Biorefinery pp 437-460 | Cite as

Anaerobic Thermophilic Mixed Culture Fermentation Processes

  • Fang ZhangEmail author
  • Raymond Jianxiong Zeng


Advantageous properties, such as higher hydrogen production, high substrate degradation rate, and efficient heat utilization for the treatment of hot wastewater, favor the thermophilic mixed culture fermentation (MCF) over mesophilic MCF. In this chapter, the typical metabolic reactions in thermophilic MCF are summarized in Sect. 2 according to the multistep process of hydrolysis/acidogenesis, acetogenesis/homoacetogenesis, and methanogenesis. The operational conditions, such as pH, H2 partial pressure, and reactor configuration, may change the microbial community or the metabolic pathway in thermophilic MCF and are reviewed in Sect. 3. Lastly, the metabolites both in the headspace and in liquid solutions are always a mixture in thermophilic MCF, which have to be concentrated and purified before utilization. There are several conventional technologies to separate the metabolites and recover energy, including biogas upgrading, two-stage fermentation, gas stripping, electrodialysis (ED), and microbial fuel cells. These typical technologies, along with other novel technologies, such as production of sole metabolite and medium-chain carboxylic acids production, are reviewed in Sect. 4. The energy cost of thermophilic biogas plants was estimated as just 10% of the energy produced, which implies that the extra energy cost for operating at a thermophilic temperature is marginal. Therefore, the coupling of the process and development of novel technologies are necessary in thermophilic MCF to promote its worldwide application.


Thermophilic mixed culture fermentation Metabolic pathway Operational factors Metabolite separation and purification Biorefinery 



The authors would like to acknowledge the financial support from the National Natural Science Foundation of China (51408530, 50978244, and 51478447), Natural Science Foundation of Hebei Province (E2015203306), Foundation of Hebei Education Department (BJ2017014), and the Program for Changjiang Scholars and Innovative Research Team in University.


  1. Alberty RA (2003) Thermodynamics of biochemical reactions. Wiley, New YorkCrossRefGoogle Scholar
  2. Angenent LT, Karim K, Al-Dahhan MH, Wrenn BA, Domíguez-Espinosa R (2004) Production of bioenergy and biochemicals from industrial and agricultural wastewater. Trends Biotechnol 22(9):477–485CrossRefGoogle Scholar
  3. Artzi L, Morag E, Barak Y, Lamed R, Bayer EA (2015) Clostridium clariflavum: key cellulosome players are revealed by proteomic analysis. MBio 6(3):e00411–15Google Scholar
  4. Bakonyi P, Kumar G, Nemestóthy N, Lin CY, Bélafi-Bakó K (2013) Biohydrogen purification using a commercial polyimide membrane module: Studying the effects of some process variables. Int J Hydrogen Energy 38(35):15092–15099CrossRefGoogle Scholar
  5. Bastidas-Oyanedel J-R, Mohd-Zaki Z, Pratt S, Steyer J-P, Batstone DJ (2010) Development of membrane inlet mass spectrometry for examination of fermentation processes. Talanta 83(2):482–492CrossRefGoogle Scholar
  6. Bastidas-Oyanedel J-R, Mohd-Zaki Z, Zeng RJ, Bernet N, Pratt S, Steyer J-P, Batstone DJ (2012) Gas controlled hydrogen fermentation. Bioresour Technol 110:503–509CrossRefGoogle Scholar
  7. Bastidas-Oyanedel J-R, Bonk F, Thomsen M, Schmidt J (2015) Dark fermentation biorefinery in the present and future (bio)chemical industry. Rev Environ Sci Biotechnolgy 14(3):473–498CrossRefGoogle Scholar
  8. Batstone DJ, Virdis B (2014) The role of anaerobic digestion in the emerging energy economy. Curr Opin Biotechnol 27:142–149CrossRefGoogle Scholar
  9. Berg IA, Kockelkorn D, Ramos-Vera WH, Say RF, Zarzycki J, Hügler M, Alber BE, Fuchs G (2010) Autotrophic carbon fixation in archaea. Nat Rev Microbiol 8(6):447–460CrossRefGoogle Scholar
