The exometabolome of Clostridium thermocellum reveals overflow metabolism at high cellulose loading

Biotechnology for Biofuels

Volumn 7, Issue 1, 2014, Pages

  Holwerda, Evert K ^a,b   Thorne, Philip G ^c   Olson, Daniel G ^a,b   Amador Noguez, Daniel ^d   Engle, Nancy L ^b,e   Tschaplinski, Timothy J ^b,e   Van Dijken, Johannes P ^f   Lynd, Lee R ^a,b,c  

^a DARTMOUTH COLLEGE   (United States)

^b BioEnergy Science Center   (United States)

^c Mascoma Corporation   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

^e OAK RIDGE NATIONAL LABORATORY   (United States)

^f DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

2,3 butanediol; Amino acids; Cellulose fermentation; Clostridium thermocellum; Fusel alcohols; High solids; Isobutanol

Indexed keywords

AMINO ACIDS; BATCH CELL CULTURE; CELLULOSE; CLOSTRIDIUM; CRYSTALLINE MATERIALS; FERMENTATION; METABOLISM; PHYSIOLOGY;

2 ,3-BUTANEDIOL; CLOSTRIDIUM THERMOCELLUM; FUSEL ALCOHOLS; HIGH-SOLIDS; ISOBUTANOL;

SUBSTRATES;

ALCOHOL; AMINO ACID; BIOFUEL; CELLULOSE; FERMENTATION; METABOLISM; PHYSIOLOGY; THERMOPHILIC BACTERIUM;

AMINO ACIDS; CELLULOSE; CONCENTRATION; FERMENTATION; MICROORGANISMS; PHYSIOLOGY;

CLOSTRIDIUM THERMOCELLUM;

EID: 84988878111     PISSN: 17546834     EISSN: None     Source Type: Journal    
DOI: 10.1186/s13068-014-0155-1     Document Type: Article

References (76)

