Applied Microbiology and Biotechnology

, Volume 103, Issue 21–22, pp 8689–8709 | Cite as

Syngas-aided anaerobic fermentation for medium-chain carboxylate and alcohol production: the case for microbial communities

  • Flávio C. F. Baleeiro
  • Sabine Kleinsteuber
  • Anke Neumann
  • Heike SträuberEmail author


Syngas fermentation has been successfully implemented in commercial-scale plants and can enable the biochemical conversion of the driest fractions of biomass through synthesis gas (H2, CO2, and CO). The process relies on optimized acetogenic strains able to reach and maintain high productivity of ethanol and acetate. In parallel, microbial communities have shown to be the best choice for the production of valuable medium-chain carboxylates through anaerobic fermentation of biomass, demanding low technical complexity and being able to realize simultaneous hydrolysis of the substrate. Each of the two technologies benefits from different strong points and has different challenges to overcome. This review discusses the rationales for merging these two seemingly disparate technologies by analyzing previous studies and drawing opinions based on the lessons learned from such studies. For keeping the technical demands of the resulting process low, a case is built for using microbial communities instead of pure strains. For that to occur, a shift from conventional syngas-based to “syngas-aided” anaerobic fermentation is suggested. Strategies for tackling the intricacies of working simultaneously with communities and syngas, such as competing pathways, and thermodynamic aspects are discussed as well as the stoichiometry and economic feasibility of the concept. Overall, syngas-aided anaerobic fermentation seems to be a promising concept for the biorefinery of the future. However, the effects of process parameters on microbial interactions have to be understood in greater detail, in order to achieve and sustain feasible medium-chain carboxylate and alcohol productivity.


Chain elongation Biorefinery Syngas fermentation Reverse beta-oxidation Open culture Acetogenesis 


Funding information

The study was funded by the Helmholtz Association, Research Program Renewable Energies. Financial support was also received from the CAPES – Brazilian Federal Agency for Support and Evaluation of Graduate Education within the Ministry of Education of Brazil (No. 88887.163504/2018-00) and from the BMBF - German Federal Ministry of Education and Research (No. 01DQ17016).

Compliance with ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Agler MT, Werner JJ, Iten LB, Dekker A, Cotta MA, Dien BS, Angenent LT (2012) Shaping reactor microbiomes to produce the fuel precursor n-butyrate from pretreated cellulosic hydrolysates. Environ Sci Technol 46(18):10229–10238.
  2. Agler MT, Spirito CM, Usack JG, Werner JJ, Angenent LT (2014) Development of a highly specific and productive process for n-caproic acid production: applying lessons from methanogenic microbiomes. Water Sci Technol 69(1):62–68. CrossRefGoogle Scholar
  3. Angenent LT, Richter H, Buckel W, Spirito CM, Steinbusch KJ, Plugge CM, Strik DP, Grootscholten TI, Buisman CJ, Hamelers HV (2016) Chain elongation with reactor microbiomes: open-culture biotechnology to produce biochemicals. Environ Sci Technol 50(6):2796–2810. CrossRefPubMedGoogle Scholar
  4. Arslan D, Steinbusch KJ, Diels L, De Wever H, Buisman CJ, Hamelers HV (2012) Effect of hydrogen and carbon dioxide on carboxylic acids patterns in mixed culture fermentation. Bioresour Technol 118:227–234. CrossRefPubMedGoogle Scholar
  5. Arslan D, Steinbusch KJJ, Diels L, Hamelers HVM, Strik DPBTB, Buisman CJN, De Wever H (2016) Selective short-chain carboxylates production: a review of control mechanisms to direct mixed culture fermentations. Crit Rev Environ Sci Technol 46(6):592–634. CrossRefGoogle Scholar
  6. Asimakopoulos K, Gavala HN, Skiadas IV (2018) Reactor systems for syngas fermentation processes: a review. Chem Eng J 348:732–744. CrossRefGoogle Scholar
  7. Bengelsdorf FR, Dürre P (2017) Gas fermentation for commodity chemicals and fuels. Microb Biotechnol 10(5):1167–1170. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bengelsdorf FR, Beck MH, Erz C, Hoffmeister S, Karl MM, Riegler P, Wirth S, Poehlein A, Weuster-Botz D, Dürre P (2018) Bacterial anaerobic synthesis gas (syngas) and CO2+H2 fermentation. Adv Appl Microbiol 103:143–221. CrossRefPubMedGoogle Scholar
  9. Biddy MJ, Scarlata C, Kinchin C (2016) Chemicals from biomass: a market assessment of bioproducts with near-term potential. National Renewable Energy Lab (NREL), Golden, CO (United States)Google Scholar
  10. Björnsson L, Murto M, Mattiasson B (2000) Evaluation of parameters for monitoring an anaerobic co-digestion process. Appl Microbiol Biotechnol 54(6):844–849CrossRefGoogle Scholar
