type: Journal    
DOI: 10.1186/s13068-014-0144-4     Document Type: Article

References (59)

1. 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, 23:364-381.
2. Papoutsakis ET: Engineering solventogenic clostridia. Curr Opin Biotechnol 2008, 19:420-429.
3. Wang Q, Venkataramanan KP, Huang H, Papoutsakis ET, Wu CH: Transcription factors and genetic circuits orchestrating the complex, multilayered response of Clostridium acetobutylicum to butanol and butyrate stress. BMC Syst Biol 2013, 7:120.
4. Venkataramanan KP, Jones SW, McCormick KP, Kunjeti SG, Ralston MT, Meyers BC, Papoutsakis ET: The Clostridium small RNome that responds to stress: the paradigm and importance of toxic metabolite stress in C. acetobutylicum. BMC Genomics 2013, 14:849.
5. 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, 105:1131-1147.
6. 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, 161:366-377.
7. 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, 161:354-365.
8. Hou S, Jones SW, Choe LH, Papoutsakis ET, Lee KH: Workflow for quantitative proteomic analysis of Clostridium acetobutylicum ATCC 824 using iTRAQ tags. Methods 2013, 61:269-276.
9. Feist AM, Herrgard MJ, Thiele I, Reed JL, Palsson BO: Reconstruction of biochemical networks in microorganisms. Nat Rev Microbiol 2009, 7:129-143.
10. Burgard AP, Pharkya P, Maranas CD: OptKnock: a bilevel programming framework for identifying gene knockout strategies for microbial strain optimization. Biotechnol Bioeng 2003, 84:647-657.
11. Oliveira AP, Nielsen J, Forster J: Modeling Lactococcus lactis using a genome-scale flux model. BMC Microbiol 2005, 5:39.
12. Alper H, Jin YS, Moxley JF, Stephanopoulos G: Identifying gene targets for the metabolic engineering of lycopene biosynthesis in Escherichia coli. Metab Eng 2005, 7:155-164.
13. Pharkya P, Maranas CD: An optimization framework for identifying reaction activation/inhibition or elimination candidates for overproduction in microbial systems. Metab Eng 2006, 8:1-13.
14. Almaas E, Kovacs B, Vicsek T, Oltvai ZN, Barabasi AL: Global organization of metabolic fluxes in the bacterium Escherichia coli. Nature 2004, 427:839-843.
15. Burgard AP, Nikolaev EV, Schilling CH, Maranas CD: Flux coupling analysis of genome-scale metabolic network reconstructions. Genome Res 2004, 14:301-312.
16. Motter AE, Gulbahce N, Almaas E, Barabasi AL: Predicting synthetic rescues in metabolic networks. Mol Syst Biol 2008, 4:168.
17. Jin YS, Jeffries TW: Stoichiometric network constraints on xylose metabolism by recombinant Saccharomyces cerevisiae. Metab Eng 2004, 6:229-238.
18. Papoutsakis ET: Equations and calculations for fermentations of butyric acid bacteria. Biotechnol Bioeng 1984, 26:174-187.
19. Desai RP, Harris LM, Welker NE, Papoutsakis ET: Metabolic flux analysis elucidates the importance of the acid-formation pathways in regulating solvent production by Clostridium acetobutylicum. Metab Eng 1999, 1:206-213.
20. Lee J, Yun H, Feist AM, Palsson BO, Lee SY: Genome-scale reconstruction and in silico analysis of the Clostridium acetobutylicum ATCC 824 metabolic network. Appl Microbiol Biotechnol 2008, 80:849-862.
21. Senger RS, Papoutsakis ET: Genome-scale model for Clostridium acetobutylicum: Part I. Metabolic network resolution and analysis. Biotechnol Bioeng 2008, 101:1036-1052.
22. McAnulty MJ, Yen JY, Freedman BG, Senger RS: Genome-scale modeling using flux ratio constraints to enable metabolic engineering of clostridial metabolism in silico. BMC Syst Biol 2012, 6:42.