  10. Bertsch J, Müller V (2015) CO metabolism in the acetogen Acetobacterium woodii. Appl Environ Microbiol 81(17):5949–5956CrossRefGoogle Scholar
  11. Blumer-Schuette SE, Brown SD, Sander KB, Bayer EA, Kataeva I, Zurawski JV, Conway JM, Adams MWW, Kelly RM (2014) Thermophilic lignocellulose deconstruction. FEMS Microbiol Rev 38(3):393–448CrossRefGoogle Scholar
  12. Bonk F, Bastidas-Oyanedel J-R, Schmidt JE (2015) Converting the organic fraction of solid waste from the city of Abu Dhabi to valuable products via dark fermentation – economic and energy assessment. Waste Manag 40:82–91CrossRefGoogle Scholar
  13. Bonk F, Bastidas-Oyanedel J-R, Yousef AF, Schmidt JE (2017) Exploring the selective lactic acid production from food waste in uncontrolled pH mixed culture fermentations using different reactor configurations. Bioresour Technol 238:416–424CrossRefGoogle Scholar
  14. Cabrera-Codony A, Montes-Morán MA, Sánchez-Polo M, Martín MJ, Gonzalez-Olmos R (2014) Biogas upgrading: optimal activated carbon properties for siloxane removal. Environ Sci Technol 48(12):7187–7195CrossRefGoogle Scholar
  15. Chaikasem S, Abeynayaka A, Visvanathan C (2014) Effect of polyvinyl alcohol hydrogel as a biocarrier on volatile fatty acids production of a two-stage thermophilic anaerobic membrane bioreactor. Bioresour Technol 168(suppl C):100–105CrossRefGoogle Scholar
  16. Chen M, Zhang F, Zhang Y, Zeng RJ (2013) Alkali production from bipolar membrane electrodialysis powered by microbial fuel cell and application for biogas upgrading. Appl Energy 103:428–434CrossRefGoogle Scholar
  17. Chen Y, Wang T, Shen N, Zhang F, Zeng RJ (2016a) High-purity propionate production from glycerol in mixed culture fermentation. Bioresour Technol 219:659–667CrossRefGoogle Scholar
  18. Chen Y, Zhang F, Wang T, Shen N, Yu Z-W, Zeng RJ (2016b) Hydraulic retention time affects stable acetate production from tofu processing wastewater in extreme-thermophilic (70 °C) mixed culture fermentation. Bioresour Technol 216:722–728CrossRefGoogle Scholar
  19. Chen Y, Jiang X, Xiao K, Shen N, Zeng RJ, Zhou Y (2017a) Enhanced volatile fatty acids (VFAs) production in a thermophilic fermenter with stepwise pH increase – Investigation on dissolved organic matter transformation and microbial community shift. Water Res 112:261–268CrossRefGoogle Scholar
  20. Chen Y, Shen N, Wang T, Zhang F, Zeng RJ (2017b) Ammonium level induces high purity propionate production in mixed culture glucose fermentation. RSC Adv 7(1):518–525CrossRefGoogle Scholar
  21. da Silva GP, Mack M, Contiero J (2009) Glycerol: a promising and abundant carbon source for industrial microbiology. Biotechnol Adv 27(1):30–39CrossRefGoogle Scholar
  22. de Vrije T, Mars A, Budde M, Lai M, Dijkema C, de Waard P, Claassen P (2007) Glycolytic pathway and hydrogen yield studies of the extreme thermophile Caldicellulosiruptor saccharolyticus. Appl Microbiol Biotechnol 74(6):1358–1367CrossRefGoogle Scholar
  23. Daelman MRJ, Sorokin D, Kruse O, van Loosdrecht MCM, Strous M (2016) Haloalkaline bioconversions for methane production from microalgae grown on sunlight. Trends Biotechnol 34(6):450–457CrossRefGoogle Scholar
  24. Dai X, Li X, Zhang D, Chen Y, Dai L (2016) Simultaneous enhancement of methane production and methane content in biogas from waste activated sludge and perennial ryegrass anaerobic co-digestion: the effects of pH and C/N ratio. Bioresour Technol 216:323–330CrossRefGoogle Scholar
  25. Dai K, Wen J-L, Zhang F, Zeng RJ (2017) Valuable biochemical production in mixed culture fermentation: fundamentals and process coupling. Appl Microbiol Biotechnol 101(17):6575–6586CrossRefGoogle Scholar
