Metabolic engineering of clostridia for the production of chemicals

Biofuels, Bioproducts and Biorefining

Volumn 9, Issue 2, 2015, Pages 211-225

  Cho, Changhee ^a   Jang, Yu Sin ^a   Moon, Hyeon Gi ^a   Lee, Joungmin ^a   Lee, Sang Yup ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

Biofuel; Biomass; Butanol; Chemical; Clostridium; Metabolic engineering

Indexed keywords

ACETONE; BIOFUELS; BIOMASS; BUTENES; BUTYRIC ACID; CHEMICALS; CLOSTRIDIUM; INDUSTRIAL CHEMICALS; METABOLISM; SUBSTRATES;

1 ,3 PROPANEDIOL; 2 ,3-BUTANEDIOL; CARBON SOURCE; FUTURE PERSPECTIVES; INDUSTRIAL USE; ISO-PROPANOLS; NATURAL PRODUCTS; RENEWABLE RESOURCE;

METABOLIC ENGINEERING;

EID: 84924710076     PISSN: 1932104X     EISSN: 19321031     Source Type: Journal    
DOI: 10.1002/bbb.1531     Document Type: Article

References (172)

1. Paredes CJ, Alsaker KV and Papoutsakis ET, A comparative genomic view of clostridial sporulation and physiology. Nat Rev Microbiol 3:969-978 (2005).
2. Dürre P, Handbook on Clostridia. Taylor & Francis, London (2005).
3. Montoya D, Arevalo C, Gonzales S, Aristizabal F and Schwarz WH, New solvent-producing Clostridium sp. strains, hydrolyzing a wide range of polysaccharides, are closely related to Clostridium butyricum. J Ind Microbiol Biot 27:329-335 (2001).
4. Tracy BP, Jones SW, Fast AG, Indurthi DC and Papoutsakis ET, Clostridia: The importance of their exceptional substrate and metabolite diversity for biofuel and biorefinery applications. Curr Opin Biotechnol 23:364-381 (2012).
5. Jones DT and Woods DR, Acetone-butanol fermentation revisited. Microbiol Rev 50:484-524 (1986).
6. Nakotte S, Schaffer S, Bohringer M and Durre P, Electroporation of, plasmid isolation from and plasmid conservation in Clostridicum acetobutylicum DSM 792. Appl Microbiol Biot 50:564-567 (1998).
7. Oultram JD, Loughlin M, Swinfield TJ, Brehm JK, Thompson DE and Minton NP, Introduction of plasmids into whole cells of Clostridium acetobutylicum by electroporation. FEMS Microbiol Lett 56:83-88 (1988).
8. Desai RP and Papoutsakis ET, Antisense RNA strategies for metabolic engineering of Clostridium acetobutylicum. Appl Environ Microbiol 65:936-945 (1999).
9. Tummala SB, Welker NE and Papoutsakis ET, Development and characterization of a gene expression reporter system for Clostridium acetobutylicum ATCC 824. Appl Environ Microbiol 65:3793-3799 (1999).
10. Girbal L, Mortier-Barriere I, Raynaud F, Rouanet C, Croux C and Soucaille P, Development of a sensitive gene expression reporter system and an inducible promoter-repressor system for Clostridium acetobutylicum. Appl Environ Microbiol 69:4985-4988 (2003).
11. Hartman AH, Liu H and Melville SB, Construction and characterization of a lactose-inducible promoter system for controlled gene expression in Clostridium perfringens. Appl Environ Microbiol 77:471-478 (2011).
12. Green EM and Bennett GN, Inactivation of an aldehyde/alcohol dehydrogenase gene from Clostridium acetobutylicum ATCC 824. Appl Biochem Biot 57/58:213-221 (1996).
13. Liyanage H, Kashket S, Young M and Kashket ER, Clostridium beijerinckii and Clostridium difficile detoxify methylglyoxal by a novel mechanism involving glycerol dehydrogenase. Appl Environ Microbiol 67:2004-2010 (2001).
14. O'Connor JR, Lyras D, Farrow KA, Adams V, Powell DR, Hinds J et al., Construction and analysis of chromosomal Clostridium difficile mutants. Mol Microbiol 61:1335-1351 (2006).
15. Sillers R, Chow A, Tracy B and Papoutsakis ET, Metabolic engineering of the non-sporulating, non-solventogenic Clostridium acetobutylicum strain M5 to produce butanol without acetone demonstrate the robustness of the acid-formation pathways and the importance of the electron balance. Metab Eng 10:321-332 (2008).
16. Liu X, Zhu Y and Yang ST, Construction and characterization of ack deleted mutant of Clostridium tyrobutyricum for enhanced butyric acid and hydrogen production. Biotechnol Prog 22:1265-1275 (2006).
17. Tracy BP, Jones SW and Papoutsakis ET, Inactivation of sigmaE and sigmaG in Clostridium acetobutylicum illuminates their roles in clostridial-cell-form biogenesis, granulose synthesis, solventogenesis, and spore morphogenesis. JBacteriol 193:1414-1426 (2011).