1. Bayer EA, Belaich JP, Shoham Y, Lamed R: The cellulosomes: multienzyme machines for degradation of plant cell wall polysaccharides. Annu Rev Microbiol 2004, 58:521-554.
2. Demain AL, Newcomb M, Wu JHD: Cellulase, clostridia, and ethanol. Microbiol Mol Biol Rev 2005, 69:124-154.
3. Lynd LR, Van Zyl WH, McBride JE, Laser M: Consolidated bioprocessing of cellulosic biomass: an update. Curr Opin in Biotechnol 2005, 16:577-583.
4. McBee RH: The anaerobic thermophilic cellulolytic bacteria. Bacteriol Rev 1950, 14:51-63.
5. McBee RH: The characteristics of Clostridium thermocellum. J Bacteriol 1954, 67:505-506.
6. Sparling R, Islam R, Cicek N, Carere C, Chow H, Levin DB: Formate synthesis by Clostridium thermocellum during anaerobic fermentation. Can J Microbiol 2006, 52:681-688.
7. Ellis LD, Holwerda EK, Hogsett D, Rogers S, Shao X, Tschaplinski T, Thorne P, Lynd LR: Closing the carbon balance for fermentation by Clostridium thermocellum (ATCC 27405). Bioresource Technol 2012, 103:293-299.
8. van der Veen D, Lo J, Brown SD, Johnson CM, Tschaplinski TJ, Martin M, Engle NL, van den Berg RA, Argyros AD, Caiazza NC, Guss AM, Lynd LR: Characterization of Clostridium thermocellum strains with disrupted fermentation end-product pathways. J Ind Microbiol & Biotechnol 2013, 40:725-734.
9. Zhou J, Olson DG, Argyros DA, Deng Y, Van Gulik WM, Van Dijken JP, Lynd LR: An atypical glycolysis in Clostridium thermocellum. Appl Environ Microbiol 2013, 79:3000-3008.
10. Argyros DA, Tripathi SA, Barrett TF, Rogers SR, Feinberg LF, Olson DG, Foden JM, Miller BB, Lynd LR, Hogsett DA, Caiazza NC: High ethanol titers from cellulose using metabolically engineered thermophilic, anaerobic microbes. Appl Environ Microbiol 2011, 77:8288-8294.
11. Tripathi SA, Olson DG, Argyros DA, Miller BB, Barrett TF, Murphy DM, McCool JD, Warner AK, Rajgarhia VB, Lynd LR, Hogsett DA, Caiazza NC: Development of pyrF-based genetic system for targeted gene deletion in Clostridium thermocellum and creation of a pta mutant. Appl Environ Microbiol 2010, 76:6591-6599.
12. Mohr G, Hong W, Zhang J, Cui G-z, Yang Y, Cui Q, Liu Y-j, Lambowitz AM: A targetron system for gene targeting in thermophiles and its application in Clostridium thermocellum. PLoS One 2013, 8:e69032.
13. Weimer PJ, Zeikus JG: Fermentation of cellulose and cellobiose by Clostridium thermocellum in absence and presence of Methanobacterium thermoautotrophicum. Appl Environ Microbiol 1977, 33:289-297.
14. Garcia-Martinez DV, Shinmyo A, Madia A, Demain AL: Studies on cellulase production by Clostridium thermocellum. Eur J Appl Microbiol Biotechnol 1980, 9:189-197.
15. Johnson EA, Madia A, Demain AL: Chemically defined minimal medium for growth of the anaerobic cellulolytic thermophile Clostridium thermocellum. Appl Environ Microbiol 1981, 41:1060-1062.
16. Saddler JN, Chan MKH: Optimization of Clostridium thermocellum growth on cellulose and pretreated wood substrates. Eur J Appl Microbiol Biotechnol 1982, 16:99-104.
17. Bayer EA, Kenig R, Lamed R: Adherence of Clostridium thermocellum to cellulose. J Bacteriol 1983, 156:818-827.
18. Kurose N, Yagyu J, Miyazaki T, Uchida M, Hanai S, Obayashi A: Evaluation of ethanol productivity from cellulose by Clostridium thermocellum. J Ferm Technol 1986, 64:447-450.
19. Vuillet S, Spinnler HE, Blachere H: Analysis of amino-acid requirements of Clostridium thermocellum. Appl Microbiol Biotechnol 1986, 23:496-498.
20. Lynd LR, Grethlein HE, Wolkin RH: Fermentation of cellulosic substrates in batch and continuous culture by Clostridium thermocellum. Appl Environ Microbiol 1989, 55:3131-3139.
21. Nochur SV, Demain AL, Roberts MF: Carbohydrate utilization by Clostridium thermocellum - importance of internal pH in regulating growth. Enz Microbial Technol 1992, 14:338-349.
22. Strobel HJ: Growth of the thermophilic bacterium Clostridium thermocellum in continuous cultures. Curr Microbiol 1995, 31:210-214.
23. Knutson BL, Strobel HJ, Nokes SE, Dawson KA, Berberich JA, Jones CR: Effect of pressurized solvents on ethanol production by the thermophilic bacterium Clostridium thermocellum. J Supercrit Fluids 1999, 16:149-156.
24. Bothun GD, Knutson BL, Berberich JA, Strobel HJ, Nokes SE: Metabolic selectivity and growth of Clostridium thermocellum in continuous culture under elevated hydrostatic pressure. Appl Microbiol Biotechnol 2004, 65:149-157.
25. Lu YP, Zhang YHP, Lynd LR: Enzyme-microbe synergy during cellulose hydrolysis by Clostridium thermocellum. Proc Natl Acad Sci U S A 2006, 103:16165-16169.
26. Islam R, Cicek N, Sparling R, Levin D: Effect of substrate loading on hydrogen production during anaerobic fermentation by Clostridium thermocellum 27405. Appl Microbiol Biotechnol 2006, 72:576-583.
27. Magnusson L, Islam R, Sparling R, Levin D, Cicek N: Direct hydrogen production from cellulosic waste materials with a single-step dark fermentation process. Internatl J Hydr Ener 2008, 33:5398-5403.
28. Raman B, Pan C, Hurst GB, Rodriguez M Jr, McKeown CK, Lankford PK, Samatova NF, Mielenz JR: Impact of pretreated switchgrass and biomass carbohydrates on Clostridium thermocellum ATCC 27405 cellulosome composition: a quantitative proteomic analysis. PLoS One 2009, 4:e5271.
29. Holwerda EK, Ellis LD, Lynd LR: Development and evaluation of methods to infer biosynthesis and substrate consumption in cultures of cellulolytic microorganisms. Biotechnol Bioeng 2013, 110:2380-2388.
30. Olson DG, Giannone RJ, Hettich RL, Lynd LR: Role of the CipA scaffoldin protein in cellulose solubilization, as determined by targeted gene deletion and complementation in Clostridium thermocellum. JBacteriol2013, 195:733-739.
31. Currie DH, Herring CD, Guss AM, Olson DG, Hogsett DA, Lynd LR: Functional heterologous expression of an engineered full length CipA from Clostridium thermocellum in Thermoanaerobacterium saccharolyticum. Biotechnol Biofuels 2013, 6:32.
32. Tailliez P, Girard H, Millet J, Beguin P: Enhanced cellulose fermentation by an asporogenous and ethanol-tolerant mutant of Clostridium-thermocellum. Appl Environ Microbiol 1989, 55:207-211.
33. Wang DIC, Avgerinos GC, Biocic I, Wang SD, Fang HY: Ethanol from cellulosic biomass. Philos T Soc B 1983, 300:323-333.
34. Hogsett D: Cellulose hydrolysis and fermentation by Clostridium thermocellum for the production of ethanol. PhD thesis. Dartmouth College, Thayer School of Engineering; 1995
35. Viljoen JA, Fred EB, Peterson WH: The fermentation of cellulose by thermophilic bacteria. J Agric Sci 1926, 16:1-17.
36. Freier D, Mothershed CP, Wiegel J: Characterizations of Clostridium thermocellum JW20. Appl Environ Microbiol 1988, 54:204-211.
37. Ng TK, Weimer PJ, Zeikus JG: Cellulolytic and physiological properties of Clostridium thermocellum. Arch Microbiol 1977, 114:1-7.
38. Lamed R, Zeikus JG: Ethanol production by thermophilic bacteria - relationship between fermentation product yields and catabolic enzyme activities in Clostridium thermocellum and Thermoanaerobium brockii. J Bacteriol 1980, 144:569-578.
39. Erbeznik M, Jones CR, Dawson KA, Strobel HJ: Clostridium thermocellum JW20 (ATCC 31549) is a coculture with Thermoanaerobacter ethanolicus. Appl Environ Microbiol 1997, 63:2949-2951.
