Production of chemicals from C1 gases (CO, CO2) by Clostridium carboxidivorans

  • Ánxela Fernández-Naveira
  • Haris Nalakath Abubackar
  • María C. Veiga
  • Christian Kennes


Bioprocesses in conventional second generation biorefineries are mainly based on the fermentation of sugars obtained from lignocellulosic biomass or agro-industrial wastes. An alternative to this process consists in gasifying those same feedstocks or even other carbon-containing materials to obtain syngas which can also be fermented by some anaerobic bacteria to produce chemicals or fuels. Carbon monoxide, carbon dioxide and hydrogen, which are the main components of syngas, are also found in some industrial waste gases, among others in steel industries. Clostridium carboxidivorans is able to metabolise such gases to produce ethanol and higher alcohols, i.e. butanol and hexanol, following the Wood–Ljungdahl pathway. This does simultaneously allow the removal of volatile pollutants involved in climate change. The bioconversion is a two step process in which organic acids (acetate, butyrate, hexanoate) are produced first, followed by the accumulation of alcohols; although partial overlap in time of acids and alcohols production may sometimes take place as well. Several parameters, among others pH, temperature, or gas-feed flow rates in bioreactors, affect the bioconversion process. Besides, the accumulation of high concentrations of alcohols in the fermentation broth inhibits the growth and metabolic activity of C. carboxidivorans.


Acetogens Clostridia Greenhouse gases Syngas Waste gas 



The authors thank Prof. I. Maddox and the WJMB for inviting them to prepare this manuscript. AFN acknowledges a pre-doctoral fellowship from the Xunta de Galicia (Spain).