  26. Dai K, Zhang F, Zhang Y, Zeng RJ (2018) The chemostat metabolite spectra of alkaline mixed culture fermentation under mesophilic, thermophilic, and extreme-thermophilic conditions. Bioresour Technol 249:322–327CrossRefGoogle Scholar
  27. Deng L, Hägg M-B (2010) Techno-economic evaluation of biogas upgrading process using CO2 facilitated transport membrane. Int J Greenhouse Gas Control 4(4):638–646CrossRefGoogle Scholar
  28. Dopson M, Ni G, Sleutels THJA (2016) Possibilities for extremophilic microorganisms in microbial electrochemical systems. FEMS Microbiol Rev 40(2):164–181CrossRefGoogle Scholar
  29. Frock AD, Kelly RM (2012) Extreme thermophiles: moving beyond single-enzyme biocatalysis. Curr Opin Chem Eng 1(4):363–372CrossRefGoogle Scholar
  30. Gannoun H, Othman NB, Bouallagui H, Moktar H (2007) Mesophilic and thermophilic anaerobic co-digestion of olive mill wastewaters and abattoir wastewaters in an upflow anaerobic filter. Ind Eng Chem Res 46(21):6737–6743CrossRefGoogle Scholar
  31. Ge H, Jensen PD, Batstone DJ (2011) Temperature phased anaerobic digestion increases apparent hydrolysis rate for waste activated sludge. Water Res 45(4):1597–1606CrossRefGoogle Scholar
  32. Ha PT, Lee TK, Rittmann BE, Park J, Chang IS (2012) Treatment of alcohol distillery wastewater using a bacteroidetes-dominant thermophilic microbial fuel cell. Environ Sci Technol 46(5):3022–3030CrossRefGoogle Scholar
  33. Hashi M, Tezel FH, Thibault J (2010) Ethanol recovery from fermentation broth via carbon dioxide stripping and adsorption. Energy Fuel 24(9):4628–4637CrossRefGoogle Scholar
  34. Ho L, Ho G (2012) Mitigating ammonia inhibition of thermophilic anaerobic treatment of digested piggery wastewater: use of pH reduction, zeolite, biomass and humic acid. Water Res 46(14):4339–4350CrossRefGoogle Scholar
  35. Hoelzle RD, Virdis B, Batstone DJ (2014) Regulation mechanisms in mixed and pure culture microbial fermentation. Biotechnol Bioeng 111(11):2139–2154CrossRefGoogle Scholar
  36. Hori T, Haruta S, Ueno Y, Ishii M, Igarashi Y (2006) Dynamic transition of a methanogenic population in response to the concentration of volatile fatty acids in a thermophilic anaerobic digester. Appl Environ Microbiol 72(2):1623–1630CrossRefGoogle Scholar
  37. Hosseini SE, Wahid MA (2016) Hydrogen production from renewable and sustainable energy resources: promising green energy carrier for clean development. Renew Sustain Energy Rev 57:850–866CrossRefGoogle Scholar
  38. Jiang L, Wang J, Liang S, Cai J, Xu Z, Cen P, Yang S, Li S (2011) Enhanced butyric acid tolerance and bioproduction by Clostridium tyrobutyricum immobilized in a fibrous bed bioreactor. Biotechnol Bioeng 108(1):31–40CrossRefGoogle Scholar
  39. Jin B, Wang S, Xing L, Li B, Peng Y (2016) Long term effect of alkali types on waste activated sludge hydrolytic acidification and microbial community at low temperature. Bioresour Technol 200:587–597CrossRefGoogle Scholar
  40. Jong BC, Kim BH, Chang IS, Liew PWY, Choo YF, Kang GS (2006) Enrichment, performance, and microbial diversity of a thermophilic mediatorless microbial fuel cell. Environ Sci Technol 40(20):6449–6454CrossRefGoogle Scholar
  41. Jönsson LJ, Martín C (2016) Pretreatment of lignocellulose: formation of inhibitory by-products and strategies for minimizing their effects. Bioresour Technol 199:103–112CrossRefGoogle Scholar
  42. Karakashev D, Batstone DJ, Angelidaki I (2005) Influence of environmental conditions on methanogenic compositions in anaerobic biogas reactors. Appl Environ Microbiol 71(1):331–338CrossRefGoogle Scholar
  43. Karakashev D, Batstone DJ, Trably E, Angelidaki I (2006) Acetate oxidation is the dominant methanogenic pathway from acetate in the absence of methanosaetaceae. Appl Environ Microbiol 72(7):5138–5141CrossRefGoogle Scholar