  11. Buckel W, Thauer RK (2013) Energy conservation via electron bifurcating ferredoxin reduction and proton/Na(+) translocating ferredoxin oxidation. Biochim Biophys Acta 1827(2):94–113. CrossRefPubMedGoogle Scholar
  12. Cavalcante WA, Leitão RC, Gehring TA, Angenent LT, Santaella ST (2017) Anaerobic fermentation for n-caproic acid production: a review. Process Biochem 54:106–119. CrossRefGoogle Scholar
  13. Chahal SP, Starr J (2006) Lactic Acid, Ullmann’s Encyclopedia of Industrial Chemistry. Wiley-VCH, GmbH & Co. KGaA, WeinheimGoogle Scholar
  14. Chakraborty S, Rene ER, Lens PNL, Veiga MC, Kennes C (2019) Enrichment of a solventogenic anaerobic sludge converting carbon monoxide and syngas into acids and alcohols. Bioresour Technol 272:130–136. CrossRefPubMedGoogle Scholar
  15. Chapleur O, Madigou C, Civade R, Rodolphe Y, Mazeas L, Bouchez T (2016) Increasing concentrations of phenol progressively affect anaerobic digestion of cellulose and associated microbial communities. Biodegradation 27(1):15–27. CrossRefPubMedGoogle Scholar
  16. Chen WS, Ye Y, Steinbusch KJJ, Strik DPBTB, Buisman CJN (2016) Methanol as an alternative electron donor in chain elongation for butyrate and caproate formation. Biomass Bioenergy 93:201–208. CrossRefGoogle Scholar
  17. Chen WS, Strik D, Buisman CJN, Kroeze C (2017) Production of caproic acid from mixed organic waste: an environmental life cycle perspective. Environ Sci Technol 51(12):7159–7168. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Costa KC, Leigh JA (2014) Metabolic versatility in methanogens. Curr Opin Biotechnol 29:70–75. CrossRefPubMedGoogle Scholar
  19. Cueto-Rojas HF, van Maris AJ, Wahl SA, Heijnen JJ (2015) Thermodynamics-based design of microbial cell factories for anaerobic product formation. Trends Biotechnol 33(9):534–546. CrossRefPubMedGoogle Scholar
  20. De Groof V, Coma M, Arnot T, Leak DJ, Lanham AB (2019) Medium chain carboxylic acids from complex organic feedstocks by mixed culture fermentation. Molecules 24(3). CrossRefGoogle Scholar
  21. de Jong E, Higson A, Walsh P, Wellisch M (2012) Bio-based chemicals value added products from biorefineries. IEA Bioenergy, Task42 Biorefinery:34Google Scholar
  22. de Kok S, Meijer J, van Loosdrecht MC, Kleerebezem R (2013) Impact of dissolved hydrogen partial pressure on mixed culture fermentations. Appl Microbiol Biotechnol 97(6):2617–2625. CrossRefPubMedGoogle Scholar
  23. de Leeuw K, Buisman CJN, Strik DPBTB (2019) Branched medium chain fatty acids: iso-caproate formation from iso-butyrate broadens the product spectrum for microbial chain elongation. Environ Sci Technol 53:7704–7713. CrossRefPubMedPubMedCentralGoogle Scholar
  24. de Medeiros EM, Posada JA, Noorman H, Osseweijer P, Filho RM (2017) Hydrous bioethanol production from sugarcane bagasse via energy self-sufficient gasification-fermentation hybrid route: Simulation and financial analysis. J Clean Prod 168:1625–1635. CrossRefGoogle Scholar
  25. de S Dias MO, Maciel Filho R, Mantelatto PE, Cavalett O, Rossell CEV, Bonomi A, Leal MRLV (2015) Sugarcane processing for ethanol and sugar in Brazil. Environ Dev 15:35–51. CrossRefGoogle Scholar
  26. de Smit SM, de Leeuw KD, Buisman CJN, Strik D (2019) Continuous n-valerate formation from propionate and methanol in an anaerobic chain elongation open-culture bioreactor. Biotechnol Biofuels 12:132.
  27. de Vrieze J, Coma M, Debeuckelaere M, Van der Meeren P, Rabaey K (2016) High salinity in molasses wastewaters shifts anaerobic digestion to carboxylate production. Water Res 98:293–301. CrossRefPubMedGoogle Scholar
  28. Diamond LW, Akinfiev NN (2003) Solubility of CO2 in water from −1.5 to 100 °C and from 0.1 to 100 MPa: evaluation of literature data and thermodynamic modelling. Fluid Phase Equilib 208(1-2):265–290. CrossRefGoogle Scholar
  29. Diender M, Stams AJ, Sousa DZ (2015) Pathways and bioenergetics of anaerobic carbon monoxide fermentation. Front Microbiol 6:1275. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Diender M, Stams AJ, Sousa DZ (2016) Production of medium-chain fatty acids and higher alcohols by a synthetic co-culture grown on carbon monoxide or syngas. Biotechnol Biofuels 9:82. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Ding HB, Tan GY, Wang JY (2010) Caproate formation in mixed-culture fermentative hydrogen production. Bioresour Technol 101(24):9550–9559. CrossRefPubMedGoogle Scholar
  32. DOE (2016) Biomass for electricity generation. United States Department of Energy. Accessed 25 Jan 2019
  33. Doud DFR, Holmes EC, Richter H, Molitor B, Jander G, Angenent LT (2017) Metabolic engineering of Rhodopseudomonas palustris for the obligate reduction of n-butyrate to n-butanol. Biotechnol Biofuels 10:178.