23. Henry CS, DeJongh M, Best AA, Frybarger PM, Linsay B, Stevens RL: High-throughput generation, optimization and analysis of genome-scale metabolic models. Nat Biotechnol 2010, 28:977-982.
24. Crown SB, Indurthi DC, Ahn WS, Choi J, Papoutsakis ET, Antoniewicz MR: Resolving the TCA cycle and pentose-phosphate pathway of Clostridium acetobutylicum ATCC 824: Isotopomer analysis, in vitro activities and expression analysis. Biotechnol J 2011, 6:300-305.
25. Au J, Choi J, Jones SW, Venkataramanan KP, Antoniewicz MR: Parallel labeling experiments validate Clostridium acetobutylicum metabolic network model for 13C metabolic flux analysis. Metabolic engineering, 26:23-33.
26. Covert MW, Palsson BO: Transcriptional regulation in constraints-based metabolic models of Escherichia coli. J Biol Chem 2002, 277:28058-28064.
27. Covert MW, Schilling CH, Palsson B: Regulation of gene expression in flux balance models of metabolism. J Theor Biol 2001, 213:73-88.
28. Shlomi T, Eisenberg Y, Sharan R, Ruppin E: A genome-scale computational study of the interplay between transcriptional regulation and metabolism. Mol Syst Biol 2007, 3:101.
29. Barua D, Kim J, Reed JL: An automated phenotype-driven approach (GeneForce) for refining metabolic and regulatory models. PLoS Comput Biol 2010, 6:e1000970.
30. Chandrasekaran S, Price ND: Probabilistic integrative modeling of genome-scale metabolic and regulatory networks in Escherichia coli and Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 2010, 107:17845-17850.
31. Schmidt BJ, Ebrahim A, Metz TO, Adkins JN, Palsson BO, Hyduke DR: GIM3E: condition-specific models of cellular metabolism developed from metabolomics and expression data. Bioinformatics 2013, 29:2900-2908.
32. Yizhak K, Gabay O, Cohen H, Ruppin E: Model-based identification of drug targets that revert disrupted metabolism and its application to ageing. Nat Commun 2013, 4:2632.
33. Ranganathan S, Suthers PF, Maranas CD: OptForce: an optimization procedure for identifying all genetic manipulations leading to targeted overproductions. PLoS Comput Biol 2010, 6:e1000744.
34. Colijn C, Brandes A, Zucker J, Lun DS, Weiner B, Farhat MR, Cheng TY, Moody DB, Murray M, Galagan JE: Interpreting expression data with metabolic flux models: predicting Mycobacterium tuberculosis mycolic acid production. PLoS Comput Biol 2009, 5:e1000489.
35. Meyer CL, Roos JW, Papoutsakis ET: Carbon-monoxide gasing leads to alcohol production and butyrate uptake without acetone formation in continuous cultures of Clostridium acetobutylicum. Appl Microbiol Biotechnol 1986, 24:159-167.
36. Jiang Y, Xu C, Dong F, Yang Y, Jiang W, Yang S: Disruption of the acetoacetate decarboxylase gene in solvent-producing Clostridium acetobutylicum increases the butanol ratio. Metab Eng 2009, 11:284-291.
37. Lehmann D, Radomski N, Lutke-Eversloh T: New insights into the butyric acid metabolism of Clostridium acetobutylicum. Appl Microbiol Biotechnol 2012, 96:1325-1339.
38. Meyer CL, Papoutsakis ET: Increased levels of ATP and NADH are associated with increased solvent production in continuous cultures of Clostridium acetobutylicum. Appl Microbiol Biotechnol 1989, 30:450-459.
39. Vasconcelos I, Girbal L, Soucaille P: Regulation of carbon and electron flow in Clostridium acetobutylicum grown in chemostat culture at neutral pH on mixtures of glucose and glycerol. J Bacteriol 1994, 176:1443-1450.
40. Meyer CL, Papoutsakis ET: Continuous and biomass recycle fermentations of Clostridium acetobutylicum.2. Novel patterns in energetics and product-formation kinetics. Bioprocess Eng 1989, 4:49-55.