40. Sato KJ, Goto SG, Yonemura ST, Sekine KJ, Okuma EK, Takagi YS, Honnami KY, Saiki T: Effects of yeast extract and vitamin B-12 on ethanol-production from cellulose by Clostridium thermocellum I-1-B. Appl Environ Microbiol 1992, 58:734-736.
41. Mori Y: Nutritional interdependence between Thermoanaerobacter thermohydrosulfuricus and Clostridium thermocellum. Arch Microbiol 1995, 164:152-154.
42. Ng TK, Benbassat A, Zeikus JG: Ethanol production by thermophilic bacteria - fermentation of cellulosic substrate by cocultures of Clostridium thermocellum and Clostridium thermohydrosulfuricum. Appl Environ Microbiol 1981, 41:1337-1343.
43. He Q, Hemme CL, Jiang H, He Z, Zhou J: Mechanisms of enhanced cellulosic bioethanol fermentation by co-cultivation of Clostridium and Thermoanaerobacter spp. Bioresour Technol 2011, 102:9586-9592.
44. Humbird D, Mohagheghi A, Dowe N, Schell DJ: Economic impact of total solids loading on enzymatic hydrolysis of dilute acid pretreated corn stover. Biotechnol Prog 2010, 26:1245-1251.
45. Prawitwong P, Waeonukul R, Tachaapaikoon C, Pason P, Ratanakhanokchai K, Deng L, Sermsathanaswadi J, Septiningrum K, Mori Y, Kosugi A: Direct glucose production from lignocellulose using Clostridium thermocellum cultures supplemented with a thermostable beta-glucosidase. Biotechn Biofuels 2013, 6:184.
46. Holwerda E, Hirst K, Lynd L: A defined growth medium with very low background carbon for culturing Clostridium thermocellum. J Ind Microbiol Biotechnol 2012, 39:943-947.
47. Stevenson IL: Production of extracellular amino acids by rumen bacteria. Can J Microbiol 1978, 24:1236-1241.
48. Kengen SWM, Stams AJM: Formation of L-alanine as a reduced end-product in carbohydrate fermentation by the hyperthermophilic archaeon Pyrococcus furiosus. Arch Microbiol 1994, 161:168-175.
49. Szech U, Braun M, Kleiner D: Uptake and excretion of amino-acids by saccharolytic clostridia. FEMS Microbiol Lett 1989, 58:11-14.
50. Tempest DW, Meers JL, Brown CM: Influence of environment on content and composition of microbial free amino acid pools. J Gen Microbiol 1970, 64:171-185.
51. Yamamoto K, Murakami R, Takamura Y: Isoprenoid quinone, cellular fatty acid composition and diaminopimelic acid isomers of newly classified thermophilic anaerobic Gram-positive bacteria. FEMS Microbiol Lett 1998, 161:351-358.
52. Baskaran S, Ahn HJ, Lynd LR: Investigation of the ethanol tolerance of Clostridium thermosaccharolyticum in continuous culture. Biotechnol Progr 1995, 11:276-281.
53. Lynd LR, Baskaran S, Casten S: Salt accumulation resulting from base added for pH control, and not ethanol, limits growth of Thermoanaerobacterium thermosaccharolyticum HG-8 at elevated feed xylose concentrations in continuous culture. Biotechnol Progr 2001, 17:118-125.
54. Steiner E, Scott J, Minton NP, Winzer K: An agr quorum sensing system that regulates granulose formation and sporulation in Clostridium acetobutylicum. Appl Environ Microbiol 2012, 78:1113-1122.
55. Burrell PC: The detection of environmental autoinducing peptide quorum-sensing genes from an uncultured Clostridium sp. in landfill leachate reactor biomass. Lett Appl Microbiol 2006, 43:455-460.
56. Wilson CM, Rodriguez M, Johnson CM, Martin SL, Chu TM, Wolfinger RD, Hauser LJ, Land ML, Klingeman DM, Syed MH, Ragauskas AJ, Tschaplinski TJ, Mielenz JR, Brown SD: Global transcriptome analysis of Clostridium thermocellum ATCC 27405 during growth on dilute acid pretreated Populus and switchgrass. Biotechnol Biofuels 2013, 6:18.
57. Latif F, Rajoka MI: Production of ethanol and xylitol from corn cobs by yeasts. Bioresour Technol 2001, 77:57-63.
58. Rao RS, Jyothi CP, Prakasham RS, Sarma PN, Rao LV: Xylitol production from corn fiber and sugarcane bagasse hydrolysates by Candida tropicalis. Bioresour Technol 2006, 97:1974-1978.