18. Heap JT, Pennington OJ, Cartman ST, Carter GP and Minton NP, The ClosTron: A universal gene knock-out system for the genus Clostridium. J Microbiol Methods 70:452-464 (2007).
19. Wang Y, Li X, Milne CB, Janssen H, Lin W, Phan G et al., Development of a gene knockout system using mobile group II introns (Targetron) and genetic disruption of acid production pathways in Clostridium beijerinckii. Appl Environ Microbiol 79:5853-5863 (2013).
20. Shao L, Hu S, Yang Y, Gu Y, Chen J, Jiang W et al., Targeted gene disruption by use of a group II intron (targetron) vector in Clostridium acetobutylicum. Cell Res 17:963-965 (2007).
21. Chen Y, McClane BA, Fisher DJ, Rood JI and Gupta P, Construction of an alpha toxin gene knockout mutant of Clostridium perfringens type A by use of a mobile group II intron. Appl Environ Microbiol 71:7542-7547 (2005).
22. Lim JH, Seo SW, Kim SY and Jung GY, Refactoring redox cofactor regeneration for high-yield biocatalysis of glucose to butyric acid in Escherichia coli. Bioresour Technol 135:568-573 (2013).
23. Lehmann D and Lutke-Eversloh T, Switching Clostridium acetobutylicum to an ethanol producer by disruption of the butyrate/butanol fermentative pathway. Metab Eng 13:464-473 (2011).
24. Jang YS, Lee JY, Lee J, Park JH, Im JA, Eom MH et al., Enhanced butanol production obtained by reinforcing the direct butanol-forming route in Clostridium acetobutylicum. mBio 3:e00314-12 (2012).
25. Jang YS, Im JA, Choi SY, Lee JI and Lee SY, Metabolic engineering of Clostridium acetobutylicum for butyric acid production with high butyric acid selectivity. Metab Eng 23:165-174 (2014).
26. 5 alcohols production. Biotechnol J 5:1297-1308 (2010).
27. Peralta-Yahya PP and Keasling JD, Advanced biofuel production in microbes. Biotechnol J 5:147-162 (2010).
28. Lutke-Eversloh T, Application of new metabolic engineering tools for Clostridium acetobutylicum. Appl Microbiol Biot 98:5823-5837 (2014).
29. Thomas L, Joseph A and Gottumukkala LD, Xylanase and cellulase systems of Clostridium sp: An insight on molecular approaches for strain improvement. Bioresour Technol 158:343-350 (2014).
30. Jang YS, Lee J, Malaviya A, Seung DY, Cho JH and Lee SY, Butanol production from renewable biomass: Rediscovery of metabolic pathways and metabolic engineering. Biotechnol J 7:186-198 (2012).
31. Gu Y, Jiang Y, Wu H, Liu X, Li Z, Li J et al., Economical challenges to microbial producers of butanol: Feedstock, butanol ratio and titer. Biotechnol J 6:1348-1357 (2011).
32. Lee SY, Park JH, Jang SH, Nielsen LK, Kim J and Jung KS, Fermentative butanol production by Clostridia. Biotechnol Bioeng 101:209-228 (2008).
33. Durre P, Biobutanol: An attractive biofuel. Biotechnol J 2:1525-1534 (2007).
34. Cooksley CM, Zhang Y, Wang H, Redl S, Winzer K and Minton NP, Targeted mutagenesis of the Clostridium acetobutylicum acetone-butanol-ethanol fermentation pathway. Metab Eng 14:630-641 (2012).
35. Kuit W, Minton NP, Lopez-Contreras AM and Eggink G, Disruption of the acetate kinase (ack) gene of Clostridium acetobutylicum results in delayed acetate production. Appl Microbiol Biot 94:729-741 (2012).
36. Harris LM, Desai RP, Welker NE and Papoutsakis ET, Characterization of recombinant strains of the Clostridium acetobutylicum butyrate kinase inactivation mutant: Need for new phenomenological models for solventogenesis and butanol inhibition? Biotechnol Bioeng 67:1-11 (2000).
37. Lee JY, Jang YS, Lee J, Papoutsakis ET and Lee SY, Metabolic engineering of Clostridium acetobutylicum M5 for highly selective butanol production. Biotechnol J 4:1432-1440 (2009).
38. Hou XH, Peng WF, Xiong L, Huang C, Chen XF, Chen XD et al., Engineering Clostridium acetobutylicum for alcohol production. J Biotechnol 166:25-33 (2013).
39. Ventura JRS, Hu H and Jahng D, Enhanced butanol production in Clostridium acetobutylicum ATCC 824 by double overexpression of 6-phosphofructokinase and pyruvate kinase genes. Appl Microbiol Biot 97:7505-7516 (2013).
40. Yu MR, Zhang YL, Tang IC and Yang ST, Metabolic engineering of Clostridium tyrobutyricum for n-butanol production. Metab Eng 13:373-382 (2011).
41. Yu MR, Du YM, Jiang WY, Chang WL, Yang ST and Tang IC, Effects of different replicons in conjugative plasmids on transformation efficiency, plasmid stability, gene expression and n-butanol biosynthesis in Clostridium tyrobutyricum. Appl Microbiol Biot 93:881-889 (2012).