41. Meyer CL, Papoutsakis ET: Continuous and biomass recycle fermentations of Clostridium acetobutylicum.1. ATP supply and demand determines product selectivity. Bioprocess Eng 1989, 4:1-10.
42. Cooksley CM, Zhang Y, Wang H, Redl S, Winzer K, Minton NP: Targeted mutagenesis of the Clostridium acetobutylicum acetone-butanol-ethanol fermentation pathway. Metab Eng 2012, 14:630-641.
43. Kuit W, Minton NP, Lopez-Contreras AM, Eggink G: Disruption of the acetate kinase (ack) geneofClostridium acetobutylicum results in delayed acetate production. Appl Microbiol Biotechnol 2012, 94:729-741.
44. Jang YS, Lee JY, Lee J, Park JH, Im JA, Eom MH, Lee J, Lee SH, Song H, Cho JH, Seung do Y, Lee SY: Enhanced butanol production obtained by reinforcing the direct butanol-forming route in Clostridium acetobutylicum. MBio 2012, 3:e00314-12.
45. Lehmann D, Lutke-Eversloh T: Switching Clostridium acetobutylicum to an ethanol producer by disruption of the butyrate/butanol fermentative pathway. Metab Eng 2011, 13:464-473.
46. Jones SW, Paredes CJ, Tracy B, Cheng N, Sillers R, Senger RS, Papoutsakis ET: The transcriptional program underlying the physiology of clostridial sporulation. Genome Biology 2008, 9:R114.
47. Huesemann M, Papoutsakis ET: Effect of acetoacetate, butyrate, and uncoupling ionophores on growth and product formation of Clostridium acetobutylicum. Biotechnol Lett 1986, 8:37-42.
48. Husemann MHW, Papoutsakis ET: Solventogenesis in Clostridium acetobutylicum fermentations related to carboxylic-acid and proton concentrations. Biotechnol Bioeng 1988, 32:843-852.
49. Feist AM, Scholten JC, Palsson BO, Brockman FJ, Ideker T: Modeling methanogenesis with a genome-scale metabolic reconstruction of Methanosarcina barkeri. Mol Syst Biol 2006, 2:2006 0004.
50. Reed JL, Famili I, Thiele I, Palsson BO: Towards multidimensional genome annotation. Nat Rev Genet 2006, 7:130-141.
51. Thiele I, Palsson BO: A protocol for generating a high-quality genome-scale metabolic reconstruction. Nat Protoc 2010, 5:93-121.
52. Kumar A, Suthers PF, Maranas CD: MetRxn: a knowledgebase of metabolites and reactions spanning metabolic models and databases. BMC Bioinformatics 2012, 13:6.
53. Childs KL, Hamilton JP, Zhu W, Ly E, Cheung F, Wu H, Rabinowicz PD, Town CD, Buell CR, Chan AP: The TIGR Plant Transcript Assemblies database. Nucleic Acids Res 2007, 35:D846-D851.
54. Mueller TJ, Berla BM, Pakrasi HB, Maranas CD: Rapid construction of metabolic models for a family of Cyanobacteria using a multiple source annotation workflow. BMC Syst Biol 2013, 7:142.
55. Schellenberger J, Lewis NE, Palsson BO: Elimination of thermodynamically infeasible loops in steady-state metabolic models. Biophys J 2011, 100:544-553.
56. Orth JD, Thiele I, Palsson BO: What is flux balance analysis? Nat Biotechnol 2010, 28:245-248.
57. Hou XH, Peng WF, Xiong L, Huang C, Chen XF, Chen XD, Zhang WG: Engineering Clostridium acetobutylicum for alcohol production. J Biotechnol 2013, 166:25-33.
58. Amador-Noguez D, Brasg IA, Feng XJ, Roquet N, Rabinowitz JD: Metabolome remodeling during the acidogenic-solventogenic transition in Clostridium acetobutylicum. Appl Environ Microbiol 2011, 77:7984-7997.
59. Tusher VG, Tibshirani R, Chu G: Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 2001, 98:5116-5121.