  44. Khiewwijit R, Temmink H, Labanda A, Rijnaarts H, Keesman KJ (2015) Production of volatile fatty acids from sewage organic matter by combined bioflocculation and alkaline fermentation. Bioresour Technol 197:295–301CrossRefGoogle Scholar
  45. Khor WC, Andersen S, Vervaeren H, Rabaey K (2017) Electricity-assisted production of caproic acid from grass. Biotechnol Biofuels 10(1):180CrossRefGoogle Scholar
  46. Kim D-H, Han S-K, Kim S-H, Shin H-S (2006) Effect of gas sparging on continuous fermentative hydrogen production. Int J Hydrogen Energy 31(15):2158–2169CrossRefGoogle Scholar
  47. Kleerebezem R, van Loosdrecht MCM (2007) Mixed culture biotechnology for bioenergy production. Curr Opin Biotechnol 18(3):207–212CrossRefGoogle Scholar
  48. Kleerebezem R, Van Loosdrecht MCM (2010) A generalized method for thermodynamic state analysis of environmental systems. Crit Rev Environ Sci Technol 40(1):1–54CrossRefGoogle Scholar
  49. Kleerebezem R, Joosse B, Rozendal R, Loosdrecht MCM (2015) Anaerobic digestion without biogas? Rev Environ Sci Biotechnol 14(4):787–801CrossRefGoogle Scholar
  50. Kongjan P, Angelidaki I (2010) Extreme thermophilic biohydrogen production from wheat straw hydrolysate using mixed culture fermentation: effect of reactor configuration. Bioresour Technol 101(20):7789–7796CrossRefGoogle Scholar
  51. Kongjan P, Min B, Angelidaki I (2009) Biohydrogen production from xylose at extreme thermophilic temperatures (70 °C) by mixed culture fermentation. Water Res 43(5):1414–1424CrossRefGoogle Scholar
  52. Kothari R, Singh DP, Tyagi VV, Tyagi SK (2012) Fermentative hydrogen production - an alternative clean energy source. Renew Sustain Energy Rev 16(4):2337–2346CrossRefGoogle Scholar
  53. Kraemer J, Bagley D (2006) Supersaturation of dissolved H2 and CO2 during fermentative hydrogen production with N2 sparging. Biotechnol Lett 28(18):1485–1491CrossRefGoogle Scholar
  54. Labatut RA, Angenent LT, Scott NR (2014) Conventional mesophilic vs. thermophilic anaerobic digestion: a trade-off between performance and stability? Water Res 53:249–258CrossRefGoogle Scholar
  55. Lee HS, Salerno MB, Rittmann BE (2008) Thermodynamic evaluation on H2 production in glucose fermentation. Environ Sci Technol 42(7):2401–2407CrossRefGoogle Scholar
  56. Lee HS, Krajmalinik-Brown R, Zhang HS, Rittmann BE (2009) An electron-flow model can predict complex redox reactions in mixed-culture fermentative BioH(2): microbial ecology evidence. Biotechnol Bioeng 104(4):687–697Google Scholar
  57. Leng L, Yang P, Mao Y, Wu Z, Zhang T, Lee P-H (2017) Thermodynamic and physiological study of caproate and 1,3-propanediol co-production through glycerol fermentation and fatty acids chain elongation. Water Res 114:200–209CrossRefGoogle Scholar
  58. Lengeler JW, Drews G, Schlegel HG (1999) Biology of the prokaryotes. Georg Thieme, StuttgartGoogle Scholar
  59. Lewandowicz G, Białas W, Marczewski B, Szymanowska D (2011) Application of membrane distillation for ethanol recovery during fuel ethanol production. J Membr Sci 375(1–2):212–219CrossRefGoogle Scholar
  60. Li W-W, Yu H-Q (2011) From wastewater to bioenergy and biochemicals via two-stage bioconversion processes: a future paradigm. Biotechnol Adv 29(6):972–982MathSciNetCrossRefGoogle Scholar
  61. Logan B, Regan J (2006) Microbial fuel cells-challenges and applications. Environ Sci Technol 40(17):5172–5180CrossRefGoogle Scholar
  62. Louis P, Duncan SH, McCrae SI, Millar J, Jackson MS, Flint HJ (2004) Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J Bacteriol 186(7):2099–2106CrossRefGoogle Scholar
  63. Lovley DR (2008) The microbe electric: conversion of organic matter to electricity. Curr Opin Biotechnol 19(6):564–571CrossRefGoogle Scholar
  64. Lü F, Chai L, Shao L, He P (2017) Precise pretreatment of lignocellulose: relating substrate modification with subsequent hydrolysis and fermentation to products and by-products. Biotechnol Biofuels 10:88CrossRefGoogle Scholar