42. Kopke M, Held C, Hujer S, Liesegang H, Wiezer A, Wollherr A et al., Clostridium ljungdahlii represents a microbial production platform based on syngas. P Natl Acad Sci USA 107:13087-13092 (2010).
43. Bai FW, Anderson WA and Moo-Young M, Ethanol fermentation technologies from sugar and starch feedstocks. Biotechnol Adv 26:89-105 (2008).
44. Krylova AY, Kozyukov EA and Lapidus AL, Ethanol and diesel fuel from plant raw materials: A review. Solid Fuel Chem 42:358-364 (2008).
45. Keis S, Shaheen R and Jones DT, Emended descriptions of Clostridium acetobutylicum and Clostridium beijerinckii, and descriptions of Clostridium saccharoperbutylacetonicum sp. nov. and Clostridium saccharobutylicum sp. nov. Int J Syst Evol Microbiol 51:2095-2103 (2001).
46. Papoutsakis ET, Engineering solventogenic clostridia. Curr Opin Biotechnol 19:420-429 (2008).
47. Sillers R, Al-Hinai MA and Papoutsakis ET, Aldehyde-alcohol dehydrogenase and/or thiolase overexpression coupled with CoA transferase downregulation lead to higher alcohol titers and selectivity in Clostridium acetobutylicum fermentations. Biotechnol Bioeng 102:38-49 (2009).
48. Biswas R, Prabhu S, Lynd LR and Guss AM, Increase in ethanol yield via elimination of lactate production in an ethanol-tolerant mutant of Clostridium thermocellum. PLoS One 9:e86389 (2014).
49. Argyros DA, Tripathi SA, Barrett TF, Rogers SR, Feinberg LF, Olson DG et al., High ethanol titers from cellulose by using metabolically engineered thermophilic, anaerobic microbes. Appl Environ Microbiol 77:8288-8294 (2011).
50. Rassadin VG, Shlygin OY, Likhterova NM, Slavin VN and Zharov AV, Problems in production of high-octane, unleaded automotive gasolines. Chem Technol Fuels Oil 42:235-242 (2006).
51. Lee J, Jang YS, Choi SJ, Im JA, Song H, Cho JH et al., Metabolic engineering of Clostridium acetobutylicum ATCC 824 for isopropanol-butanol-ethanol fermentation. Appl Environ Microbiol 78:1416-1423 (2012).
52. Collas F, Kuit W, Clement B, Marchal R, Lopez-Contreras AM and Monot F, Simultaneous production of isopropanol, butanol, ethanol and 2, 3-butanediol by Clostridium acetobutylicum ATCC 824 engineered strains. AMB Express 2:45 (2012).
53. Dusseaux S, Croux C, Soucaille P and Meynial-Salles I, Metabolic engineering of Clostridium acetobutylicum ATCC 824 for the high-yield production of a biofuel composed of an isopropanol/butanol/ethanol mixture. Metab Eng 18:1-8 (2013).
54. Dai Z, Dong H, Zhu Y, Zhang Y, Li Y and Ma Y, Introducing a single secondary alcohol dehydrogenase into butanol-tolerant Clostridium acetobutylicum Rh8 switches ABE fermentation to high level IBE fermentation. Biotechnol Biofuels 5:44 (2012).
55. Jang YS, Malaviya A and Lee SY, Acetone-butanol-ethanol production with high productivity using Clostridium acetobutylicum BKM19. Biotechnol Bioeng 110:1646-1653 (2013).
56. Jang YS, Malaviya A, Lee J, Im JA, Lee SY, Eom MH et al., Metabolic engineering of Clostridium acetobutylicum for the enhanced production of isopropanol-butanol-ethanol fuel mixture. Biotechnol Prog 29:1083-1088 (2013).
57. Atsumi S, Hanai T and Liao JC, Non-fermentative pathways for synthesis of branched-chain higher alcohols as biofuels. Nature 451:86-89 (2008).
58. Higashide W, Li Y, Yang Y and Liao JC, Metabolic engineering of Clostridium cellulolyticum for production of isobutanol from cellulose. Appl Environ Microbiol 77:2727-2733 (2011).
59. Lay JJ, Lee YJ and Noike T, Feasibility of biological hydrogen production from organic fraction of municipal solid waste. Water Res 33:2579-2586 (1999).
60. Hallenbeck PC, Fermentative hydrogen production: Principles, progress, and prognosis. Int J Hydrogen Energ 34:7379-7389 (2009).
61. Demuez M, Cournac L, Guerrini O, Soucaille P and Girbal L, Complete activity profile of Clostridium acetobutylicum [FeFe]-hydrogenase and kinetic parameters for endogenous redox partners. FEMS Microbiol Lett 275:113-121 (2007).
62. Liu XG, Zhu Y and Yang ST, Butyric acid and hydrogen production by Clostridium tyrobutyricum ATCC 25755 and mutants. Enzyme Microb Technol 38:521-528 (2006).
63. Zhao X, Xing DF, Fu N, Liu BF and Ren NQ, Hydrogen production by the newly isolated Clostridium beijerinckii RZF-1108. Bioresour Technol 102:8432-8436 (2011).
64. Nakayama SI, Kosaka T, Hirakawa H, Matsuura K, Yoshino S and Furukawa K, Metabolic engineering for solvent productivity by downregulation of the hydrogenase gene cluster hupCBA in Clostridium saccharoperbutylacetonicum strain N1-4. Appl Microbiol Biot 78:483-493 (2008).
65. Lin CY and Lay CH, Carbon/nitrogen-ratio effect on fermentative hydrogen production by mixed microflora. Int J Hydrogen Energ 29:41-45 (2004).
66. Hawkes FR, Hussy I, Kyazze G, Dinsdale R and Hawkes DL, Continuous dark fermentative hydrogen production by mesophilic microflora: Principles and progress. Int J Hydrogen Energ 32:172-184 (2007).
67. Morimoto K, Kimura T, Sakka K and Ohmiya K, Overexpression of a hydrogenase gene in Clostridium paraputrificum to enhance hydrogen gas production. FEMS Microbiol Lett 246:229-234 (2005).
68. Klein M, Ansorge-Schumacher MB, Fritsch M and Hartmeier W, Influence of hydrogenase overexpression on hydrogen production of Clostridium acetobutylicum DSM 792. Enzyme Microb Technol 46:384-390 (2010).
69. Cai G, Jin B, Monis P and Saint C, A genetic and metabolic approach to redirection of biochemical pathways of Clostridium butyricum for enhancing hydrogen production. Biotechnol Bioeng 110:338-342 (2013).
70. Liu H, Xu Y, Zheng Z and Liu D, 1, 3-Propanediol and its copolymers: Research, development and industrialization. Biotechnol J 5:1137-1148 (2010).
71. Menzel K, Zeng AP and Deckwer WD, High concentration and productivity of 1, 3-propanediol from continuous fermentation of glycerol by Klebsiella pneumoniae. Enzyme Microb Technol 20:82-86 (1997).
72. Biebl H, Menzel K, Zeng AP and Deckwer WD, Microbial production of 1, 3-propanediol. Appl Microbiol Biot 52: 289-297 (1999).
73. Zeng AP and Biebl H, Bulk chemicals from biotechnology: The case of 1, 3-propanediol production and the new trends. Adv Biochem Eng Biotechnol 74:239-259 (2002).
74. Katrlik J, Vostiar I, Sefcovicova J, Tkac J, Mastihuba V, Valach M et al., A novel microbial biosensor based on cells of Gluconobacter oxydans for the selective determination of 1, 3-propanediol in the presence of glycerol and its application to bioprocess monitoring. Anal Bioanal Chem 388:287-295 (2007).
75. Liu HJ, Zhang DJ, Xu YH, Mu Y, Sun YQ and Xiu ZL, Microbial production of 1, 3-propanediol from glycerol by Klebsiella pneumoniae under micro-aerobic conditions up to a pilot scale. Biotechnol Lett 29:1281-1285 (2007).
76. Sauer M, Marx H and Mattanovich D, Microbial production of 1, 3-propanediol. Recent Pat Biotechnol 2:191-197 (2008).
77. Zhang GL, Ma BB, Xu XL, Li C and Wang LW, Fast conversion of glycerol to 1, 3-propanediol by a new strain of Klebsiella pneumoniae. Biochem Eng J 37:256-260 (2007).
78. Biebl H, Fermentation of glycerol by Clostridium pasteurianum-batch and continuous culture studies. J Ind Microbiol Biot 27:18-26 (2001).
79. Papanikolaou S, Ruiz-Sanchez P, Pariset B, Blanchard F and Fick M, High production of 1, 3-propanediol from industrial glycerol by a newly isolated Clostridium butyricum strain. JBiotechnol 77:191-208 (2000).
80. Barbirato F, Himmi EH, Conte T and Bories A, 1, 3-propanediol production by fermentation: An interesting way to valorize glycerin from the ester and ethanol industries. Ind Crops Prod 7:281-289 (1998).
81. Forsberg CW, Production of 1, 3-propanediol from glycerol by Clostridium acetobutylicum and other Clostridium species. Appl Environ Microbiol 53:639-643 (1987).
82. Otte B, Grunwaldt E, Mahmoud O and Jennewein S, Genome shuffling in Clostridium diolis DSM 15410 for improved 1, 3-propanediol production. Appl Environ Microbiol 75:7610-7616 (2009).
83. Gonzalez-Pajuelo M, Meynial-Salles I, Mendes F, Andrade JC, Vasconcelos I and Soucaille P, Metabolic engineering of Clostridium acetobutylicum for the industrial production of 1, 3-propanediol from glycerol. Metab Eng 7:329-336 (2005).
84. Garg SK and Jain A, Fermentative production of 2, 3-butanediol - a Review. Bioresour Technol 51:103-109 (1995).
85. Syu MJ, Biological production of 2, 3-butanediol. Appl Microbiol Biot 55:10-18 (2001).
86. Celinska E and Grajek W, Biotechnological production of 2, 3-butanediol-Current state and prospects. Biotechnol Adv 27:715-725 (2009).
87. Kopke M, Mihalcea C, Liew FM, Tizard JH, Ali MS, Conolly JJ et al., 2, 3-Butanediol production by acetogenic bacteria, an alternative route to chemical synthesis, using Industrial waste gas. Appl Environ Microbiol 77:5467-5475 (2011).
88. Evans PJ and Wang HY, Enhancement of butanol formation by Clostridium acetobutylicum in the presence of decanol-oleyl alcohol mixed extractants. Appl Environ Microbiol 54:1662-1667 (1988).
89. Raedts J, Siemerink MAJ, Levisson M, van der Oost J and Kengen SWM, Molecular characterization of an NADPH-dependent acetoin reductase/2, 3-butanediol dehydrogenase from Clostridium beijerinckii NCIMB 8052. Appl Environ Microbiol 80:2011-2020 (2014).
90. Siemerink MA, Kuit W, Lopez Contreras AM, Eggink G, van der Oost J and Kengen SW, D-2, 3-butanediol production due to heterologous expression of an acetoin reductase inClostridium acetobutylicum. Appl Environ Microbiol 77:2582-2588 (2011).
91. Sossai P, Butyric acid: What is the future for this old substance? Swiss Med Wkly 142:w13596 (2012).
92. Dwidar M, Park JY, Mitchell RJ and Sang BI, The future of butyric acid in industry. Sci World J 2012:471417 (2012).
93. Zhang C, Yang H, Yang F and Ma Y, Current progress on butyric acid production by fermentation. Curr Microbiol 59:656-663 (2009).
94. Canganella F and Wiegel J, Continuous cultivation of Clostridium thermobutyricum in a rotary fermentor system. JInd Microbiol Biot 24:7-13 (2000).
95. He GQ, Kong Q, Chen QH and Ruan H, Batch and fed-batch production of butyric acid by Clostridium butyricum ZJUCB. JZhejiang Univ Sci B 6:1076-1080 (2005).
96. Hartmanis MG, Butyrate kinase from Clostridium acetobutylicum. J Biol Chem 262:617-621 (1987).
97. Huang KX, Huang S, Rudolph FB and Bennett GN, Identification and characterization of a second butyrate kinase from Clostridium acetobutylicum ATCC 824. J Mol Microbiol Biot 2:33-38 (2000).
98. Lehmann D, Radomski N and Lütke-Eversloh T, New insights into the butyric acid metabolism of Clostridium acetobutylicum. Appl Microbiol Biot 96:1325-1339 (2012).
99. Baek J-M, Mazumdar S, Lee S-W, Jung M-Y, Lim J-H, Seo S-W et al., Butyrate production in engineered Escherichia coli with synthetic scaffolds. Biotechnol Bioeng 110:2790-2794 (2013).
100. Joung S-M, Kurumbang N, Sang B-I and Oh M-K, Effects of carbon source and metabolic engineering on butyrate production in Escherichia coli. Korean J Chem Eng 28:1587-1592 (2011).
101. Saini M, Wang ZW, Chiang CJ and Chao YP, Metabolic engineering of Escherichia coli for production of butyric Acid. J Agric Food Chem 62:4342-4348 (2014).
102. Zhang Y, Yu M and Yang ST, Effects of ptb knockout on butyric acid fermentation by Clostridium tyrobutyricum. Biotechnol Prog 28:52-59 (2012).
103. Vital M, Howe AC and Tiedje JM, Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data. mBio 5:e00889-14 (2014).
104. Jiang L, Zhu L, Xu X, Li Y, Li S and Huang H, Genome sequence of Clostridium tyrobutyricum ATCC 25755, a butyric acid-overproducing strain. Genome Announc 1:e00308-13 (2013).
105. Bassi D, Fontana C, Gazzola S, Pietta E, Puglisi E, Cappa F et al., Draft genome sequence of Clostridium tyrobutyricum strain UC7086, isolated from grana padano cheese with late-blowing defect. Genome Announc 1:e00614-13 (2013).
106. Zhu Y, Liu XG and Yang ST, Construction and characterization of pta gene-deleted mutant of Clostridium tyrobutyricum for enhanced butyric acid fermentation. Biotechnol Bioeng 90:154-166 (2005).
107. Jang YS, Woo HM, Im JA, Kim IH and Lee SY, Metabolic engineering of Clostridium acetobutylicum for enhanced production of butyric acid. Appl Microbiol Biot 97:9355-9363 (2013).
108. Clark SW, Bennett GN and Rudolph FB, Isolation and characterization of mutants of Clostridium acetobutylicum ATCC 824 deficient in acetoacetyl-coenzyme A:acetate/butyrate:coenzyme A-transferase (EC 2.8.3.9) and in other solvent pathway enzymes. Appl Environ Microbiol 55:970-976 (1989).
109. Nolling J, Breton G, Omelchenko MV, Makarova KS, Zeng Q, Gibson R et al., Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J Bacteriol 183:4823-4838 (2001).
110. Ueki T, Nevin KP, Woodard TL and Lovley DR, Converting carbon dioxide to butyrate with an engineered strain of Clostridium ljungdahlii. mBio 5:e01636-14 (2014).