  1. Abdehagh N, Tezel FH, Thibault J (2014) Separation techniques in butanol production: challenges and developments. Biomass Bioenerg 60:222–246CrossRefGoogle Scholar
  2. Abubackar HN, Veiga MC, Kennes C (2011) Biological conversion of carbon monoxide-rich syngas or waste gases to bioethanol. Biofuels Bioprod Biorefin 5:93–114CrossRefGoogle Scholar
  3. Abubackar HN, Veiga MC, Kennes C (2015) Carbon monoxide fermentation to ethanol by Clostridium autoethanogenum in a bioreactor with no accumulation of acetic acid. Bioresour Technol 186:122–127CrossRefGoogle Scholar
  4. Ahmed A, Cateni BG, Huhnke RL, Lewis RS (2006) Effects of biomass-generated producer gas constituents on cell growth, product distribution and hydrogenase activity of Clostridium carboxidivorans P7(T). Biomass Bioenerg 30:665–667Google Scholar
  5. Bruant G, Lévesque MJ, Peter C, Guiot SR, Masson L (2010) Genomic analysis of carbon monoxide utilization and butanol production by Clostridium carboxidivorans strain P7T. PLoS One 5:13033CrossRefGoogle Scholar
  6. Cotter JL, Chinn MS, Grunden AM (2009) Ethanol and acetate production by Clostridium ljungdahlii and Clostridium autoethanogenum using resting cells. Bioprocess Biosyst Eng 32:369–380CrossRefGoogle Scholar
  7. de Klerk A, Li Y-W, Zennaro R (2013) Fischer-tropch technology (Chap 3). In: Maitlis PM, de Klerk A (eds) Greener Fischer–Tropsch processes for fuels and feedstocks. Wiley-VCH, Weinheim, pp 53–79CrossRefGoogle Scholar
  8. Drake HL, Gossner AS, Daniel SL (2008) Old acetogens, new light. Ann NY Acad Sci 1125:100–128CrossRefGoogle Scholar
  9. Dürre P (2016) Butanol formation from gaseous substrates. FEMS Microbiol Lett 363:1–7CrossRefGoogle Scholar
  10. Dürre P, Hollergschwandner C (2004) Initiation of endospore formation in Clostridium acetobutylicum. Anaerobe 10:69–74CrossRefGoogle Scholar
  11. Dürre P, Fischer R-J, Kuhn A, Lorenz K, Schreiber W, Sturzenhofecker B, Ullmann S, Winzer K, Sauer U (1995) Solventogenic enzymes of Clostridium acetobutylicum: catalytic properties, genetic organization, and transcriptional regulation. FEMS Microbiol Rev 17:251–262CrossRefGoogle Scholar
  12. Fernández-Naveira Á, Abubackar HN, Veiga MC, Kennes C (2016a) Efficient butanol–ethanol (B–E) production from carbon monoxide fermentation in Clostridium carboxidivorans. Appl Microbiol Biotechnol 100:3361–3370Google Scholar
  13. Fernández-Naveira Á, Abubackar HN, Veiga MC, Kennes C (2016b) Carbon monoxide bioconversion to butanol-ethanol by Clostridium carboxidivorans: kinetics and toxicity of alcohols. Appl Microbiol Biotechnol 100:4231–4240Google Scholar
  14. Fernández-Naveira Á, Veiga MC, Kennes C Production of higher alcohols through anaerobic H–B–E fermentation of syngas or waste gas (submitted)Google Scholar
  15. Gößner AS, Picardal F, Tanner RS, Drake HL (2008) Carbon metabolism of the moderately acid-tolerant acetogen Clostridium drakei isolated from peat. FEMS Microbiol Lett 287:236–242CrossRefGoogle Scholar
  16. Gowen CM, Fong SS (2011) Applications of systems biology towards microbial fuel production. Trends Microbiol 10:516–524CrossRefGoogle Scholar
  17. Guedon E, Payot S, Desvaux M, Petitdemange H (1999) Carbon and electron flow in Clostridium cellulolyticum grown in chemostat culture on synthetic medium. J Bacteriol 181:3262–3269Google Scholar
  18. Haryanto A, Fernando SD, Pordesimo LO and Adhikari S. 2009. Upgrading of syngas derived from biomass gasification: a thermodynamic analysis. Biomass Bioenerg 33:882–889CrossRefGoogle Scholar
  19. Heiskanen H, Virkajärvi I, Viikari L (2007) The effect of syngas composition on the growth and product formation of Butyribacterium methylotrophicum. Enzyme Microb Tech 41:362–367CrossRefGoogle Scholar
  20. Hemme CL, Mouttaki H, Lee Y-J, Zhang G, Goodwin L, Lucas S, Copeland A, Lapidus A, Glavina del Rio T, Tice H, Saunders E, Brettin T, Detter JC, Han CS, Pitluck S, Land ML, Hauser LJ, Kyrpides N, Mikhailova N, He Z, Wu L, Van Nostrand JD, Henrissat B, He Q, Lawson PA, Tanner RS, Lynd LR, Wiegel J, Fields MW, Arkin AP, Schadt CW, Stevenson BS, McInerney MJ, Yang Y, Dong H, Xing D, Ren N, Wang A, Huhnke RL, Mielenz JR, Ding S-Y, Himmel ME, Taghavi S, van der Lelie D, Rubin EM, Zhou J (2010) Sequencing of multiple clostridial genomes related to biomass conversion and biofuel production. J Bacteriol 192:6494–6496CrossRefGoogle Scholar
  21. Jansen M, Hansen TA (2001) Non-growth-associated demethylation of dimethylsulfonopropionate by (homo)acetogenic bacteria. Appl Environ Microbiol 67:300–306CrossRefGoogle Scholar
  22. Jeong J, Bertsch J, Hess V, Choi S, Choi I-G, Chang IS, Volker M (2015) Energy conservation model based on genomic and experimental analyses of a carbon monoxide-utilizing, butyrate-forming acetogen, Eubacterium limosum KIST612. Appl Environ Microbiol 84:4782–4790Google Scholar
  23. Jin Y, Guo L, Veiga MC, Kennes C (2009) Optimization of the treatment of carbon monoxide-polluted air in biofilters. Chemosphere 74:332–337CrossRefGoogle Scholar
  24. Kane MD, Breznak (1991) Acetonema longum gen. Nov. Sp. Nov., and H2/CO2 acetogenic bacterium from the termite, Pterotermes occidentis. Arch Microbiol 156:91–98CrossRefGoogle Scholar
  25. Kennes C, Rene E, Veiga MC (2009) Bioprocesses for air pollution control. J Chem Technol Bioetchnol 84:1419–1436CrossRefGoogle Scholar
  26. Kennes D, Abubackar HN, Diaz M, Veiga MC, Kennes C (2016) Bioethanol production from biomass: carbohydrate vs syngas fermentation. J Chem Technol Bioetchnol 91:304–317CrossRefGoogle Scholar
  27. Klasson KT, Ackerson CMD, Clausen EC, Gaddy JL (1993) Biological conversion of coal and coal-derived synthesis gas. Fuel 72:1673–1678CrossRefGoogle Scholar
  28. Köpke M, Liew FM (2011) Recombinant microorganism and methods of production thereof. Patent US 20110236941 A1Google Scholar
  29. Köpke M, Straub M, Dürre P (2013) Clostridium difficileis an autotrophic bacterialpathogen. PLoS One 8(4):e62157CrossRefGoogle Scholar
  30. Krasna AI (1979) Hydrogenase: properties and applications. Enzyme Microb Tech 1(3):165–172CrossRefGoogle Scholar
  31. Kubiak AM, Minton NP (2015) The potential of clostridial spores as therapeutic delivery vehicles in tumor therapy. Res Microbiol 166:244–254CrossRefGoogle Scholar
  32. Küsel K, Dorsch T, Acker G, Stackebrandt E, Drake HL (2000) Clostridium scatologenes strain SL1 isolated as an acetogenic bacterium from acidic sediments. Int J Syst Evol Microbiol 50:537–546CrossRefGoogle Scholar
  33. 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. 27:79–87CrossRefGoogle Scholar
  34. Liew F, Martin ME, Tappel RC, Heijstra BD, Mihalcea C, Köpke M (2016) Gas fermentation—a flexible platform for commercial scale production of low-carbon-fuels and chemicals from waste and renewable feedstocks. Front Microb 7:694CrossRefGoogle Scholar
  35. 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 55:2085–2091CrossRefGoogle Scholar
  36. Liu K, Atiyeh HK, Tanner RS, Wilkins MR, Huhnke RL (2012) Fermentative production of ethanol from syngas using novel moderately alkaliphilic strains of Alkalibaculum bacchii. Bioresour Technol 104:336–341CrossRefGoogle Scholar
  37. 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 152:337–346CrossRefGoogle Scholar
  38. Maddox IS, Steiner E, Hirsch S, Wessner S, Gutierrez NA, Gapes JR, Schuster KC (2000) The cause of ‘‘acid-crash’’ and ‘‘acidogenic fermentations’’ during the batch acetone-butanol-ethanol (ABE-) fermentation process. J Mol Microbiol Biotechnol 2:95–100Google Scholar
  39. Meyer CL, Papoutsakis ET (1989) Increased levels of ATP and NADH are associated with increased solvent production in continuous cultures of Clostridium acetobutylicum. Appl Microbiol Biotechnol 30: 450–459Google Scholar
  40. Michael K, Steffi N, Peter D (2011) The past, present, and future of biofuels–biobutanol as promising alternative. In: dos Santos Bernades MA (ed) Biofuel production-recent developments and prospects. InTech, Rijeka, pp 451–486Google Scholar
  41. Mohammadi M, Najafpour GD, Younesi H, Lahijani P, Uzir MH, Mohamed AR (2011) Bioconversion of synthesis gas to second generation biofuels: a review. Renew Sustain Energy Rev 15:4255–4257CrossRefGoogle Scholar
  42. 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 190:114–121CrossRefGoogle Scholar
  43. Ragsdale SW, Pierce E (2008) Acetogenesis and the Wood–Ljungdahl pathway of CO(2) fixation. Biochim Biophys Acta. 1784:1873–1898CrossRefGoogle Scholar
  44. Ramió-Pujol S, Bañeras L, Ganigué R Colprim J (2015) Impact of formate on the growth and productivity of Clostridium ljungdahlii PETC and Clostridium carboxidivorans P7 grown on syngas. Int Microbiol 17:195–204Google Scholar
  45. Richter H, Molitor B, Wei H, Chen W, Aristilde L, Angenent LT (2016) Ethanol production in syngas-fermenting Clostridium ljungdahlii is controlled by thermodynamics rather than by enzyme expression. Energy Environ Sci 9:2392CrossRefGoogle Scholar
  46. Shen GJ, Shieh JS, Grethlein AJ, Jain MK, Zeikus JH (1999) Biochemical basis for carbon monoxide tolerance and butanol production by Butyribacterium methylotrophicum. Appl Microbiol Biotechnol 51:827–832CrossRefGoogle Scholar
  47. Ukpong MN, Atiyeh HK, De Lorme MJM, Liu K (2012) Physiological response of Clostridium carboxidivorans during conversion of synthesis gas to solvents in a gas-fed bioreactor. Biotechnol Bioeng 109:2720–2728CrossRefGoogle Scholar
  48. Van Groenestijn JW, Abubackar HN, Veiga MC, Kennes C (2013) Bioethanol (Chap. 18). In: Kennes C, Veiga MC (eds) Air pollution prevention and control: bioreactors and bioenergy. Wiley, Chichester, pp 431–463CrossRefGoogle Scholar
  49. Xu D, Lewis RS (2012) Syngas fermentation to biofuels: effects of ammonia impurity in raw syngas on hydrogenase activity. Biomass Bioenerg 45:303–310Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Ánxela Fernández-Naveira
    • 1
  • Haris Nalakath Abubackar
    • 1
  • María C. Veiga
    • 1
  • Christian Kennes
    • 1
  1. 1.Chemical Engineering Laboratory, Faculty of Sciences and Center for Advanced Scientific Research (CICA)University of La CoruñaLa CoruñaSpain

Personalised recommendations