Skip to main content

Continuous succinic acid production from xylose by Actinobacillus succinogenes

Bioprocess and Biosystems Engineering volume 39, pages 233–244 (2016)Cite this article

Abstract

Continuous, anaerobic fermentations of D-xylose were performed by Actinobacillus succinogenes 130Z in a custom, biofilm reactor at dilution rates of 0.05, 0.10 and 0.30 h−1. Succinic acid yields on xylose (0.55–0.68 g g−1), titres (10.9–29.4 g L−1) and productivities (1.5–3.4 g L−1 h−1) were lower than those of a previous study on glucose, but product ratios (succinic acid/acetic acid = 3.0–5.0 g g−1) and carbohydrate consumption rates were similar. Also, mass balance closures on xylose were up to 18.2 % lower than those on glucose. A modified HPLC method revealed pyruvic acid excretion at appreciable concentrations (1.2–1.9 g L−1) which improved the mass balance closure by up to 16.8 %. Furthermore, redox balances based on the accounted xylose consumed and the excreted metabolites, indicated an overproduction of reducing power. The oxidative pentose phosphate pathway was shown to be a plausible source of the additional reducing power.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Werpy T, Petersen G (2004) Top value added chemicals from biomass, volume 1. Results of screening for potential candidates from sugars and synthesis gas

  2. Lynd L, Wyman C, Gerngross T (1999) Biocommodity Engineering. Biotechnol Prog 15:777–793. doi:10.1021/bp990109e

    Article  CAS  Google Scholar 

  3. Bozell JJ, Petersen GR (2010) Technology development for the production of biobased products from biorefinery carbohydrates—the US Department of Energy’s “top 10” revisited. Green Chem 12:539. doi:10.1039/b922014c

    Article  CAS  Google Scholar 

  4. Jansen MLA, van Gulik WM (2014) Towards large scale fermentative production of succinic acid. Curr Opin Biotechnol 30C:190–197. doi:10.1016/j.copbio.2014.07.003

    Article  CAS  Google Scholar 

  5. Choi S, Woo C, Ho J, Yup S (2015) Biorefineries for the production of top building block chemicals and their derivatives. Metab Eng 1–17. doi: 10.1016/j.ymben.2014.12.007

  6. Cok B, Tsiropoulos I, Roes AL, Patel MK (2014) Succinic acid production derived from carbohydrates: an energy and greenhouse gas assessment of a platform chemical toward a bio-based economy. Biofuels Bioprod Biorefining 8:16–29. doi:10.1002/bbb.1427

    Article  CAS  Google Scholar 

  7. McKinlay JB, Vieille C, Zeikus JG (2007) Prospects for a bio-based succinate industry. Appl Microbiol Biotechnol 76:727–740. doi:10.1007/s00253-007-1057-y

    Article  CAS  Google Scholar 

  8. Zeikus JG, Jain MK, Elankovan P (1999) Biotechnology of succinic acid production and markets for derived industrial products. Appl Microbiol Biotechnol 51:545–552. doi:10.1007/s002530051431

    Article  CAS  Google Scholar 

  9. Howe-Grant M, Kroschwitz J (1991) Kirk-Othmer encyclopedia of chemical technology, 4th edn. Wiley, New York

    Google Scholar 

  10. Bechthold I, Bretz K, Kabasci S et al (2008) Succinic acid: a new platform chemical for biobased polymers from renewable resources. Chem Eng Technol 31:647–654. doi:10.1002/ceat.200800063

    Article  CAS  Google Scholar 

  11. Bradfield MFA, Nicol W (2014) Continuous succinic acid production by Actinobacillus succinogenes in a biofilm reactor: steady-state metabolic flux variation. Biochem Eng J 85:1–7. doi:10.1016/j.bej.2014.01.009

    Article  CAS  Google Scholar 

  12. Maharaj K, Bradfield MFA, Nicol W (2014) Succinic acid-producing biofilms of Actinobacillus succinogenes: reproducibility, stability and productivity. Appl Microbiol Biotechnol. doi:10.1007/s00253-014-5779-3

    Google Scholar 

  13. Yan Q, Zheng P, Tao S-T, Dong J-J (2014) Fermentation process for continuous production of succinic acid in a fibrous bed bioreactor. Biochem Eng J 91:92–98. doi:10.1016/j.bej.2014.08.002

    Article  CAS  Google Scholar 

  14. Van Heerden C, Nicol W (2013) Continuous succinic acid fermentation by Actinobacillus succinogenes. Biochem Eng J 73:5–11. doi:10.1016/j.bej.2013.01.015

    Article  CAS  Google Scholar 

  15. Lee PC, Lee SY, Chang HN (2010) Kinetic study on succinic acid and acetic acid formation during continuous cultures of Anaerobiospirillum succiniciproducens grown on glycerol. Bioprocess Biosyst Eng 33:465–471. doi:10.1007/s00449-009-0355-4

    Article  CAS  Google Scholar 

  16. Nghiem NP, Davison BH, Suttle BE, Richardson GR (1997) Production of succinic acid by Anaerobiospirillum succiniciproducens. Appl Biochem Biotechnol 63–65:565–576. doi:10.1007/BF02920454

    Article  Google Scholar 

  17. Kim DY, Yim SC, Lee PC et al (2004) Batch and continuous fermentation of succinic acid from wood hydrolysate by Mannheimia succiniciproducens MBEL55E. Enzyme Microb Technol 35:648–653. doi:10.1016/j.enzmictec.2004.08.018

    Article  CAS  Google Scholar 

  18. Lee PC, Lee SY, Hong SH, Chang HN (2003) Batch and continuous cultures of Mannheimia succiniciproducens MBEL55E for the production of succinic acid from whey and corn steep liquor. Bioprocess Biosyst Eng 26:63–67. doi:10.1007/s00449-003-0341-1

    Article  CAS  Google Scholar 

  19. Oh I, Lee H, Park C et al (2008) Succinic acid production by continuous fermentation process using Mannheimia succiniciproducens LPK7. J Microbiol Biotechnol 18:908–912

    CAS  Google Scholar 

  20. Beauprez JJ, De Mey M, Soetaert WK (2010) Microbial succinic acid production: natural versus metabolic engineered producers. Process Biochem 45:1103–1114. doi:10.1016/j.procbio.2010.03.035

    Article  CAS  Google Scholar 

  21. Vemuri GN, Eiteman MA, Altman E (2002) Effects of growth mode and pyruvate carboxylase on succinic acid production by metabolically engineered strains of Escherichia coli. Appl Environ Microbiol 68:1715–1727. doi:10.1128/AEM.68.4.1715-1727.2002

    Article  CAS  Google Scholar 

  22. Jantama K, Zhang X, Moore JC et al (2008) Eliminating side products and increasing succinate yields in engineered strains of Escherichia coli C. Biotechnol Bioeng 101:881–893. doi:10.1002/bit.22005

    Article  CAS  Google Scholar 

  23. Yan Q, Zheng P, Dong J-J, Sun Z-H (2014) A fibrous bed bioreactor to improve the productivity of succinic acid by Actinobacillus succinogenes. J Chem Technol Biotechnol 89:1760–1766. doi:10.1002/jctb.4257

    Article  CAS  Google Scholar 

  24. Urbance SE, