Insights into electron flux through manipulation of fermentation conditions and assessment of protein expression profiles in Clostridium thermocellum

Applied Microbiology and Biotechnology

Volumn 98, Issue 14, 2014, Pages 6497-6510

  Rydzak, Thomas ^a,c   Grigoryan, Marina ^b   Cunningham, Zack J ^a   Krokhin, Oleg V ^b   Ezzati, Peyman ^b   Cicek, Nazim ^a   Levin, David B ^a   Wilkins, John A ^b   Sparling, Richard ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

^c OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

Biofuels; Clostridium thermocellum; Electron flux; Enzyme inhibitors; Hydrogenase; Pyruvate

Indexed keywords

BIOFUELS; CARBON DIOXIDE; CARBON MONOXIDE; CLOSTRIDIUM; ELECTRON TRANSITIONS; FERMENTATION; MASS SPECTROMETRY; METABOLISM; PHYSIOLOGY; REDOX REACTIONS;

CLOSTRIDIUM THERMOCELLUM; ELECTRON FLUX; ENZYME INHIBITORS; HYDROGENASES; PYRUVATES;

PROTEINS;

CARBON DIOXIDE; CARBON MONOXIDE; CELLOBIOSE; FERREDOXIN DEPENDENT HYDROGENASE; FERREDOXIN NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE REDUCTASE; HYDROGEN; HYDROGENASE; LYASE; PYRUVATE SYNTHASE; PYRUVIC ACID; UNCLASSIFIED DRUG; RECOMBINANT PROTEIN;

BACTERIUM; BIOFUEL; BIOTECHNOLOGY; CARBON DIOXIDE; ELECTRON; ENZYME ACTIVITY; ETHANOL; FERMENTATION; GENE EXPRESSION; INHIBITION; PROTEIN;

ARTICLE; BACTERIAL GROWTH; CLOSTRIDIUM THERMOCELLUM; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME INHIBITION; ENZYME SYNTHESIS; FERMENTATION; LIMIT OF DETECTION; MASS SPECTROMETRY; NONHUMAN; OXIDATION REDUCTION REACTION; PROTEIN EXPRESSION; PROTEIN METABOLISM; BIOSYNTHESIS; GENE EXPRESSION; GENETICS; METABOLIC FLUX ANALYSIS; METABOLISM;

CLOSTRIDIUM THERMOCELLUM;

CLOSTRIDIUM THERMOCELLUM; FERMENTATION; GENE EXPRESSION; MASS SPECTROMETRY; METABOLIC FLUX ANALYSIS; METABOLIC NETWORKS AND PATHWAYS; RECOMBINANT PROTEINS;

EID: 84903640402     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-5798-0     Document Type: Article

References (49)