  65. Luo G, Xie L, Zhou Q, Angelidaki I (2011) Enhancement of bioenergy production from organic wastes by two-stage anaerobic hydrogen and methane production process. Bioresour Technol 102(18):8700–8706CrossRefGoogle Scholar
  66. Luo G, Johansson S, Boe K, Xie L, Zhou Q, Angelidaki I (2012) Simultaneous hydrogen utilization and in situ biogas upgrading in an anaerobic reactor. Biotechnol Bioeng 109(4):1088–1094CrossRefGoogle Scholar
  67. Madigan M, Martinko J, Bender K, Buckley D, Stahl D (2002) The Brock biology of microorganisms (Global ed). Pearson Education Limited, HarlowGoogle Scholar
  68. Meynial-Salles I, Dorotyn S, Soucaille P (2008) A new process for the continuous production of succinic acid from glucose at high yield, titer, and productivity. Biotechnol Bioeng 99(1):129–135CrossRefGoogle Scholar
  69. Moon HG, Jang YS, Cho C, Lee J, Binkley R, Lee SY (2016) One hundred years of clostridial butanol fermentation. FEMS Microbiol Lett 363(3):fnw001Google Scholar
  70. Moresi M, Sappino F (2000) Electrodialytic recovery of some fermentation products from model solutions: techno-economic feasibility study. J Membr Sci 164(1–2):129–140CrossRefGoogle Scholar
  71. Narihiro T, Nobu MK, Tamaki H, Kamagata Y, Sekiguchi Y, Liu W-T (2016) Comparative genomics of syntrophic branched-chain fatty acid degrading bacteria. Microb Environ 31(3):288–292CrossRefGoogle Scholar
  72. Nielsen HB, Mladenovska Z, Ahring BK (2007) Bioaugmentation of a two-stage thermophilic (68°C/55°C) anaerobic digestion concept for improvement of the methane yield from cattle manure. Biotechnol Bioeng 97(6):1638–1643CrossRefGoogle Scholar
  73. Pawar S, Niel EJ (2013) Thermophilic biohydrogen production: how far are we? Appl Microbiol Biotechnol 97(18):7999–8009CrossRefGoogle Scholar
  74. Pawar SS, Nkemka VN, Zeidan AA, Murto M, van Niel EWJ (2013) Biohydrogen production from wheat straw hydrolysate using Caldicellulosiruptor saccharolyticus followed by biogas production in a two-step uncoupled process. Int J Hydrogen Energy 38(22):9121–9130CrossRefGoogle Scholar
  75. Perry RH, Green DW (2008) Perry’s chemical engineers’ handbook. McGraw-Hill, New YorkGoogle Scholar
  76. Peters JW, Miller AF, Jones AK, King PW, Adams MW (2016) Electron bifurcation. Curr Opin Chem Biol 31:146–152CrossRefGoogle Scholar
  77. Petersson A, Wellinger A (2009) Biogas upgrading technologies–developments and innovations, vol 37. IEA-Task, p 20Google Scholar
  78. Poehlein A, Schmidt S, Kaster A-K, Goenrich M, Vollmers J, Thürmer A, Bertsch J, Schuchmann K, Voigt B, Hecker M, Daniel R, Thauer RK, Gottschalk G, Müller V (2012) An ancient pathway combining carbon dioxide fixation with the generation and utilization of a sodium ion gradient for ATP synthesis. PLoS One 7(3):e33439CrossRefGoogle Scholar
  79. Price ND, Reed JL, Palsson BO (2004) Genome-scale models of microbial cells: evaluating the consequences of constraints. Nat Rev Microbiol 2(11):886–897CrossRefGoogle Scholar
  80. Qiu C, Wen J, Jia X (2011) Extreme-thermophilic biohydrogen production from lignocellulosic bioethanol distillery wastewater with community analysis of hydrogen-producing microflora. Int J Hydrogen Energy 36(14):8243–8251CrossRefGoogle Scholar
  81. Redwood MD, Orozco RL, Majewski AJ, Macaskie LE (2012) An integrated biohydrogen refinery: synergy of photofermentation, extractive fermentation and hydrothermal hydrolysis of food wastes. Bioresour Technol 119:384–392CrossRefGoogle Scholar
  82. Ryckebosch E, Drouillon M, Vervaeren H (2011) Techniques for transformation of biogas to biomethane. Biomass Bioenergy 35(5):1633–1645CrossRefGoogle Scholar
  83. Sawers RG (2005) Formate and its role in hydrogen production in Escherichia coli. Biochem Soc Trans 33(Pt 1):42–46CrossRefGoogle Scholar
