Skip to main content

Glycolysis as the Central Core of Fermentation

  • Chapter
  • First Online:
Book cover Anaerobes in Biotechnology

Part of the book series: Advances in Biochemical Engineering/Biotechnology ((ABE,volume 156))

Abstract

The increasing concerns of greenhouse gas emissions have increased the interest in dark fermentation as a means of productions for industrial chemicals, especially from renewable cellulosic biomass. However, the metabolism, including glycolysis, of many candidate organisms for cellulosic biomass conversion through consolidated bioprocessing is still poorly understood and the genomes have only recently been sequenced. Because a variety of industrial chemicals are produced directly from sugar metabolism, the careful understanding of glycolysis from a genomic and biochemical point of view is essential in the development of strategies for increasing product yields and therefore increasing industrial potential. The current review discusses the different pathways available for glycolysis along with unexpected variations from traditional models, especially in the utilization of alternate energy intermediates (GTP, pyrophosphate). This reinforces the need for a careful description of interactions between energy metabolites and glycolysis enzymes for understanding carbon and electron flux regulation.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

ABE:

Acetone–Butanol–Ethanol process

ADP:

Adenosine diphosphate

ATP:

Adenosine triphosphate

ED:

Entner–Doudoroff pathway

EMP:

Embden–Meyerhof–Parnas pathway

GTP:

Guanosine triphosphate

NADH:

Nicotinamide adenine dinucleotide

NADPH:

Nicotinamide adenine dinucleotide phosphate

PPi:

Pyrophosphate

PPP:

Pentose phosphate pathway

TCA:

Tricarboxylic acid cycle

References

  1. McGovern PE, Zhang J, Tang J, Zhang Z, Hall GR, Moreau RA, Nuñez A, Butrym ED, Richards MP, Wang C-S, Cheng G, Zhao Z, Wang C (2004) Fermented beverages of pre- and proto-historic China. Proc Natl Acad Sci USA 101:17593–17598

    Google Scholar 

  2. Rogers P, Chen J, Zidwick MJO (2013) Organic acid and solvent production. Part I: acetic, lactic, gluconic, succinic and polyhydroxyalkanoic acids. Prokaryotes 511–755

    Google Scholar 

  3. Ross D (1961) The acetone-butanol fermentation. Prog Ind Microbiol 3:71–90

    CAS  Google Scholar 

  4. Jones DT, Woods DR (1986) Acetone-butanol fermentation revisited. Microbiol Rev 50:484–524

    CAS  Google Scholar 

  5. Gabriel CL (1928) Butanol fermentation process 1. Ind Eng Chem 20:1063–1067

    Article  CAS  Google Scholar 

  6. Gottschalk G (1986) Bacterial metabolism, 2nd edn. Springer-Verlag, New York

    Book  Google Scholar 

  7. Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180

    CAS  Google Scholar 

  8. Häggström L (1985) Acetone-butanol fermentation and its variants. Biotechnol Adv 3:13–28

    Article  Google Scholar 

  9. Demain AL, Newcomb M, Wu JHD (2005) Cellulase, clostridia, and ethanol. Microbiol Mol Biol Rev 69:124–154

    Article  CAS  Google Scholar 

  10. Bao G, Dong H, Zhu Y, Mao S, Zhang T, Zhang Y, Chen Z, Li Y (2014) Comparative genomic and proteomic analyses of Clostridium acetobutylicum Rh8 and its parent strain DSM 1731 revealed new understandings on butanol tolerance. Biochem Biophys Res Commun 450:1612–1618

    Article  CAS  Google Scholar 

  11. Linville JL, Rodriguez M, Land M, Syed MH, Engle NL, Tschaplinski TJ, Mielenz JR, Cox CD (2013) Industrial robustness: understanding the mechanism of tolerance for the Populus hydrolysate-tolerant mutant strain of Clostridium thermocellum. PLoS One 8:1–16

    Article  CAS  Google Scholar 

  12. Olson DG, Sparling R, Lynd LR (2015) Ethanol production by engineered thermophiles. Curr Opin Biotechnol 33:130–141

    Article  CAS  Google Scholar 

  13. McKendry P (2002) Energy production from biomass (part 1): overview of biomass. Bioresour Technol 83:37–46

    Article  CAS  Google Scholar 

  14. Hamelinck CN, Van Hooijdonk G, Faaij APC (2005) Ethanol from lignocellulosic biomass: techno-economic performance in short-, middle- and long-term. Biomass Bioenergy 28:384–410