  34. Endres H-J, Siebert-Raths A (2009) Technische Biopolymere. Rahmenbedingungen, Marktsituation, Herstellung, Aufbau und Eigenschaften 1st edn München: HanserCrossRefGoogle Scholar
  35. Esquivel-Elizondo S, Delgado AG, Rittmann BE, Krajmalnik-Brown R (2017) The effects of CO2 and H2 on CO metabolism by pure and mixed microbial cultures. Biotechnol Biofuels 10:220. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Esquivel-Elizondo S, Miceli J 3rd, Torres CI, Krajmalnik-Brown R (2018) Impact of carbon monoxide partial pressures on methanogenesis and medium chain fatty acids production during ethanol fermentation. Biotechnol Bioeng 115(2):341–350. CrossRefPubMedGoogle Scholar
  37. Fernández-Naveira Á, Abubackar HN, Veiga MC, Kennes C (2016) Efficient butanol-ethanol (B-E) production from carbon monoxide fermentation by Clostridium carboxidivorans. Appl Microbiol Biotechnol 100(7):3361–3370. CrossRefPubMedGoogle Scholar
  38. Fernández-Naveira Á, Veiga MC, Kennes C (2017) H-B-E (hexanol-butanol-ethanol) fermentation for the production of higher alcohols from syngas/waste gas. J Chem Technol Biotechnol 92(4):712–731. CrossRefGoogle Scholar
  39. Fernández-Naveira Á, Veiga MC, Kennes C (2019) Selective anaerobic fermentation of syngas into either C2-C6 organic acids or ethanol and higher alcohols. Bioresour Technol 280:387–395. CrossRefPubMedGoogle Scholar
  40. Ganigué R, Ramió-Pujol S, Sanchez P, Baneras L, Colprim J (2015) Conversion of sewage sludge to commodity chemicals via syngas fermentation. Water Sci Technol 72(3):415–420. CrossRefPubMedGoogle Scholar
  41. Ganigué R, Sánchez-Paredes P, Bañeras L, Colprim J (2016) Low fermentation pH is a trigger to alcohol production, but a killer to chain elongation. Front Microbiol 7:702. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Garvie EI (1980) Bacterial lactate dehydrogenases. Microbiol Rev 44(1):106PubMedPubMedCentralGoogle Scholar
  43. Ge S, Usack JG, Spirito CM, Angenent LT (2015) Long-term n-caproic acid production from yeast-fermentation beer in an anaerobic bioreactor with continuous product extraction. Environ Sci Technol 49(13):8012–8021. CrossRefPubMedGoogle Scholar
  44. Gildemyn S, Molitor B, Usack JG, Nguyen M, Rabaey K, Angenent LT (2017) Upgrading syngas fermentation effluent using Clostridium kluyveri in a continuous fermentation. Biotechnol Biofuels 10:83. CrossRefPubMedPubMedCentralGoogle Scholar
  45. González-Cabaleiro R, Lema JM, Rodríguez J, Kleerebezem R (2013) Linking thermodynamics and kinetics to assess pathway reversibility in anaerobic bioprocesses. Energy Environ Sci 6(12):3780. CrossRefGoogle Scholar
  46. González-Cabaleiro R, Lema JM, Rodríguez J (2015) Metabolic energy-based modelling explains product yielding in anaerobic mixed culture fermentations. PLoS One 10(5):e0126739. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Granda CB Production of highly pure fatty acids from anaerobic digestion. In: World Congress on Industrial Biotechnology, Montréal, 2015Google Scholar
  48. Greenwood NN, Earnshaw A (2012) Chemistry of the Elements. ElsevierGoogle Scholar
  49. Grimalt-Alemany A, Lezyk M, Lange L, Skiadas IV, Gavala HN (2018) Enrichment of syngas-converting mixed microbial consortia for ethanol production and thermodynamics-based design of enrichment strategies. Biotechnol Biofuels 11(1):198. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Grootscholten TI, Steinbusch KJ, Hamelers HV, Buisman CJ (2013) Improving medium chain fatty acid productivity using chain elongation by reducing the hydraulic retention time in an upflow anaerobic filter. Bioresour Technol 136:735–738. CrossRefPubMedGoogle Scholar
  51. Grootscholten TIM, Strik DPBTB, Steinbusch KJJ, Buisman CJN, Hamelers HVM (2014) Two-stage medium chain fatty acid (MCFA) production from municipal solid waste and ethanol. Appl Energy 116:223–229. CrossRefGoogle Scholar