111. Lee JW, Na D, Park JM, Lee J, Choi S and Lee SY, Systems metabolic engineering of microorganisms for natural and non-natural chemicals. Nat Chem Biol 8:536-546 (2012).
112. Lee SY, Lee DY and Kim TY, Systems biotechnology for strain improvement. Trends Biotechnol 23:349-358 (2005).
113. Anbarasan P, Baer ZC, Sreekumar S, Gross E, Binder JB, Blanch HW et al., Integration of chemical catalysis with extractive fermentation to produce fuels. Nature 491:235-239 (2012).
114. Sreekumar S, Baer ZC, Gross E, Padmanaban S, Goulas K, Gunbas G et al., Chemocatalytic upgrading of tailored fermentation products toward biodiesel. ChemSusChem 7:2445-2448 (2014).
115. Bormann S, Baer ZC, Sreekumar S, Kuchenreuther JM, Dean Toste F, Blanch HW et al., Engineering Clostridium acetobutylicum for production of kerosene and diesel blendstock precursors. Metab Eng 25:124-130 (2014).
116. Seedorf H, Fricke WF, Veith B, Bruggemann H, Liesegang H, Strittmatter A et al., The genome of Clostridium kluyveri, a strict anaerobe with unique metabolic features. P Natl Acad Sci USA 105:2128-2133 (2008).
117. Feinberg L, Foden J, Barrett T, Davenport KW, Bruce D, Detter C et al., Complete genome sequence of the cellulolytic thermophile Clostridium thermocellum DSM1313. J Bacteriol 193:2906-2907 (2011).
118. Yokoyama S, Oshima K, Nomura I, Hattori M and Suzuki T, Complete genomic sequence of the O-desmethylangolensin-producing bacterium Clostridium rRNA cluster XIVa strain SY8519, isolated from adult human intestine. J Bacteriol 193:5568-5569 (2011).
119. Bao G, Wang R, Zhu Y, Dong H, Mao S, Zhang Y et al., Complete genome sequence of Clostridium acetobutylicum DSM 1731, a solvent-producing strain with multireplicon genome architecture. J Bacteriol 193:5007-5008 (2011).
120. Hu S, Zheng H, Gu Y, Zhao J, Zhang W, Yang Y et al., Comparative genomic and transcriptomic analysis revealed genetic characteristics related to solvent formation and xylose utilization in Clostridium acetobutylicum EA 2018. BMC Genomics 12:93 (2011).
121. Li LL, Taghavi S, Izquierdo JA and van der Lelie D, Complete genome sequence of Clostridium sp. strain BNL1100, a cellulolytic mesophile isolated from corn stover. J Bacteriol 194:6982-6983 (2012).
122. Hartwich K, Poehlein A and Daniel R, The purine-utilizing bacterium Clostridium acidurici 9a: A genome-guided metabolic reconsideration. PLoS One 7:e51662 (2012).
123. Wang Y, Li X, Mao Y and Blaschek HP, Genome-wide dynamic transcriptional profiling in Clostridium beijerinckii NCIMB 8052 using single-nucleotide resolution RNA-Seq. BMC Genomics 13:102 (2012).
124. Senger RS and Papoutsakis ET, Genome-scale model for Clostridium acetobutylicum: Part I. Metabolic network resolution and analysis. Biotechnol Bioeng 101:1036-1052 (2008).
125. Senger RS and Papoutsakis ET, Genome-scale model for Clostridium acetobutylicum: Part II. Development of specific proton flux states and numerically determined sub-systems. Biotechnol Bioeng 101:1053-1071 (2008).
126. Lee J, Yun H, Feist AM, Palsson BO and Lee SY, Genome-scale reconstruction and in silico analysis of the Clostridium acetobutylicum ATCC 824 metabolic network. Appl Microbiol Biot 80:849-862 (2008).
127. Roberts SB, Gowen CM, Brooks JP and Fong SS, Genome-scale metabolic analysis of Clostridium thermocellum for bioethanol production. BMC Syst Biol 4:31 (2010).
128. Salimi F, Zhuang K and Mahadevan R, Genome-scale metabolic modeling of a clostridial co-culture for consolidated bioprocessing. Biotechnol J 5:726-738 (2010).
129. Milne CB, Eddy JA, Raju R, Ardekani S, Kim PJ, Senger RS et al., Metabolic network reconstruction and genome-scale model of butanol-producing strain Clostridium beijerinckii NCIMB 8052. BMC Syst Biol 5:130 (2011).
130. Nagarajan H, Sahin M, Nogales J, Latif H, Lovley DR, Ebrahim A et al., Characterizing acetogenic metabolism using a genome-scale metabolic reconstruction of Clostridium ljungdahlii. Microb Cell Fact 12:118 (2013).
131. Gorwa MF, Croux C and Soucaille P, Molecular characterization and transcriptional analysis of the putative hydrogenase gene of Clostridium acetobutylicum ATCC 824. J Bacteriol 178:2668-2675 (1996).
132. Fontaine L, Meynial-Salles I, Girbal L, Yang X, Croux C and Soucaille P, Molecular characterization and transcriptional analysis of adhE2, the gene encoding the NADH-dependent aldehyde/alcohol dehydrogenase responsible for butanol production in alcohologenic cultures of Clostridium acetobutylicum ATCC 824. J Bacteriol 184:821-830 (2002).