    Article  CAS  Google Scholar 

  15. Carroll A, Somerville CR (2009) Cellulosic biofuels. Annu Rev Plant Biol 60:165–82

    Article  CAS  Google Scholar 

  16. Lynd LR (1996) Overview and evaluation of fuel ethanol from cellulosic biomass: technology, economics, the environment, and policy. Annu Rev Energy Environ 21:403–465

    Article  Google Scholar 

  17. Hethener P, Brauman A, Garcia J-L (1992) Clostridium termitidis sp. nov., a cellulolytic bacterium from the gut of the wood-feeding termite, Nasutitermes lujae. Syst Appl Microbiol 15:52–58

    Article  CAS  Google Scholar 

  18. Ren Z, Ward TE, Logan BE, Regan JM (2007) Characterization of the cellulolytic and hydrogen-producing activities of six mesophilic Clostridium species. J Appl Microbiol 103:2258–2266

    Article  CAS  Google Scholar 

  19. Schellenberg JJ, Verbeke TJ, McQueen P, Krokhin OV, Zhang X, Alvare G, Fristensky B, Thallinger GG, Henrissat B, Wilkins JA, Levin DB, Sparling R (2014) Enhanced whole genome sequence and annotation of Clostridium stercorarium DSM8532T using RNA-seq transcriptomics and high-throughput proteomics. BMC Genomics 15:567

    Article  CAS  Google Scholar 

  20. Phillips JR, Klasson KT, Clausen EC, Gaddy JL (1993) Biological production of ethanol from coal synthesis gas. Appl Biochem Biotechnol 39–40:559–571

    Article  Google Scholar 

  21. Yu M, Zhang Y, Tang IC, Yang ST (2011) Metabolic engineering of Clostridium tyrobutyricum for n-butanol production. Metab Eng 13:373–382

    Article  CAS  Google Scholar 

  22. Bellido C, Infante C, Coca M, González-Benito G, García-Cubero MT (2015) Efficient acetone-butanol-ethanol production by Clostridium beijerinckii from sugar beet pulp. Bioresour Technol 190:332–338

    Article  CAS  Google Scholar 

  23. Warnick TA, Methé BA, Leschine SB (2002) Clostridium phytofermentans sp. nov., a cellulolytic mesophile from forest soil. Int J Syst Evol Microbiol 52:1155–1160

    Article  CAS  Google Scholar 

  24. Wiegel J, Ljungdahl LG (1981) Thermoanaerobacter ethanolicus gen. nov., spec. nov., a new, extreme thermophilic, anaerobic bacterium. Arch Microbiol 128:343–348

    Article  CAS  Google Scholar 

  25. Hemme CL, Fields MW, He Q, Deng Y, Lin L, Tu Q, Mouttaki H, Zhou A, Feng X, Zuo Z, Ramsay BD, He Z, Wu L, Van Nostrand J, Xu J, Tang YJ, Wiegel J, Phelps TJ, Zhou J (2011) Correlation of genomic and physiological traits of Thermoanaerobacter species with biofuel yields. Appl Environ Microbiol 77:7998–8008

    Article  CAS  Google Scholar 

  26. Shaw AJ, Jenney FE, Adams MWW, Lynd LR (2008) End-product pathways in the xylose fermenting bacterium, Thermoanaerobacterium saccharolyticum. Enzyme Microb Technol 42:453–458

    Article  CAS  Google Scholar 

  27. Bhandiwad A, Shaw AJ, Guss A, Guseva A, Bahl H, Lynd LR (2014) Metabolic engineering of Thermoanaerobacterium saccharolyticum for n-butanol production. Metab Eng 21:17–25

    Article  CAS  Google Scholar 

  28. Chung D, Cha M, Guss AM, Westpheling J (2014) Direct conversion of plant biomass to ethanol by engineered Caldicellulosiruptor bescii. Proc Natl Acad Sci USA 111:8931–6

    Article  CAS  Google Scholar 

  29. Bielen AAM, Verhaart MRA (2013) Biohydrogen production by the thermophilic bacterium Caldicellulosiruptor saccharolyticus: current status and perspectives. Life 3:52–85