  84. Schuchmann K, Muller V (2014) Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat Rev Microbiol 12(12):809–821CrossRefGoogle Scholar
  85. Schut GJ, Adams MWW (2009) The iron-hydrogenase of thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J Bacteriol 191(13):4451–4457CrossRefGoogle Scholar
  86. Seeliger S, Janssen P, Schink B (2002) Energetics and kinetics of lactate fermentation to acetate and propionate via methylmalonyl-CoA or acrylyl-CoA. FEMS Microbiol Lett 211(1):65–70CrossRefGoogle Scholar
  87. Serna-Maza A, Heaven S, Banks CJ (2014) Ammonia removal in food waste anaerobic digestion using a side-stream stripping process. Bioresour Technol 152:307–315CrossRefGoogle Scholar
  88. Smith ET, Blamey JM, Zhou ZH, Adams MWW (1995) A variable-temperature direct electrochemical study of metalloproteins from hyperthermophilic microorganisms involved in hydrogen production from pyruvate. Biochemistry 34(21):7161–7169CrossRefGoogle Scholar
  89. Smith AL, Skerlos SJ, Raskin L (2015) Anaerobic membrane bioreactor treatment of domestic wastewater at psychrophilic temperatures ranging from 15 oC to 3 oC. Environ Sci Water Res Technol 1(1):56–64CrossRefGoogle Scholar
  90. Soboh B, Linder D, Hedderich R (2004) A multisubunit membrane-bound [NiFe] hydrogenase and an NADH-dependent Fe-only hydrogenase in the fermenting bacterium Thermoanaerobacter tengcongensis. Microbiology 150(7):2451–2463CrossRefGoogle Scholar
  91. Sousa DZ, Smidt H, Alves MM, Stams AJM (2009) Ecophysiology of syntrophic communities that degrade saturated and unsaturated long-chain fatty acids. FEMS Microbiol Ecol 68(3):257–272CrossRefGoogle Scholar
  92. Sowunmi A, Mamone RM, Bastidas-Oyanedel J-R, Schmidt JE (2016) Biogas potential for electricity generation in the Emirate of Abu Dhabi. Biomass Convers Biorefin 6(1):39–47CrossRefGoogle Scholar
  93. Speight JG (2005) Lange’s handbook of chemistry. McGraw-Hill, New YorkGoogle Scholar
  94. Steinbusch KJJ, Hamelers HVM, Plugge CM, Buisman CJN (2011) Biological formation of caproate and caprylate from acetate: fuel and chemical production from low grade biomass. Energ Environ Sci 4(1):216–224CrossRefGoogle Scholar
  95. Stephen AJ, Archer SA, Orozco RL, Macaskie LE (2017) Advances and bottlenecks in microbial hydrogen production. J Microbial Biotechnol 10(5):1120–1127CrossRefGoogle Scholar
  96. Straub CT, Zeldes BM, Schut GJ, Adams MWW, Kelly RM (2017) Extremely thermophilic energy metabolisms: biotechnological prospects. Curr Opin Biotechnol 45:104–112CrossRefGoogle Scholar
  97. Svetlitchnyi VA, Kensch O, Falkenhan DA, Korseska SG, Lippert N, Prinz M, Sassi J, Schickor A, Curvers S (2013) Single-step ethanol production from lignocellulose using novel extremely thermophilic bacteria. Biotechnol Biofuels 6:31CrossRefGoogle Scholar
  98. Tapia-Venegas E, Ramirez-Morales J, Silva-Illanes F, Toledo-Alarcón J, Paillet F, Escudie R, Lay C-H, Chu C-Y, Leu H-J, Marone A, Lin C-Y, Kim D-H, Trably E, Ruiz-Filippi G (2015) Biohydrogen production by dark fermentation: scaling-up and technologies integration for a sustainable system. Rev Environ Sci Biotechnol 14(4):761–785CrossRefGoogle Scholar
  99. Temudo MF, Kleerebezem R, van Loosdrecht M (2007) Influence of the pH on (open) mixed culture fermentation of glucose: a chemostat study. Biotechnol Bioeng 98(1):69–79CrossRefGoogle Scholar
  100. Temudo MF, Mato T, Kleerebezem R, van Loosdrecht MCM (2009) Xylose anaerobic conversion by open-mixed cultures. Appl Microbiol Biotechnol 82(2):231–239CrossRefGoogle Scholar
  101. Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41(1):100–180Google Scholar
  102. Thauer RK, Kaster AK, Seedorf H, Buckel W, Hedderich R (2008) Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6(8):579–591CrossRefGoogle Scholar