133. Tummala SB, Junne SG, Paredes CJ and Papoutsakis ET, Transcriptional analysis of product-concentration driven changes in cellular programs of recombinant Clostridium acetobutylicum strains. Biotechnol Bioeng 84:842-854 (2003).
134. Tomas CA, Alsaker KV, Bonarius HP, Hendriksen WT, Yang H, Beamish JA et al., DNA array-based transcriptional analysis of asporogenous, nonsolventogenic Clostridium acetobutylicum strains SKO1 and M5. J Bacteriol 185:4539-4547 (2003).
135. Alsaker KV, Spitzer TR and Papoutsakis ET, Transcriptional analysis of spo0A overexpression in Clostridium acetobutylicum and its effect on the cell's response to butanol stress. JBacteriol 186:1959-1971 (2004).
136. Tomas CA, Beamish J and Papoutsakis ET, Transcriptional analysis of butanol stress and tolerance in Clostridium acetobutylicum. J Bacteriol 186:2006-2018 (2004).
137. Maamar H, Abdou L, Boileau C, Valette O and Tardif C, Transcriptional analysis of the cip-cel gene cluster from Clostridium cellulolyticum. J Bacteriol 188:2614-2624 (2006).
138. Shi Z and Blaschek HP, Transcriptional analysis of Clostridium beijerinckii NCIMB 8052 and the hyper-butanol-producing mutant BA101 during the shift from acidogenesis to solventogenesis. Appl Environ Microbiol 74:7709-7714 (2008).
139. Grimmler C, Held C, Liebl W and Ehrenreich A, Transcriptional analysis of catabolite repression in Clostridium acetobutylicum growing on mixtures of D-glucose and D-xylose. J Biotechnol 150:315-323 (2010).
140. Servinsky MD, Kiel JT, Dupuy NF and Sund CJ, Transcriptional analysis of differential carbohydrate utilization by Clostridium acetobutylicum. Microbiology 156:3478-3491 (2010).
141. Janssen H, Doring C, Ehrenreich A, Voigt B, Hecker M, Bahl H et al., A proteomic and transcriptional view of acidogenic and solventogenic steady-state cells of Clostridium acetobutylicum in a chemostat culture. Appl Microbiol Biot 87:2209-2226 (2010).
142. Wang Y, Li X, Mao Y and Blaschek HP, Single-nucleotide resolution analysis of the transcriptome structure of Clostridium beijerinckii NCIMB 8052 using RNA-Seq. BMC Genomics 12:479 (2011).
143. Janssen H, Grimmler C, Ehrenreich A, Bahl H and Fischer RJ, A transcriptional study of acidogenic chemostat cells of Clostridium acetobutylicum-solvent stress caused by a transient n-butanol pulse. J Biotechnol 161:354-365 (2012).
144. Schwarz KM, Kuit W, Grimmler C, Ehrenreich A and Kengen SW, A transcriptional study of acidogenic chemostat cells of Clostridium acetobutylicum-cellular behavior in adaptation to n-butanol. J Biotechnol 161:366-377 (2012).
145. Honicke D, Janssen H, Grimmler C, Ehrenreich A and Lutke-Eversloh T, Global transcriptional changes of Clostridium acetobutylicum cultures with increased butanol:acetone ratios. N Biotechnol 29:485-493 (2012).
146. Vasileva D, Janssen H, Honicke D, Ehrenreich A and Bahl H, Effect of iron limitation and fur gene inactivation on the transcriptional profile of the strict anaerobe Clostridium acetobutylicum. Microbiology 158:1918-1929 (2012).
147. Venkataramanan KP, Jones SW, McCormick KP, Kunjeti SG, Ralston MT, Meyers BC et al., The Clostridium small RNome that responds to stress: The paradigm and importance of toxic metabolite stress in Clostridium acetobutylicum. BMC Genomics 14:849 (2013).
148. Wang Y, Li X and Blaschek HP, Effects of supplementary butyrate on butanol production and the metabolic switch in Clostridium beijerinckii NCIMB 8052: Genome-wide transcriptional analysis with RNA-Seq. Biotechnol Biofuels 6:138 (2013).
149. Xu C, Huang R, Teng L, Wang D, Hemme CL, Borovok I etal., Structure and regulation of the cellulose degradome in Clostridium cellulolyticum. Biotechnol Biofuels 6:73 (2013).
150. Zhang Y and Ezeji TC, Transcriptional analysis of Clostridium beijerinckii NCIMB 8052 to elucidate role of furfural stress during acetone butanol ethanol fermentation. Biotechnol Biofuels 6:66 (2013).
151. Wei H, Fu Y, Magnusson L, Baker JO, Maness PC, Xu Q etal., Comparison of transcriptional profiles of Clostridium thermocellum grown on cellobiose and pretreated yellow poplar using RNA-Seq. Front Microbiol 5:142 (2014).