    Article  CAS  Google Scholar 

  30. 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

    CAS  Google Scholar 

  31. Tracy BP, Jones SW, Fast AG, Indurthi DC, Papoutsakis ET (2012) Clostridia: the importance of their exceptional substrate and metabolite diversity for biofuel and biorefinery applications. Curr Opin Biotechnol 23:364–381

    Article  CAS  Google Scholar 

  32. Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66:506–577

    Article  CAS  Google Scholar 

  33. Lynd LR, Van Zyl WH, McBride JE, Laser M (2005) Consolidated bioprocessing of cellulosic biomass: an update. Curr Opin Biotechnol 16:577–583

    Article  CAS  Google Scholar 

  34. Stouthamer AH (1973) A theoretical study on the amount of ATP required for synthesis of microbial cell material. Antonie Van Leeuwenhoek 39:545–565

    Article  CAS  Google Scholar 

  35. Schneider DA, Gourse RL (2004) Relationship between growth rate and ATP concentration in Escherichia coli: a bioassay for available cellular ATP. J Biol Chem 279:8262–8268

    Article  CAS  Google Scholar 

  36. Prescott LM, Harley JP, Klein DA (2005) Microbiology. McGraw-Hill, New York

    Google Scholar 

  37. Entner N, Doudoroff M (1952) Glucose and gluconic acid oxidation of Pseudomonas saccharophila. J Biol Chem 196:853–862

    CAS  Google Scholar 

  38. Conway T (1992) The Entner–Doudoroff pathway: history, physiology and molecular biology. FEMS Microbiol Rev 9:1–27

    Article  CAS  Google Scholar 

  39. Barker BTP, Hillier VF (1912) Cider sickness. J Agric Sci 5(01):68–85

    Article  Google Scholar 

  40. Swings J, De Ley J (1977) The biology of Zymomonas. Bacteriol Rev 41:1–46

    CAS  Google Scholar 

  41. Andreesen JR, Gottschalk G (1969) The occurrence of a modified Entner–Doudoroff pathway in Clostridium aceticum. Arch Microbiol 69:160–170

    CAS  Google Scholar 

  42. Romano AH, Conway T (1996) Evolution of carbohydrate metabolic pathways. Res Microbiol 147:448–455

    Article  CAS  Google Scholar 

  43. Bender R, Andreesen JR, Gottschalk G (1971) 2-Keto-3-deoxygluconate, an intermediate in the fermentation of gluconate by Clostridia. J Bacteriol 107:570–573

    CAS  Google Scholar 

  44. Ahmed H, Ettema TJG, Tjaden B, Geerling ACM, van der Oost J, Siebers B (2005) The semi-phosphorylative Entner–Doudoroff pathway in hyperthermophilic archaea: a re-evaluation. Biochem J 390:529–540

    Article  CAS  Google Scholar 

  45. Boyle J (2005) In: Nelson D, Cox M (eds) Lehninger principles of biochemistry, 4th edn. Biochem Mol Biol Educ 33:74–75

    Google Scholar 

  46. Ronimus RS, Morgan HW (2003) Distribution and phylogenies of enzymes of the Embden–Meyerhof–Parnas pathway from archaea and hyperthermophilic bacteria support a gluconeogenic origin of metabolism. Archaea 1:199–221

    Article  CAS  Google Scholar 

  47. Cárdenas ML, Cornish-Bowden A, Ureta T (1998) Evolution and regulatory role of the hexokinases. Biochim Biophys Acta Mol Cell Res 1401:242–264

    Article  Google Scholar 

  48. Ito S, Fushinobu S, Yoshioka I, Koga S, Matsuzawa H, Wakagi T (2001) Structural basis for the ADP-specificity of a novel glucokinase from a hyperthermophilic archaeon. Structure 9:205–214

    Article  CAS  Google Scholar 

  49. Labes A, Schonheit P (2003) ADP-dependent glucokinase from the hyperthermophilic sulfate-reducing archaeon Archaeoglobus fulgidus strain 7324. Arch Microbiol 180:69–75

    Article  CAS  Google Scholar 

  50. Holwerda EK (2014) The exometabolome of Clostridium thermocellum reveals overflow metabolism at high cellulose loading. Biothechnol Biofuels 7:1–11