  103. Tuck CO, Pérez E, Horváth IT, Sheldon RA, Poliakoff M (2012) Valorization of biomass: deriving more value from waste. Science 337(6095):695–699CrossRefGoogle Scholar
  104. Turina P, Petersen J, Gräber P (2016) Thermodynamics of proton transport coupled ATP synthesis. Biochim Biophys Acta Bioenerg 1857(6):653–664CrossRefGoogle Scholar
  105. Ueno Y, Sasaki D, Fukui H, Haruta S, Ishii M, Igarashi Y (2006) Changes in bacterial community during fermentative hydrogen and acid production from organic waste by thermophilic anaerobic microflora. J Appl Microbiol 101(2):331–343CrossRefGoogle Scholar
  106. Ueno Y, Fukui H, Goto M (2007) Operation of a two-stage fermentation process producing hydrogen and methane from organic waste. Environ Sci Technol 41(4):1413–1419CrossRefGoogle Scholar
  107. van der Ha D, Nachtergaele L, Kerckhof F-M, Rameiyanti D, Bossier P, Verstraete W, Boon N (2012) Conversion of biogas to bioproducts by algae and methane oxidizing bacteria. Environ Sci Technol 46(24):13425–13431CrossRefGoogle Scholar
  108. Wang X, Wang Y, Zhang X, Xu T (2012) In situ combination of fermentation and electrodialysis with bipolar membranes for the production of lactic acid: operational compatibility and uniformity. Bioresour Technol 125:165–171CrossRefGoogle Scholar
  109. Wang X, Wang Y, Zhang X, Feng H, Xu T (2013) In-situ combination of fermentation and electrodialysis with bipolar membranes for the production of lactic acid: continuous operation. Bioresour Technol 147:442–448CrossRefGoogle Scholar
  110. Wang H, Zhang Y, Angelidaki I (2016) Ammonia inhibition on hydrogen enriched anaerobic digestion of manure under mesophilic and thermophilic conditions. Water Res 105:314–319CrossRefGoogle Scholar
  111. Wang D, Liu Y, Ngo HH, Zhang C, Yang Q, Peng L, He D, Zeng G, Li X, Ni B-J (2017) Approach of describing dynamic production of volatile fatty acids from sludge alkaline fermentation. Bioresour Technol 238:343–351CrossRefGoogle Scholar
  112. Wijekoon KC, Visvanathan C, Abeynayaka A (2011) Effect of organic loading rate on VFA production, organic matter removal and microbial activity of a two-stage thermophilic anaerobic membrane bioreactor. Bioresour Technol 102(9):5353–5360CrossRefGoogle Scholar
  113. Willquist K, Zeidan A, van Niel E (2010) Physiological characteristics of the extreme thermophile Caldicellulosiruptor saccharolyticus: an efficient hydrogen cell factory. Microb Cell Fact 9(1):89CrossRefGoogle Scholar
  114. Wu Y, Wang C, Liu X, Ma H, Wu J, Zuo J, Wang K (2016) A new method of two-phase anaerobic digestion for fruit and vegetable waste treatment. Bioresour Technol 211:16–23CrossRefGoogle Scholar
  115. Xu J, Hao J, Guzman JJL, Spirito CM, Harroff LA, Angenent LT (2018) Temperature-phased conversion of acid whey waste into medium-chain carboxylic acids via lactic acid: no external e-donor. Joule 2(2):280–295CrossRefGoogle Scholar
  116. Xue C, Liu F, Xu M, Zhao J, Chen L, Ren J, Bai F, Yang S-T (2016) A novel in situ gas stripping-pervaporation process integrated with acetone-butanol-ethanol fermentation for hyper n-butanol production. Biotechnol Bioeng 113(1):120–129CrossRefGoogle Scholar
  117. Yentekakis IV, Goula G (2017) Biogas management: advanced utilization for production of renewable energy and added-value chemicals. Front Environ Sci 5:7Google Scholar
  118. Young J, Chung D, Bomble Y, Himmel M, Westpheling J (2014) Deletion of Caldicellulosiruptor bescii CelA reveals its crucial role in the deconstruction of lignocellulosic biomass. Biotechnol Biofuels 7(1):142CrossRefGoogle Scholar
  119. Yun Y-M, Kim D-H, Cho S-K, Shin H-S, Jung K-W, Kim H-W (2016) Mitigation of ammonia inhibition by internal dilution in high-rate anaerobic digestion of food waste leachate and evidences of microbial community response. Biotechnol Bioeng 113(9):1892–1901CrossRefGoogle Scholar