  52. Guiot SR, Cimpoia R, Carayon G (2011) Potential of wastewater-treating anaerobic granules for biomethanation of synthesis gas. Environ Sci Technol 45(5):2006–2012. CrossRefPubMedGoogle Scholar
  53. He P, Han W, Shao L, Lu F (2018) One-step production of C6-C8 carboxylates by mixed culture solely grown on CO. Biotechnol Biofuels 11:4. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Heimann A, Jakobsen R, Blodau C (2009) Energetic constraints on H2-dependent terminal electron accepting processes in anoxic environments: a review of observations and model approaches. Environ Sci Technol 44(1):24–33CrossRefGoogle Scholar
  55. Hu Y, Jing Z, Sudo Y, Niu Q, Du J, Wu J, Li YY (2015) Effect of influent COD/SO42- ratios on UASB treatment of a synthetic sulfate-containing wastewater. Chemosphere 130:24–33. CrossRefPubMedGoogle Scholar
  56. Jankowska E, Duber A, Chwialkowska J, Stodolny M, Oleskowicz-Popiel P (2018) Conversion of organic waste into volatile fatty acids – the influence of process operating parameters. Chem Eng J 345:395–403. CrossRefGoogle Scholar
  57. Jaros A, Rova U, Berglund K (2012) Effect of acetate on fermentation production of butyrate. Cellul Chem Technol 46(5-6):341–347Google Scholar
  58. Jeon BS, Choi O, Um Y, Sang BI (2016) Production of medium-chain carboxylic acids by Megasphaera sp. MH with supplemental electron acceptors. Biotechnol Biofuels 9:129. CrossRefPubMedPubMedCentralGoogle Scholar
  59. Jourdin L, Raes SMT, Buisman CJN, Strik DPBTB (2018) Critical biofilm growth throughout unmodified carbon felts allows continuous bioelectrochemical chain elongation from CO2 up to caproate at high current density. Front Energy Res 6.
  60. Kenealy WR, Waselefsky DM (1985) Studies on the substrate range of Clostridium kluyveri; the use of propanol and succinate. Arch Microbiol 141(3):187–194CrossRefGoogle Scholar
  61. Kleerebezem R, Stams AJ (2000) Kinetics of syntrophic cultures: a theoretical treatise on butyrate fermentation. Biotechnol Bioeng 67(5):529–543CrossRefGoogle Scholar
  62. Kleerebezem R, van Loosdrecht MC (2007) Mixed culture biotechnology for bioenergy production. Curr Opin Biotechnol 18(3):207–212. CrossRefPubMedGoogle Scholar
  63. Kleerebezem R, Van Loosdrecht MCM (2010) A generalized method for thermodynamic state analysis of environmental systems. Crit Rev Environ Sci Technol 40(1):1–54. CrossRefGoogle Scholar
  64. Köpke M, Held C, Hujer S, Liesegang H, Wiezer A, Wollherr A, Ehrenreich A, Liebl W, Gottschalk G, Dürre P (2010) Clostridium ljungdahlii represents a microbial production platform based on syngas. Proc Natl Acad Sci U S A 107(29):13087–13092. CrossRefPubMedPubMedCentralGoogle Scholar
  65. Kosaric N, Duvnjak Z, Farkas A, Sahm H, Bringer-Meyer S, Goebel O, Mayer D (2000) Ethanol. In: Ullmann’s encyclopedia of industrial chemistry. Wiley-VCH, GmbH & Co. KGaA, WeinheimGoogle Scholar
  66. Koster IW, Koomen E (1988) Ammonia inhibition of the maximum growth rate (μm) of hydrogenotrophic methanogens at various pH-levels and temperatures. Appl Microbiol Biotechnol 28(4-5):500–505CrossRefGoogle Scholar
  67. Kremp F, Poehlein A, Daniel R, Müller V (2018) Methanol metabolism in the acetogenic bacterium Acetobacterium woodii. Environ Microbiol 20(12):4369–4384. CrossRefGoogle Scholar
  68. Kucek LA, Nguyen M, Angenent LT (2016a) Conversion of L-lactate into n-caproate by a continuously fed reactor microbiome. Water Res 93:163–171. CrossRefPubMedGoogle Scholar
  69. Kucek LA, Spirito CM, Angenent LT (2016b) High n-caprylate productivities and specificities from dilute ethanol and acetate: chain elongation with microbiomes to upgrade products from syngas fermentation. Energy Environ Sci 9(11):3482–3494. CrossRefGoogle Scholar
  70. Kucek LA, Xu J, Nguyen M, Angenent LT (2016c) Waste conversion into n-caprylate and n-caproate: resource recovery from wine lees using anaerobic reactor microbiomes and in-line extraction. Front Microbiol 7:1892.