    Article  CAS  Google Scholar 

  51. Phillips NF, Horn PJ, Wood HG (1993) The polyphosphate- and ATP-dependent glucokinase from Propionibacterium shermanii: both activities are catalyzed by the same protein. Arch Biochem Biophys 300:309–319

    Article  CAS  Google Scholar 

  52. Hsieh PC, Kowalczyk TH, Phillips NFB (1996) Kinetic mechanisms of polyphosphate glucokinase from Mycobacterium tuberculosis. Biochemistry 35:9772–9781

    Article  CAS  Google Scholar 

  53. Anderson CM, Stenkamp RE, Steitz TA (1978) Sequencing a protein by X-ray crystallography. J Mol Biol 123:15–33

    Article  CAS  Google Scholar 

  54. Rosano C, Sabini E, Rizzi M, Deriu D, Murshudov G, Bianchi M, Serafini G, Magnani M, Bolognesi M (1999) Binding of non-catalytic ATP to human hexokinase I highlights the structural components for enzyme-membrane association control. Structure 7:1427–1437

    Article  CAS  Google Scholar 

  55. Aleshin AE, Zeng C, Bartunik HD, Fromm HJ, Honzatko RB (1998) Regulation of hexokinase I: crystal structure of recombinant human brain hexokinase complexed with glucose and phosphate. J Mol Biol 282:345–357

    Article  CAS  Google Scholar 

  56. Koga S, Yoshioka I, Sakuraba H, Takahashi M, Sakasegawa S, Shimizu S, Ohshima T (2000) Biochemical characterization, cloning, and sequencing of ADP-dependent (AMP-forming) glucokinase from two hyperthermophilic archaea, Pyrococcus furiosus and Thermococcus litoralis. J Biochem 128:1079–1085

    Article  CAS  Google Scholar 

  57. Dörr C, Zaparty M, Tjaden B, Brinkmann H, Siebers B (2003) The hexokinase of the hyperthermophile Thermoproteus tenax: ATP-dependent hexokinases and ADP-dependent glucokinases, two alternatives for glucose phosphorylation in Archaea. J Biol Chem 278:18744–18753

    Article  CAS  Google Scholar 

  58. Kornberg A (1995) Inorganic polyphosphate: toward making a forgotten polymer unforgettable. J Bacteriol 177:491–496

    Article  CAS  Google Scholar 

  59. Szymona M, Widomski J (1974) A kinetic study on inorganic polyphosphate glucokinase from Mycobacterium tuberculosis H37RA. Physiol Chem Phys 6:393–404

    CAS  Google Scholar 

  60. Phillips NF, Hsieh PC, Kowalczyk TH (1999) Polyphosphate glucokinase. Prog Mol Subcell Biol 23:101–125

    Article  CAS  Google Scholar 

  61. Moreno-Sánchez R, Encalada R, Marín-Hernández A, Saavedra E (2008) Experimental validation of metabolic pathway modeling. FEBS J 275:3454–3469

    Article  CAS  Google Scholar 

  62. Mertens E (1991) Pyrophosphate-dependent phosphofructokinase, an anaerobic glycolytic enzyme? FEBS 285:1–5

    Article  CAS  Google Scholar 

  63. Mertens E, Ladror US, Lee JA, Miretsky A, Morris A, Rozario C, Kemp RG, Müller M (1998) The pyrophosphate-dependent phosphofructokinase of the protist, Trichomonas vaginalis, and the evolutionary relationships of protist phosphofructokinases. J Mol Evol 47:739–750

    Article  CAS  Google Scholar 

  64. Peng ZY, Mansour TE (1992) Purification and properties of a pyrophosphate-dependent phosphofructokinase from Toxoplasma gondii. Mol Biochem Parasitol 54:223–230

    Article  CAS  Google Scholar 

  65. Wood HG, O’brien WE, Micheales G (1977) Properties of carboxytransphosphorylase; pyruvate, phosphate dikinase; pyrophosphate-phosphofructikinase and pyrophosphate-acetate kinase and their roles in the metabolism of inorganic pyrophosphate. Adv Enzymol Relat Areas Mol Biol 45:85–155

    CAS  Google Scholar 

  66. Michels PA, Chevalier N, Opperdoes FR, Rider MH, Rigden DJ (1997) The glycosomal ATP-dependent phosphofructokinase of Trypanosoma brucei must have evolved from an ancestral pyrophosphate-dependent enzyme. Eur J Biochem 250:698–704