59. Airaudo CB, Gaytesorbier A, Armand P: Stability of glutamine and pyroglutamic acid under model system conditions - influence of physical and technological factors. J Food Sci 1987, 52:1750-1752.
60. Snowden MK, Baxter JH, Bergana MM, Reyzer I, Pound V: Stability of N-acetylglutamine and glutamine in aqueous solution and in a liquid nutritional product by an improved HPLC method. J Food Sci 2002, 67:384-389.
61. Park CB, Ryu DDY, Lee SB: Inhibitory effect of L-pyroglutamate on extremophiles: correlation with growth temperature and pH. FEMS Microbiol Lett 2003, 221:187-190.
62. Zhang K, Sawaya MR, Eisenberg DS, Liao JC: Expanding metabolism for biosynthesis of nonnatural alcohols. Proc Natl Acad Sci USA 2008, 105:20653-20658.
63. Higashide W, Li YC, Yang YF, Liao JC: Metabolic engineering of Clostridium cellulolyticum for production of isobutanol from cellulose. Appl Environ Microbiol 2011, 77:2727-2733.
64. Kanehisa M, Goto S: KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 2000, 28:27-30.
65. Xiao ZJ, Wang XM, Huang YL, Huo FF, Zhu XK, Xi LJ, Lu JR: Thermophilic fermentation of acetoin and 2,3-butanediol by a novel Geobacillus strain. Biotechnol Biofuels 2012, 5:11.
66. Celinska E, Grajek W: Biotechnological production of 2,3-butanediol - current state and prospects. Biotechnol Adv 2009, 27:715-725.
67. Siemerink MAJ, Kuit W, Contreras AML, Eggink G, van der Oost J, Kengen SWM: D-2,3-Butanediol production due to heterologous expression of an acetoin reductase in Clostridium acetobutylicum. Appl Environ Microbiol 2011, 77:2582-2588.
68. Yu EKC, Chan MKH, Saddler JN: Butanediol production from lignocellulosic substrates by Klebsiella pneomoniae grown in sequential co-culture with Clostridium thermocellum. Appl Microbiol Biotechnol 1985, 22:399-404.
69. Guedon E, Payot S, Desvaux M, Petitdemange H: Relationships between cellobiose catabolism, enzyme levels, and metabolic intermediates in Clostridium cellulolyticum grown in a synthetic medium. Biotechnol Bioeng 2000, 67:327-335.
70. Desvaux M, Guedon E, Petitdemange H: Cellulose catabolism by Clostridium cellulolyticum growing in batch culture on defined medium. Appl Environ Microbiol 2000, 66:2461-2470.
71. Guedon E, Desvaux M, Petitdemange H: Improvement of cellulolytic properties of Clostridium cellulolyticum by metabolic engineering. Appl Environ Microbiol 2002, 68:53-58.
72. Saddler JN, Chan MKH: Conversion of pretreated lignocellulosic substrate to ethanol by Clostridium thermocellum in mono-culture and co-culture with Clostridium thermosaccharolyticum and Clostridium thermohydrosulphuricum. Can J Microbiol 1984, 30:212-220.
73. Venkateswaran S, Demain AL: The Clostridium thermocellum-Clostridium thermosaccharolyticum ethanol-production process - nutritional studies and scale-down. Chem Eng Commun 1986, 45:53-60.
74. Rouwenhorst RJ, Jzn JF, Scheffers WA, Vandijken JP: Determination of protein concentration by total organic -carbon analysis. J Biochem Bioph Methods 1991, 22:119-128.
75. Li YC, Tschaplinski TJ, Engle NL, Hamilton CY, Rodriguez M, Liao JC, Schadt CW, Guss AM, Yang YF, Graham DE: Combined inactivation of the Clostridium cellulolyticum lactate and malate dehydrogenase genes substantially increases ethanol yield from cellulose and switchgrass fermentations. Biotechnol Biofuels 2012, 5:13.
76. Zhang GF, Mortier KA, Storozhenko S, Van De Steene J, Van Der Straeten D, Lambert WE: Free and total para-aminobenzoic acid analysis in plants with high-performance liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Sp 2005, 19:963-969.