  71. Lambrecht J, Cichocki N, Schattenberg F, Kleinsteuber S, Harms H, Müller S, Sträuber H (2019) Key sub-community dynamics of medium-chain carboxylate production. Microb Cell Factories 18(1):92. CrossRefGoogle Scholar
  72. Latif H, Zeidan AA, Nielsen AT, Zengler K (2014) Trash to treasure: production of biofuels and commodity chemicals via syngas fermenting microorganisms. Curr Opin Biotechnol 27:79–87. CrossRefPubMedGoogle Scholar
  73. Liebetrau J, Weinrich S, Sträuber H, Kretzschmar J (2019) Anaerobic fermentation of organic material: biological processes and their control parameters. energy from organic materials (biomass). Encyclopedia of Sustainability Science and Technology Series. Springer, New York, pp 779–807CrossRefGoogle Scholar
  74. Liew F, Henstra AM, Winzer K, Köpke M, Simpson SD, Minton NP (2016a) Insights into CO2 fixation pathway of Clostridium autoethanogenum by targeted mutagenesis. MBio 7(3).
  75. Liew F, Martin ME, Tappel RC, Heijstra BD, Mihalcea C, Kopke M (2016b) Gas fermentation - a flexible platform for commercial scale production of low-carbon-fuels and chemicals from waste and renewable feedstocks. Front Microbiol 7:694. CrossRefPubMedPubMedCentralGoogle Scholar
  76. Lindley N, Loubiere P, Pacaud S, Mariotto C, Goma G (1987) Novel products of the acidogenic fermentation of methanol during growth of Eubacterium limosum in the presence of high concentrations of organic acids. Microbiology 133(12):3557–3563CrossRefGoogle Scholar
  77. Liou JS, Balkwill DL, Drake GR, Tanner RS (2005) Clostridium carboxidivorans sp. nov., a solvent-producing clostridium isolated from an agricultural settling lagoon, and reclassification of the acetogen Clostridium scatologenes strain SL1 as Clostridium drakei sp. nov. Int J Syst Evol Microbiol 55(Pt 5):2085–2091. CrossRefPubMedGoogle Scholar
  78. Liu H, Wang J, Wang A, Chen J (2011) Chemical inhibitors of methanogenesis and putative applications. Appl Microbiol Biotechnol 89(5):1333–1340. CrossRefPubMedGoogle Scholar
  79. Liu K, Atiyeh HK, Stevenson BS, Tanner RS, Wilkins MR, Huhnke RL (2014) Mixed culture syngas fermentation and conversion of carboxylic acids into alcohols. Bioresour Technol 152:337–346. CrossRefPubMedGoogle Scholar
  80. Liu C, Luo G, Wang W, He Y, Zhang R, Liu G (2018) The effects of pH and temperature on the acetate production and microbial community compositions by syngas fermentation. Fuel 224:537–544. CrossRefGoogle Scholar
  81. Marounek M, Fliegrova K, Bartos S (1989) Metabolism and some characteristics of ruminal strains of Megasphaera elsdenii. Appl Environ Microbiol 55(6):1570–1573PubMedPubMedCentralGoogle Scholar
  82. Mock J, Zheng Y, Mueller AP, Ly S, Tran L, Segovia S, Nagaraju S, Köpke M, Dürre P, Thauer RK (2015) Energy conservation associated with ethanol formation from H2 and CO2 in Clostridium autoethanogenum involving electron bifurcation. J Bacteriol 197(18):2965–2980. CrossRefPubMedPubMedCentralGoogle Scholar
  83. Molitor B, Richter H, Martin ME, Jensen RO, Juminaga A, Mihalcea C, Angenent LT (2016) Carbon recovery by fermentation of CO-rich off gases - Turning steel mills into biorefineries. Bioresour Technol 215:386–396. CrossRefPubMedGoogle Scholar
  84. Molitor B, Marcellin E, Angenent LT (2017) Overcoming the energetic limitations of syngas fermentation. Curr Opin Chem Biol 41:84–92. CrossRefPubMedGoogle Scholar
  85. Nzeteu CO, Trego AC, Abram F, O’Flaherty V (2018) Reproducible, high-yielding, biological caproate production from food waste using a single-phase anaerobic reactor system. Biotechnol Biofuels 11:108. CrossRefPubMedPubMedCentralGoogle Scholar
  86. Oswald F, Zwick M, Omar O, Hotz EN, Neumann A (2018) Growth and product formation of Clostridium ljungdahlii in presence of cyanide. Front Microbiol 9:1213. CrossRefPubMedPubMedCentralGoogle Scholar
  87. Pacaud S, Loubiere P, Goma G (1985) Methanol metabolism by Eubacterium limosum B2: Effects of pH and carbon dioxide on growth and organic acid production. Curr Microbiol 12(5):245–250CrossRefGoogle Scholar