    Article  CAS  Google Scholar 

  67. Siebers B, Klenk HP, Hensel R (1998) PP(i)-dependent phosphofructokinase from Thermoproteus tenax, an archaeal descendant of an ancient line in phosphofructokinase evolution. J Bacteriol 180:2137–2143

    CAS  Google Scholar 

  68. Wu LF, Reizer A, Reizer J, Cai B, Tomich JM, Saier MH (1991) Nucleotide sequence of the Rhodobacter capsulatus fruK gene, which encodes fructose-1-phosphate kinase: evidence for a kinase superfamily including both phosphofructokinases of Escherichia coli. J Bacteriol 173:3117–3127

    Article  CAS  Google Scholar 

  69. Ding YHR, Ronimus RS, Morgan HW (2000) Sequencing, cloning, and high-level expression of the pfp gene, encoding a PP(i)-dependent phosphofructokinase from the extremely thermophilic eubacterium Dictyoglomus thermophilum. J Bacteriol 182:4661–4666

    Article  CAS  Google Scholar 

  70. Kotlarz D, Buc H (1982) Phosphofructokinases from Escherichia coli. Methods Enzymol 90 Pt E:60–70

    Google Scholar 

  71. Ronimus RS, Morgan HW (2001) The biochemical properties and phylogenies of phosphofructokinases from extremophiles. Extremophiles 5:357–373

    Article  CAS  Google Scholar 

  72. Sigrell JA, Cameron AD, Jones TA, Mowbray SL (1998) Structure of Escherichia coli ribokinase in complex with ribose and dinucleotide determined to 1.8 A resolution: insights into a new family of kinase structures. Structure 6:183–193

    Article  CAS  Google Scholar 

  73. Verhees CH, Tuininga JE, Kengen SWM, Stams AJM, Van Der Oost J, De Vos WM (2001) ADP-dependent phosphofructokinases in mesophilic and thermophilic methanogenic archaea. J Bacteriol 183:7145–7153

    Article  CAS  Google Scholar 

  74. Tuininga JE, Verhees CH, van der Oost J, Kengen SW, Stams AJ, de Vos WM (1999) Molecular and biochemical characterization of the ADP-dependent phosphofructokinase from the hyperthermophilic archaeon Pyrococcus furiosus. J Biol Chem 274:21023–21028

    Article  CAS  Google Scholar 

  75. Fothergill-Gilmore LA, Michels PA (1993) Evolution of glycolysis. Prog Biophys Mol Biol 59:105–235

    Article  CAS  Google Scholar 

  76. Brinkmann H, Cerff R, Salomon M, Soll J (1989) Cloning and sequence analysis of cDNAs encoding the cytosolic precursors of subunits GapA and GapB of chloroplast glyceraldehyde-3-phosphate dehydrogenase from pea and spinach. Plant Mol Biol 13:81–94

    Article  CAS  Google Scholar 

  77. Valverde F, Losada M, Serrano A (1997) Functional complementation of an Escherichia coli gap mutant supports an amphibolic role for NAD(P)-dependent glyceraldehyde-3-phosphate dehydrogenase of Synechocystis sp. Strain PCC 6803. J Bacteriol 179:4513–4522

    Article  CAS  Google Scholar 

  78. Krietsch WK, Bücher T (1970) 3-Phosphoglycerate kinase from rabbit skeletal muscle and yeast. Eur J Biochem 17:568–580

    Article  CAS  Google Scholar 

  79. Kuntz GWK, Krietsch WKG (1982) Phosphoglycerate kinase from spinach, blue-green algae, and yeast. Methods Enzymol 90:110–114

    Article  CAS  Google Scholar 

  80. Encalada R, Rojo-Domínguez A, Rodríguez-Zavala JS, Pardo JP, Quezada H, Moreno-Sánchez R, Saavedra E (2009) Molecular basis of the unusual catalytic preference for GDP/GTP in Entamoeba histolytica 3-phosphoglycerate kinase. FEBS J 276:2037–2047