1. Ballongue J, Amine J, Petitdemange E, Gay R (1986) Enhancement of solvents production by Clostridium acetobutylicum cultivated on reducing compounds depletive medium. Biomass 10:121-129
2. Bayer EA, Belaich JP, Shoham Y, Lamed R (2004) The cellulosomes: multienzyme machines for degradation of plant cell wall polysaccharides. Annu Rev Microbiol 58:521-554 (Pubitemid 39551996)
3. Bennett BD, Kimball EH, GaoM, Osterhout R, Van Dien SJ, Rabinowitz JD (2009) Absolute metabolite concentrations and implied enzyme activity site occupancy in Escherichia coli. Nat Chem Biol 5:593-599
4. Biegel E, Schmidt S, González JM, Müller V (2011) Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes. Cell Mol Life Sci 68:613-634
5. Brush EJ, Lipsett KA, Kozarich JW (1988) Inactivation of Escherichia coli pyruvate formate-lyase by hypophosphite: evidence for a rate-limiting phosphorus-hydrogen bond cleavage. Biochemistry 27:2217-2222
6. + translocating ferredoxin oxidation. Biochim Biophys Acta 1827:94-113
7. Calusinska M, Happe T, Joris B, Wilmotte A (2010) The surprising diversity of clostridial hydrogenases: a comparative genomic perspective. Microbiology 156:1575-1588
8. Carere CR, Kalia V, Sparling R, Cicek N, Levin D (2008) Pyruvate catabolism and hydrogen synthesis pathway genes of Clostridium thermocellum ATCC 27405. Indian J Microbiol 48:252-266
9. 2 and ethanol-producing bacteria. BMC Microbiol 12:295
10. Cho H-S, Kim YM, Min BE, Jung GY, Park JM (2011) Improvement of hydrogen production yield by rebalancing NADPH/NADH ratio in a recombinant Escherichia coli. J Nanoelectron Optoelectron 6:1-5
11. Datta R, Zeikus JG (1985) Modulation of acetone-butanol-ethanol fermentation by carbon monoxide and organic acids. Appl Environ Microbiol 49:522-529 (Pubitemid 15138036)
12. De Lacey AL, Stadler C, Fernandez VM, Hatchikian EC, Fan HJ, Li S, Hall MB (2002) IR spectroelectrochemical study of the binding of carbon monoxide to the active site of Desulfovibrio fructosovorans Ni-Fe hydrogenase. J Biol Inorg Chem 7:318-326 (Pubitemid 36056384)
13. Deng Y, Olson DG, Zhou J, Herring CD, Joe Shaw A, Lynd LR (2013) Redirecting carbon flux through exogenous pyruvate kinase to achieve high ethanol yields in Clostridium thermocellum. Metab Eng 15:151-158
14. Desvaux M, Guedon E, Petitdemange H (2001) Kinetics and metabolism of cellulose degradation at high substrate concentrations in steady-state continuous cultures of Clostridium cellulolyticum on a chemically defined medium. Appl Environ Microbiol 67:3837-3845 (Pubitemid 33641668)
15. Fauque G, Peck HD Jr, Moura JJG, Huynh BH, Berlier Y, DerVartanian DV, Teixeira M, Przybyla AE, Lespinat PA, Moura I, LeGall M (1988) The three classes of hydrogenases from sulfate-reducing bacteria of the genus Desulfovibrio. FEMS Microbiol Rev 4:299-344
16. Freier D, Mothershed CP, Wiegel J (1988) Characterization of Clostridium thermocellum JW20. Appl Environ Microbiol 54:204-211
17. Garrett RH (1995) Biochemistry. Saunders College Publishing, New York
18. Guedon E, Payot S, Desvaux M, Petitdemange H (1999) Carbon and electron flow in Clostridium cellulolyticum grown in chemostat culture on synthetic medium. J Bacteriol 181:3262-3269 (Pubitemid 29236935)
19. Hallahan DL, Fernandez VM, Hatchikian EC, Hall DO (1986) Differential inhibition of catalytic sites in Desulfovibrio gigas hydrogenase. Biochimie 68:49-54 (Pubitemid 16126905)
20. Han B, Higgs RE (2008) Proteomics: from hypothesis to quantitative assay on a single platform. Guidelines for developing MRM assays using ion trap mass spectrometers. Brief Funct Genom Proteomics 7:340-354
21. Islam R, Cicek N, Sparling R, Levin D (2006) Effect of substrate loading on hydrogen production during anaerobic fermentation by Clostridium thermocellum 27405. Appl Microbiol Biotechnol 72:576-583 (Pubitemid 44273086)
22. Junelles AM, Janati-Idrissi R, Petitdemange H, Gay R (1987) Effect of pyruvate on glucose metabolism in Clostridium acetobutylicum. Biochimie 69:1183-1190
23. Keshishian H, Addona T, Burgess M, Kuhn E, Carr SA (2007) Quantitative, multiplexed assays for low abundance proteins in plasma by targeted mass spectrometry and stable isotope dilution. Mol Cell Proteomics 6:2212-2229
24. Kim BH, Bellows P, Datta R, Zeikus JG (1984) Control of carbon and electron flow in Clostridium acetobutylicum fermentations: utilization of carbon monoxide to inhibit hydrogen production and to enhance butanol yields. Appl Environ Microbiol 48:764-770 (Pubitemid 14010845)
25. Knappe J, Sawers G (1990) A radical-chemical route to acetyl-CoA: the anaerobically induced pyruvate formate-lyase systemof Escherichia coli. FEMS Microbiol Rev 6:383-398 (Pubitemid 20281612)