  88. Pham V, Holtzapple M, El-Halwagi M (2010) Techno-economic analysis of biomass to fuel conversion via the MixAlco process. J Ind Microbiol Biotechnol 37(11):1157–1168. CrossRefPubMedGoogle Scholar
  89. Phillips JR, Atiyeh HK, Tanner RS, Torres JR, Saxena J, Wilkins MR, Huhnke RL (2015) Butanol and hexanol production in Clostridium carboxidivorans syngas fermentation: Medium development and culture techniques. Bioresour Technol 190:114–121. CrossRefPubMedGoogle Scholar
  90. Plugge CM, Zhang W, Scholten JC, Stams AJ (2011) Metabolic flexibility of sulfate-reducing bacteria. Front Microbiol 2:81. CrossRefPubMedPubMedCentralGoogle Scholar
  91. Popp D, Harms H, Sträuber H (2016) The alkaloid gramine in the anaerobic digestion process-inhibition and adaptation of the methanogenic community. Appl Microbiol Biotechnol 100(16):7311–7322. CrossRefPubMedGoogle Scholar
  92. Prabhu R, Altman E, Eiteman MA (2012) Lactate and acrylate metabolism by Megasphaera elsdenii under batch and steady-state conditions. Appl Environ Microbiol 78(24):8564–8570. CrossRefPubMedPubMedCentralGoogle Scholar
  93. Rabaey K, Rozendal RA (2010) Microbial electrosynthesis - revisiting the electrical route for microbial production. Nat Rev Microbiol 8(10):706–716. CrossRefPubMedGoogle Scholar
  94. Ragsdale SW (2004) Life with carbon monoxide. Crit Rev Biochem Mol Biol 39(3):165–195. CrossRefPubMedGoogle Scholar
  95. Ramachandriya KD, Kundiyana DK, Wilkins MR, Terrill JB, Atiyeh HK, Huhnke RL (2013) Carbon dioxide conversion to fuels and chemicals using a hybrid green process. Appl Energy 112:289–299. CrossRefGoogle Scholar
  96. Ramió-Pujol S, Ganigué R, Bañeras L, Colprim J (2015) Incubation at 25°C prevents acid crash and enhances alcohol production in Clostridium carboxidivorans P7. Bioresour Technol 192:296–303. CrossRefPubMedGoogle Scholar
  97. Reddy MV, ElMekawy A, Pant D (2018) Bioelectrochemical synthesis of caproate through chain elongation as a complementary technology to anaerobic digestion. Biofuels Bioprod Biorefin 12(6):966–977. CrossRefGoogle Scholar
  98. Richter H, Loftus SE, Angenent LT (2013) Integrating syngas fermentation with the carboxylate platform and yeast fermentation to reduce medium cost and improve biofuel productivity. Environ Technol 34(13-16):1983–1994. CrossRefPubMedGoogle Scholar
  99. Richter H, Molitor B, Diender M, Sousa DZ, Angenent LT (2016a) A narrow pH range supports butanol, hexanol, and octanol production from syngas in a continuous co-culture of Clostridium ljungdahlii and Clostridium kluyveri with in-line product extraction. Front Microbiol 7:1773. CrossRefPubMedPubMedCentralGoogle Scholar
  100. Richter H, Molitor B, Wei H, Chen W, Aristilde L, Angenent LT (2016b) Ethanol production in syngas-fermenting Clostridium ljungdahlii is controlled by thermodynamics rather than by enzyme expression. Energy Environ Sci 9(7):2392–2399. CrossRefGoogle Scholar
  101. Roghair M, Hoogstad T, Strik D, Plugge CM, Timmers PHA, Weusthuis RA, Bruins ME, Buisman CJN (2018a) Controlling ethanol use in chain elongation by CO2 loading rate. Environ Sci Technol 52(3):1496–1505. CrossRefPubMedPubMedCentralGoogle Scholar
  102. Roghair M, Liu Y, Adiatma JC, Weusthuis RA, Bruins ME, Buisman CJN, Strik D (2018b) Effect of n-caproate concentration on chain elongation and competing processes. ACS Sustain Chem Eng 6(6):7499–7506. CrossRefPubMedPubMedCentralGoogle Scholar
  103. Sander R (2015) Compilation of Henry's law constants (version 4.0) for water as solvent. Atmos Chem Phys 15(8):4399–4981. CrossRefGoogle Scholar
  104. Savant DV, Shouche YS, Prakash S, Ranade DR (2002) Methanobrevibacter acididurans sp. nov., a novel methanogen from a sour anaerobic digester. Int J Syst Evol Microbiol 52(Pt 4):1081–1087. CrossRefPubMedGoogle Scholar