    Article  CAS  Google Scholar 

  81. Reher M, Gebhard S, Schönheit P (2007) Glyceraldehyde-3-phosphate ferredoxin oxidoreductase (GAPOR) and nonphosphorylating glyceraldehyde-3-phosphate dehydrogenase (GAPN), key enzymes of the respective modified Embden-Meyerhof pathways in the hyperthermophilic crenarchaeota Pyrobaculum aerophi. FEMS Microbiol Lett 273:196–205

    Article  CAS  Google Scholar 

  82. Van Der Oost J, Schut G, Kengen SWM, Hagen WR, Thomm M, De Vos WM (1998) The ferredoxin-dependent conversion of glyceraldehyde-3-phosphate in the hyperthermophilic archaeon Pyrococcus furiosus represents a novel site of glycolytic regulation. J Biol Chem 273:28149–28154

    Article  Google Scholar 

  83. Boyd DA, Cvitkovitch DG, Hamilton IR (1995) Sequence, expression, and function of the gene for the phosphate dehydrogenase of Streptococcus mutans. J Bacteriol 177:2622–2627

    Google Scholar 

  84. Brown AT, Wittenberger CL (1971) Mechanism for regulating the distribution of glucose carbon between the Embden–Meyerhof and hexose-monophosphate pathways in Streptococcus faecalis. J Bacteriol 106:456–467

    CAS  Google Scholar 

  85. Iddar A, Valverde F, Assobhei O, Serrano A, The S (2005) Widespread occurrence of non-phosphorylating dehydrogenase among Gram-positive bacteria. Int Microbiol 8:251–258

    CAS  Google Scholar 

  86. Iddar A, Valverde F, Serrano A, Soukri A (2002) Expression, purification, and characterization of recombinant nonphosphorylating NADP-dependent glyceraldehyde-3-phosphate dehydrogenase from Clostridium acetobutylicum. Protein Expr Purif 25:519–526

    Article  CAS  Google Scholar 

  87. Schramm A, Siebers B, Tjaden B, Brinkmann H, Hensel R (2000) Pyruvate kinase of the hyperthermophilic crenarchaeote Thermoproteus tenax: physiological role and phylogenetic aspects. J Bacteriol 182:2001–2009

    Article  CAS  Google Scholar 

  88. Imanaka H, Yamatsu A, Fukui T, Atomi H, Imanaka T (2006) Phosphoenolpyruvate synthase plays an essential role for glycolysis in the modified Embden–Meyerhof pathway in Thermococcus kodakarensis. Mol Microbiol 61:898–909

    Article  CAS  Google Scholar 

  89. Tjaden B, Plagens A, Dörr C, Siebers B, Hensel R (2006) Phosphoenolpyruvate synthetase and pyruvate, phosphate dikinase of Thermoproteus tenax: key pieces in the puzzle of archaeal carbohydrate metabolism. Mol Microbiol 60:287–298

    Article  CAS  Google Scholar 

  90. Bielen AAM, Willquist K, Engman J, van der Oost J, van Niel EWJ, Kengen SWM (2010) Pyrophosphate as a central energy carrier in the hydrogen-producing extremely thermophilic Caldicellulosiruptor saccharolyticus. FEMS Microbiol Lett 307:48–54

    Article  CAS  Google Scholar 

  91. Feng XM, Cao LJ, Adam RD, Zhang XC, Lu SQ (2008) The catalyzing role of PPDK in Giardia lamblia. Biochem Biophys Res Commun 367:394–398

    Article  CAS  Google Scholar 

  92. Yutin N, Galperin MY (2013) A genomic update on clostridial phylogeny: Gram-negative spore formers and other misplaced clostridia. Environ Microbiol 15:2631–2641

    CAS  Google Scholar 

  93. Rydzak T, Levin DB, Cicek N, Sparling R (2009) Growth phase-dependent enzyme profile of pyruvate catabolism and end-product formation in Clostridium thermocellum ATCC 27405. J Biotechnol 140:169–175

    Article  CAS  Google Scholar 

  94. 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

    Article  CAS  Google Scholar 

  95. Carere CR, Kalia V, Sparling R, Cicek N, Levin DB (2008) Pyruvate catabolism and hydrogen synthesis pathway genes of Clostridium thermocellum ATCC 27405. Indian J Microbiol 48:252–266

    Article  CAS  Google Scholar 

  96. 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

    Article  CAS  Google Scholar 

  97. Lynd L, Grethlein H, Wolkin R (1989) Fermentation of cellulosic substrates in batch and continuous culture by Clostridium thermocellum. Appl Environ Microbiol 55:3131–3139