26. Kridelbaugh DM, Nelson J, Engle NL, Tschaplinski TJ, Graham DE (2013) Nitrogen and sulfur requirements for Clostridium thermocellum and Caldicellulosiruptor bescii on cellulosic substrates in minimal nutrient media. Bioresour Technol 130:125-135
27. Krokhin OV, Spicer V (2009) Peptide retention standards and hydrophobicity indexes in reversed-phase high-performance liquid chromatography of peptides. Anal Chem 81:9522-9530
28. Lamed R, Zeikus JG (1980) Ethanol production by thermophilic bacteria: relationship between fermentation product yields of and catabolic enzyme activities in Clostridium thermocellum and Thermoanaerobium brockii. J Bacteriol 144:569-578 (Pubitemid 11164174)
29. Lange V, Picotti P, Domon B, Aebersold R (2008) Selected reaction monitoring for quantitative proteomics: a tutorial. Mol Syst Biol 4:222
30. Li HF, Knutson BL, Nokes SE, Lynn BC, Flythe MD (2012a) Metabolic control of Clostridium thermocellum via inhibition of hydrogenase activity and the glucose transport rate. Appl Microbiol Biotechnol 93:1777-1784
31. Li Y, Tschaplinski TJ, Engle NL, Hamilton CY, Rodriguez M, Schadt CW,GussAM,YangY,GrahamDE (2012b) Combined inactivation of the Clostridium cellulolyticum lactate and malate dehydrogenase genes substantially increases ethanol yield from cellulose and switchgrass fermentations. Biotechnol Biofuels 5:2
32. Lynd LR, Grethlein HE (1987) Hydrolysis of dilute acid pretreated mixed hardwood and purified microcrystalline cellulose by cell-free broth from Clostridium thermocellum. Biotechnol Bioeng 29:92-100 (Pubitemid 17059300)
33. Lynd LR, van Zyl WH, McBride JE, Laser M (2005) Consolidated bioprocessing of cellulosic biomass: an update. Curr Opin Biotechnol 16:577-583 (Pubitemid 41393839)
34. Maness P-C, Thammannagowda S (2008) Fermentation and electrohydrogenic approaches to hydrogen production. http://www.hydrogen.energy.gov/pdfs/ progress08/ii-f-6-maness.pdf
35. Moat AG, Foster JW, Spector MP (2002) Microbial physiology, 4th edn. Wiley-Liss Inc, New York
36. Pei J, Zhou G, Jiang Y, Yilin L, Huazhong L, Shao W, Weigel J (2010) Thermoanaerobacter spp. control ethanol pathway via transcriptional regulation and versatility of key enzymes.Metab Eng 12:420-428
37. Raman B, McKeown CK, Rodriguez M Jr, Brown SD, Mielenz JR (2011) Transcriptomic analysis of Clostridium thermocellum ATCC 27405 cellulose fermentation. BMC Microbiol 11:134
38. Rydzak T, Levin DB, Cicek N, Sparling R (2009) Growth phase-dependant enzyme profile of pyruvate catabolism and end-product formation in Clostridium thermocellum ATCC 27405. J Biotechnol 140:169-175
39. Rydzak T, Levin DB, Cicek N, Sparling R (2011) End-product induced metabolic shifts in Clostridium thermocellum ATCC 27405. Appl Microbiol Biotechnol 92:199-209
40. Rydzak T, McQueen PD, Krokhin OV, Spicer V, Ezzati P, Dwivedi RC, Shamshurin D, Levin DB,Wilkins JA, Sparling R (2012) Proteomic analysis of Clostridium thermocellum core metabolism: relative protein expression profiles and growth phase-dependent changes in protein expression. BMC Microbiol 12:214
41. Sander R (1999) Compilation of Henry's law constants for inorganic and organic species of potential importance in environmental chemistry (version 3). Max-Planck Institute of Chemistry, Mainz, Germany
42. Sauer U, Canonaco F, Heri S, Perrenoud A, Fisher E (2004) The soluble and membrane-bound transhydrogenase UdhA and PntAB have divergent functions in NADPH metabolism of Escherichia coli. J Biol Chem 279:6613-6619
43. Schut GJ, Adams MW (2009) The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J Bacteriol 191:4451-4457
44. Sparling R, Islam R, Cicek N, Carere C, Chow H, Levin DB (2006) Formate synthesis by Clostridium thermocellum during anaerobic fermentation. Can J Microbiol 52:681-688 (Pubitemid 44525749)
45. Stevenson DM,Weimer PJ (2005) Expression of 17 genes in Clostridium thermocellum ATCC 27405 during fermentation of cellulose or cellobiose in continuous culture. Appl Environ Microbiol 71:4672-4678 (Pubitemid 41129524)
46. Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100-180 (Pubitemid 8082287)
47. Vasconcelos I, Girbal L, Soucaille P (1994) Regulation of carbon and electron flow in Clostridium acetobutylicum grown in chemostat culture at neutral pH on mixtures of glucose and glycerol. J Bacteriol 176:1443-1450 (Pubitemid 24080062)
48. 2 pathways. Microb Biotechnol 1:382-394
49. Wang S, Huang H, Moll J, Thauer RK (2010) NADP + reduction with reduced ferredoxin and NADP + reduction with NADH are coupled via an electron-bifurcating enzyme complex in Clostridium kluyveri. J Bacteriol 192:5115-5123