152. Schaffer S, Isci N, Zickner B and Durre P, Changes in protein synthesis and identification of proteins specifically induced during solventogenesis in Clostridium acetobutylicum. Electrophoresis 23:110-121 (2002).
153. Sullivan L and Bennett GN, Proteome analysis and comparison of Clostridium acetobutylicum ATCC 824 and Spo0A strain variants. J Ind Microbiol Biot 33:298-308 (2006).
154. Williams TI, Combs JC, Lynn BC and Strobel HJ, Proteomic profile changes in membranes of ethanol-tolerant Clostridium thermocellum. Appl Microbiol Biot 74:422-432 (2007).
155. Gold ND and Martin VJ, Global view of the Clostridium thermocellum cellulosome revealed by quantitative proteomic analysis. J Bacteriol 189:6787-6795 (2007).
156. Raman B, Pan C, Hurst GB, Rodriguez M, Jr., McKeown CK, Lankford PK et al., Impact of pretreated Switchgrass and biomass carbohydrates on Clostridium thermocellum ATCC 27405 cellulosome composition: A quantitative proteomic analysis. PLoS One 4:e5271 (2009).
157. Blouzard JC, Coutinho PM, Fierobe HP, Henrissat B, Lignon S, Tardif C et al., Modulation of cellulosome composition in Clostridium cellulolyticum: Adaptation to the polysaccharide environment revealed by proteomic and carbohydrate-active enzyme analyses. Proteomics 10:541-554 (2010).
158. Mao S, Luo Y, Zhang T, Li J, Bao G, Zhu Y et al., Proteome reference map and comparative proteomic analysis between a wild type Clostridium acetobutylicum DSM 1731 and its mutant with enhanced butanol tolerance and butanol yield. JProteome Res 9:3046-3061 (2010).
159. Tolonen AC, Haas W, Chilaka AC, Aach J, Gygi SP and Church GM, Proteome-wide systems analysis of a cellulosic biofuel-producing microbe. Mol Syst Biol 7:461 (2011).
160. Mao S, Luo Y, Bao G, Zhang Y, Li Y and Ma Y, Comparative analysis on the membrane proteome of Clostridium acetobutylicum wild type strain and its butanol-tolerant mutant. Mol Biosyst 7:1660-1677 (2011).
161. Sivagnanam K, Raghavan VG, Shah M, Hettich RL, Verberkmoes NC and Lefsrud MG, Comparative shotgun proteomic analysis of Clostridium acetobutylicum from butanol fermentation using glucose and xylose. Proteome Sci 9:66 (2011).
162. Rydzak T, McQueen PD, Krokhin OV, Spicer V, Ezzati P, Dwivedi RC et al., Proteomic analysis of Clostridium thermocellum core metabolism: Relative protein expression profiles and growth phase-dependent changes in protein expression. BMC Microbiol 12:214 (2012).
163. Yu T, Xu X, Peng Y, Luo Y and Yang K, Cell wall proteome of Clostridium thermocellum and detection of glycoproteins. Microbiol Res 167:364-371 (2012).
164. Bai X and Ji Z, Phosphoproteomic investigation of a solvent producing bacterium Clostridium acetobutylicum. Appl Microbiol Biot 95:201-211 (2012).
165. Burton E and Martin VJ, Proteomic analysis of Clostridium thermocellum ATCC 27405 reveals the upregulation of an alternative transhydrogenase-malate pathway and nitrogen assimilation in cells grown on cellulose. Can J Microbiol 58:1378-1388 (2012).
166. Morisaka H, Matsui K, Tatsukami Y, Kuroda K, Miyake H, Tamaru Y et al., Profile of native cellulosomal proteins of Clostridium cellulovorans adapted to various carbon sources. AMB Express 2:37 (2012).
167. Yang S, Giannone RJ, Dice L, Yang ZK, Engle NL, Tschaplinski TJ et al., Clostridium thermocellum ATCC27405 transcriptomic, metabolomic and proteomic profiles after ethanol stress. BMC Genomics 13:336 (2012).
168. Han B, Ujor V, Lai LB, Gopalan V and Ezeji TC, Use of proteomic analysis to elucidate the role of calcium in acetone-butanol-ethanol fermentation by Clostridium beijerinckii NCIMB 8052. Appl Environ Microbiol 79:282-293 (2013).
169. Hou S, Jones SW, Choe LH, Papoutsakis ET and Lee KH, Workflow for quantitative proteomic analysis of Clostridium acetobutylicum ATCC 824 using iTRAQ tags. Methods 61:269-276 (2013).
170. Matsui K, Bae J, Esaka K, Morisaka H, Kuroda K and Ueda M, Exoproteome profiles of Clostridium cellulovorans grownon various carbon sources. Appl Environ Microbiol 79:6576-6584 (2013).
171. Jang YS, Han MJ, Lee J, Im JA, Lee YH, Papoutsakis ET et al., Proteomic analyses of the phase transition from acidogenesis to solventogenesis using solventogenic and non-solventogenic Clostridium acetobutylicum strains. Appl Microbiol Biot 98:5105-5115 (2014).
172. Papoutsakis ET, Equations and calculations for fermentations of butyric acid bacteria. Biotechnol Bioeng 26:174-187 (1984).