    CAS  Google Scholar 

  98. Ellis LD, Holwerda EK, Hogsett D, Rogers S, Shao X, Tschaplinski T, Thorne P, Lynd LR (2012) Closing the carbon balance for fermentation by Clostridium thermocellum (ATCC 27405). Bioresour Technol 103:293–299

    Article  CAS  Google Scholar 

  99. Roberts SB, Gowen CM, Brooks JP, Fong SS (2010) Genome-scale metabolic analysis of Clostridium thermocellum for bioethanol production. BMC Syst Biol 4:31

    Article  CAS  Google Scholar 

  100. Raman B, McKeown CK, Rodriguez M, Brown SD, Mielenz JR (2011) Transcriptomic analysis of Clostridium thermocellum ATCC 27405 cellulose fermentation. BMC Microbiol 11:134

    Article  CAS  Google Scholar 

  101. 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

    Article  CAS  Google Scholar 

  102. Burton E, Martin VJJ (2012) 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

    Article  CAS  Google Scholar 

  103. Patni NJ, Alexander JK (1971) Utilization of glucose by Clostridium thermocellum: presence of glucokinase and other glycolytic enzymes in cell extracts. J Bacteriol 105:220–225

    CAS  Google Scholar 

  104. Zhou J, Olson DG, Argyros DA, Deng Y, van Gulik WM, van Dijken JP, Lynd LR (2013) Atypical glycolysis in Clostridium thermocellum. Appl Environ Microbiol 79:3000–3008

    Article  CAS  Google Scholar 

  105. Golovchenko N, Chuvilskaya N, Akimenko V (1986) Regulation of biosynthesis of cellulolytic enzymes and enzymes catalyzing initial catabolism of glucose and cellobiose in Clostridium thermocellum. Microbiology 55:23–25

    Google Scholar 

  106. Erbeznik M, Jones CR, Dawson KA, Strobel HJ (1997) Clostridium thermocellum JW20 (ATCC 31549) is a coculture with Thermoanaerobacter ethanolicus. Appl Environ Microbiol 63:2949–2951

    CAS  Google Scholar 

  107. Nochur SV, Jacobson GR, Roberts MF, Demain AL (1992) Mode of sugar phosphorylation in Clostridium thermocellum. Appl Biochem Biotechnol 33:33–41

    Article  CAS  Google Scholar 

  108. Glass TL, Sherwood JS (1994) Phosphorylation of glucose by a guanosine-5′-triphosphate (GTP)-dependent glucokinase in Fibrobacter succinogenes subsp. succinogenes S85. Arch Microbiol 162:180–186

    CAS  Google Scholar 

  109. Lou J, Dawson KA, Strobel HJ (1997) Cellobiose and cellodextrin metabolism by the ruminal bacterium Ruminococcus albus. Curr Microbiol 35:221–227

    Article  CAS  Google Scholar 

  110. Müller M (1992) Energy metabolism of ancestral eukaryotes: a hypothesis based on the biochemistry of a mitochondriate parasitic protists. Biosystems 28:33–40

    Article  Google Scholar 

  111. Müller M, Lee JA, Gordon P, Sensen CW (2001) Presence of prokaryotic and eukaryotic species in all subgroups of the PP i -dependent group II phosphofructokinase protein family presence of prokaryotic and eukaryotic species in all subgroups of the PP i -dependent group II phosphofructokinase protein. J Bacteriol 183:6714–6716

    Article  Google Scholar 

  112. Hutchins A, Holden J, Adams M (2001) Phosphoenolpyruvate synthetase from the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol 183:709–715

    Article  CAS  Google Scholar 

  113. Chao YP, Patnaik R, Roof WD, Young RF, Liao JC (1993) Control of gluconeogenic growth by pps and pck in Escherichia coli. J Bacteriol 175:6939–6944

    Article  CAS  Google Scholar 

  114. Acosta H, Dubourdieu M, Quiñones W, Cáceres A, Bringaud F, Concepción JL (2004) Pyruvate phosphate dikinase and pyrophosphate metabolism in the glycosome of Trypanosoma cruzi epimastigotes. Comp Biochem Physiol B Biochem Mol Biol 138:347–356