  120. Zamanzadeh M, Hagen LH, Svensson K, Linjordet R, Horn SJ (2016) Anaerobic digestion of food waste – effect of recirculation and temperature on performance and microbiology. Water Res 96:246–254CrossRefGoogle Scholar
  121. Zhang P, Chen Y, Zhou Q (2009) Waste activated sludge hydrolysis and short-chain fatty acids accumulation under mesophilic and thermophilic conditions: effect of pH. Water Res 43(15):3735–3742CrossRefGoogle Scholar
  122. Zhang P, Chen Y, Zhou Q, Zheng X, Zhu X, Zhao Y (2010) understanding short-chain fatty acids accumulation enhanced in waste activated sludge alkaline fermentation: kinetics and microbiology. Environ Sci Technol 44(24):9343–9348CrossRefGoogle Scholar
  123. Zhang Y, Pinoy L, Meesschaert B, Van der Bruggen B (2011) Separation of small organic ions from salts by ion-exchange membrane in electrodialysis. AIChE J 57(8):2070–2078CrossRefGoogle Scholar
  124. Zhang F, Zhang Y, Chen M, Zeng RJ (2012) Hydrogen supersaturation in thermophilic mixed culture fermentation. Int J Hydrogen Energy 37(23):17809–17816CrossRefGoogle Scholar
  125. Zhang F, Ding J, Shen N, Zhang Y, Ding Z-W, Dai K, Zeng RJ (2013a) In situ hydrogen utilization for high fraction acetate production in mixed culture hollow-fiber membrane biofilm reactor. Appl Microbiol Biotechnol 97(23):10233–10240CrossRefGoogle Scholar
  126. Zhang F, Ding J, Zhang Y, Chen M, Ding Z-W, van Loosdrecht MCM, Zeng RJ (2013b) Fatty acids production from hydrogen and carbon dioxide by mixed culture in the membrane biofilm reactor. Water Res 47(16):6122–6129CrossRefGoogle Scholar
  127. Zhang F, Zhang Y, Chen M, van Loosdrecht MCM, Zeng RJ (2013c) A modified metabolic model for mixed culture fermentation with energy conserving electron bifurcation reaction and metabolite transport energy. Biotechnol Bioeng 110(7):1884–1894CrossRefGoogle Scholar
  128. Zhang Y, Zhang F, Chen M, Chu P-N, Ding J, Zeng RJ (2013d) Hydrogen supersaturation in extreme-thermophilic (70°C) mixed culture fermentation. Appl Energy 109:213–219CrossRefGoogle Scholar
  129. Zhang F, Chen Y, Dai K, Zeng R (2014a) The chemostat study of metabolic distribution in extreme-thermophilic (70 °C) mixed culture fermentation. Appl Microbiol Biotechnol 98(24):10267–10273CrossRefGoogle Scholar
  130. Zhang F, Zhang Y, Ding J, Dai K, van Loosdrecht MCM, Zeng RJ (2014b) Stable acetate production in extreme-thermophilic (70°C) mixed culture fermentation by selective enrichment of hydrogenotrophic methanogens. Sci Rep 4:5268CrossRefGoogle Scholar
  131. Zhang F, Chen Y, Dai K, Shen N, Zeng RJ (2015a) The glucose metabolic distribution in thermophilic (55 °C) mixed culture fermentation: a chemostat study. Int J Hydrogen Energy 40(2):919–926CrossRefGoogle Scholar
  132. Zhang F, Zhang Y, Chen Y, Dai K, van Loosdrecht MCM, Zeng RJ (2015b) Simultaneous production of acetate and methane from glycerol by selective enrichment of hydrogenotrophic methanogens in extreme-thermophilic (70 °C) mixed culture fermentation. Appl Energy 148:326–333CrossRefGoogle Scholar
  133. Zhang F, Yang J-H, Dai K, Ding Z-W, Wang L-G, Li Q-R, Gao F-M, Zeng RJ (2016) Microbial dynamics of the extreme-thermophilic (70 °C) mixed culture for hydrogen production in a chemostat. Int J Hydrogen Energy 41(26):11072–11080CrossRefGoogle Scholar
  134. Zheng H, O’Sullivan C, Mereddy R, Zeng RJ, Duke M, Clarke WP (2010) Experimental and theoretical investigation of diffusion processes in a membrane anaerobic reactor for bio-hydrogen production. Int J Hydrogen Energy 35(11):5301–5311CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Fujian Provincial Key Laboratory of Soil Environmental Health and RegulationCollege of Resources and Environment, Fujian Agriculture and Forestry UniversityFuzhouChina

Personalised recommendations