  105. Scarborough MJ, Lawson CE, Hamilton JJ, Donohue TJ, Noguera DR (2018a) Metatranscriptomic and thermodynamic insights into medium-chain fatty acid production using an anaerobic microbiome. mSystems 3(6):e00221-18Google Scholar
  106. Scarborough MJ, Lynch G, Dickson M, McGee M, Donohue TJ, Noguera DR (2018b) Increasing the economic value of lignocellulosic stillage through medium-chain fatty acid production. Biotechnol Biofuels 11:200. CrossRefPubMedPubMedCentralGoogle Scholar
  107. Schoberth S, Gottschalk G (1969) Considerations on the energy metabolism of Clostridium kluyveri. Arch Microbiol 65(4):318–328Google Scholar
  108. Schuchmann K, Müller V (2014) Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat Rev Microbiol 12(12):809–821. CrossRefPubMedGoogle Scholar
  109. Schuchmann K, Müller V (2016) Energetics and application of heterotrophy in acetogenic bacteria. Appl Environ Microbiol 82(14):4056–4069. CrossRefPubMedPubMedCentralGoogle Scholar
  110. Seinfeld JH, Pandis SN (2016) Atmospheric chemistry and physics: from air pollution to climate change. Wiley, HobokenGoogle Scholar
  111. Shen N, Dai K, Xia X-Y, Zeng RJ, Zhang F (2018) Conversion of syngas (CO and H2) to biochemicals by mixed culture fermentation in mesophilic and thermophilic hollow-fiber membrane biofilm reactors. J Clean Prod 202:536–542. CrossRefGoogle Scholar
  112. Sikarwar VS, Zhao M, Clough P, Yao J, Zhong X, Memon MZ, Shah N, Anthony EJ, Fennell PS (2016) An overview of advances in biomass gasification. Energy Environ Sci 9(10):2939–2977. CrossRefGoogle Scholar
  113. Sipma J, Meulepas RJ, Parshina SN, Stams AJ, Lettinga G, Lens PN (2004) Effect of carbon monoxide, hydrogen and sulfate on thermophilic (55°C) hydrogenogenic carbon monoxide conversion in two anaerobic bioreactor sludges. Appl Microbiol Biotechnol 64(3):421–428. CrossRefPubMedGoogle Scholar
  114. Spirito CM, Richter H, Rabaey K, Stams AJ, Angenent LT (2014) Chain elongation in anaerobic reactor microbiomes to recover resources from waste. Curr Opin Biotechnol 27:115–122. CrossRefPubMedGoogle Scholar
  115. Steinbusch KJ, Hamelers HV, Buisman CJ (2008) Alcohol production through volatile fatty acids reduction with hydrogen as electron donor by mixed cultures. Water Res 42(15):4059–4066. CrossRefPubMedGoogle Scholar
  116. 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. Energy Environ Sci 4(1):216–224. CrossRefGoogle Scholar
  117. Sträuber H, Lucas R, Kleinsteuber S (2016) Metabolic and microbial community dynamics during the anaerobic digestion of maize silage in a two-phase process. Appl Microbiol Biotechnol 100(1):479–491. CrossRefPubMedGoogle Scholar
  118. Sträuber H, Bühligen F, Kleinsteuber S, Dittrich-Zechendorf M (2018) Carboxylic acid production from ensiled crops in anaerobic solid-state fermentation - trace elements as pH controlling agents support microbial chain elongation with lactic acid. Eng Life Sci 18(7):447–458. CrossRefGoogle Scholar
  119. Takors R, Kopf M, Mampel J, Bluemke W, Blombach B, Eikmanns B, Bengelsdorf FR, Weuster-Botz D, Dürre P (2018) Using gas mixtures of CO, CO2 and H2 as microbial substrates: the do's and don'ts of successful technology transfer from laboratory to production scale. Microb Biotechnol 11(4):606–625. CrossRefPubMedPubMedCentralGoogle Scholar
  120. Urban C, Xu J, Sträuber H, dos Santos Dantas TR, Mühlenberg J, Härtig C, Angenent LT, Harnisch F (2017) Production of drop-in fuels from biomass at high selectivity by combined microbial and electrochemical conversion. Energy Environ Sci 10(10):2231–2244. CrossRefGoogle Scholar
  121. Vassilev I, Hernández PA, Batlle-Vilanova P, Freguia S, Krömer JO, Jr K, Ledezma P, Virdis B (2018) Microbial electrosynthesis of isobutyric, butyric, caproic acids, and corresponding alcohols from carbon dioxide. ACS Sustain Chem Eng 6(7):8485–8493CrossRefGoogle Scholar
  122. Vassilev I, Kracke F, Freguia S, Keller J, Kromer JO, Ledezma P, Virdis B (2019) Microbial electrosynthesis system with dual biocathode arrangement for simultaneous acetogenesis, solventogenesis and carbon chain elongation. Chem Commun (Camb) 55(30):4351–4354. CrossRefGoogle Scholar