    Article  CAS  Google Scholar 

  115. Lamed R, Zeikus JG (1981) Thermostable, ammonium-activated malic enzyme of Clostridium thermocellum. Biochim Biophys Acta 660:251–255

    Article  CAS  Google Scholar 

  116. Taillefer M, Rydzak T, Levin DB, Oresnik IJ, Sparling R (2015) Reassessment of the transhydrogenase/malate shunt pathway in Clostridium thermocellum ATCC 27405 through kinetic characterization of malic enzyme and malate dehydrogenase. Appl Environ Microbiol 81:2423–2432

    Article  CAS  Google Scholar 

  117. Heinonen JK (2001) Biological role of inorganic pyrophosphate. Kluwer Academic Publishers, Boston

    Book  Google Scholar 

  118. Willquist K, van Niel EWJ (2010) Lactate formation in Caldicellulosiruptor saccharolyticus is regulated by the energy carriers pyrophosphate and ATP. Metab Eng 12:282–290

    Article  CAS  Google Scholar 

  119. Baltscheffsky M, Schultz A, Baltscheffsky H (1999) H+ -PPases: a tightly membrane-bound family. FEBS Lett 457:527–533

    Article  CAS  Google Scholar 

  120. Hungate RE (1963) Polysaccharide storage and growth efficiency in Ruminococcus albus. J Bacteriol 86:848–854

    CAS  Google Scholar 

  121. Guedon E, Desvaux M, Petitdemange H (2000) Kinetic analysis of Clostridium cellulolyticum carbohydrate metabolism: importance of glucose 1-phosphate and glucose 6-phosphate branch points for distribution of carbon fluxes inside and outside cells as revealed by steady- state continuous culture. J Bacteriol 182:2010–2017

    Article  CAS  Google Scholar 

  122. Mertens E (1993) ATP versus pyrophosphate: glycolysis revisited in parasitic protists. Parasitol Today 9:122–126

    Article  CAS  Google Scholar 

  123. Mertens E, De Jonckheere J, Van Schaftingen E (1993) Pyrophosphate-dependent phosphofructokinase from the amoeba Naegleria fowleri, an AMP-sensitive enzyme. Biochem J 292 3:797–803

    Google Scholar 

  124. Susskind BM, Warren LG, Reeves RE (1982) A pathway for the interconversion of hexose and pentose in the parasitic amoeba Entamoeba histolytica. Biochem J 204:191–196

    Article  CAS  Google Scholar 

  125. Nakahigashi K, Toya Y, Ishii N, Soga T, Hasegawa M, Watanabe H, Takai Y, Honma M, Mori H, Tomita M (2009) Systematic phenome analysis of Escherichia coli multiple-knockout mutants reveals hidden reactions in central carbon metabolism. Mol Syst Biol 5:306

    Article  CAS  Google Scholar 

  126. Rydzak T, Grigoryan M, Cunningham ZJ, Krokhin OV, Ezzati P, Cicek N, Levin DB, Wilkins JA, Sparling R (2014) Insights into electron flux through manipulation of fermentation conditions and assessment of protein expression profiles in Clostridium thermocellum. Appl Microbiol Biotechnol 98:6497–6510

    Article  CAS  Google Scholar 

  127. 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

    Article  CAS  Google Scholar 

  128. Carere CR, Rydzak T, Verbeke TJ, Cicek N, Levin DB, Sparling R (2012) Linking genome content to biofuel production yields: a meta-analysis of major catabolic pathways among select H2 and ethanol-producing bacteria. BMC Microbiol 12:295

    Article  CAS  Google Scholar 

  129. Bapteste E, Moreira D, Philippe H (2003) Rampant horizontal gene transfer and phospho-donor change in the evolution of the phosphofructokinase. Gene 318:185–191

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was funded through the Genome Canada-funded Microbial Genomics for Biofuels and Co-products Biorefineries project and through NSERC Discovery Grant (RGPIN-2014-06173).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Sparling .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Taillefer, M., Sparling, R. (2016). Glycolysis as the Central Core of Fermentation. In: Hatti-Kaul, R., Mamo, G., Mattiasson, B. (eds) Anaerobes in Biotechnology. Advances in Biochemical Engineering/Biotechnology, vol 156. Springer, Cham. https://doi.org/10.1007/10_2015_5003

Download citation

Publish with us

Policies and ethics