  123. Vasudevan D, Richter H, Angenent LT (2014) Upgrading dilute ethanol from syngas fermentation to n-caproate with reactor microbiomes. Bioresour Technol 151:378–382. CrossRefPubMedGoogle Scholar
  124. Wade WG (2015) Eubacterium. In: Whitman WB, Rainey F, Kämpfer P, Trujillo M, Chun J, DeVos P, Hedlund B, Dedysh S (eds) Bergey's Manual of Systematics of Archaea and Bacteria. CrossRefGoogle Scholar
  125. Wang H, Li X, Wang Y, Tao Y, Lu S, Zhu X, Li D (2018) Improvement of n-caproic acid production with Ruminococcaceae bacterium CPB6: selection of electron acceptors and carbon sources and optimization of the culture medium. Microb Cell Factories 17(1):99. CrossRefGoogle Scholar
  126. Weghoff MC, Bertsch J, Müller V (2015) A novel mode of lactate metabolism in strictly anaerobic bacteria. Environ Microbiol 17(3):670–677. CrossRefPubMedGoogle Scholar
  127. Weimer PJ, Moen GN (2013) Quantitative analysis of growth and volatile fatty acid production by the anaerobic ruminal bacterium Megasphaera elsdenii T81. Appl Microbiol Biotechnol 97(9):4075–4081. CrossRefPubMedGoogle Scholar
  128. Werner JJ, Knights D, Garcia ML, Scalfone NB, Smith S, Yarasheski K, Cummings TA, Beers AR, Knight R, Angenent LT (2011) Bacterial community structures are unique and resilient in full-scale bioenergy systems. Proc Natl Acad Sci U S A 108(10):4158–4163. CrossRefPubMedPubMedCentralGoogle Scholar
  129. Wu Q, Guo W, Bao X, Meng X, Yin R, Du J, Zheng H, Feng X, Luo H, Ren N (2018) Upgrading liquor-making wastewater into medium chain fatty acid: Insights into co-electron donors, key microflora, and energy harvest. Water Res 145:650–659. CrossRefPubMedGoogle Scholar
  130. Wu Q, Guo W, You S, Bao X, Luo H, Wang H, Ren N (2019) Concentrating lactate-carbon flow on medium chain carboxylic acids production by hydrogen supply. Bioresour Technol 291:121573. CrossRefPubMedGoogle Scholar
  131. Yasin M, Jeong Y, Park S, Jeong J, Lee EY, Lovitt RW, Kim BH, Lee J, Chang IS (2015) Microbial synthesis gas utilization and ways to resolve kinetic and mass-transfer limitations. Bioresour Technol 177:361–374. CrossRefPubMedGoogle Scholar
  132. Zhang F, Ding J, Zhang Y, Chen M, Ding ZW, van Loosdrecht MC, Zeng RJ (2013) Fatty acids production from hydrogen and carbon dioxide by mixed culture in the membrane biofilm reactor. Water Res 47(16):6122–6129. CrossRefPubMedGoogle Scholar
  133. Zhang J, Taylor S, Wang Y (2016) Effects of end products on fermentation profiles in Clostridium carboxidivorans P7 for syngas fermentation. Bioresour Technol 218:1055–1063. CrossRefPubMedGoogle Scholar
  134. Zhang W, Dai K, Xia XY, Wang HJ, Chen Y, Lu YZ, Zhang F, Zeng RJ (2018) Free acetic acid as the key factor for the inhibition of hydrogenotrophic methanogenesis in mesophilic mixed culture fermentation. Bioresour Technol 264:17–23. CrossRefPubMedGoogle Scholar
  135. Zhu X, Tao Y, Liang C, Li X, Wei N, Zhang W, Zhou Y, Yang Y, Bo T (2015) The synthesis of n-caproate from lactate: a new efficient process for medium-chain carboxylates production. Sci Rep 5:14360. CrossRefPubMedPubMedCentralGoogle Scholar
  136. Zhu X, Zhou Y, Wang Y, Wu T, Li X, Li D, Tao Y (2017) Production of high-concentration n-caproic acid from lactate through fermentation using a newly isolated Ruminococcaceae bacterium CPB6. Biotechnol Biofuels 10:102. CrossRefPubMedPubMedCentralGoogle Scholar
  137. Zinder SH, Anguish T, Cardwell SC (1984) Selective inhibition by 2-bromoethanesulfonate of methanogenesis from acetate in a thermophilic anaerobic digestor. Appl Environ Microbiol 47(6):1343–1345PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Environmental MicrobiologyUFZ - Helmholtz Centre for Environmental ResearchLeipzigGermany
  2. 2.Technical Biology (TeBi), Institute of Process Engineering in Life SciencesKIT - Karlsruhe Institute of TechnologyKarlsruheGermany

Personalised recommendations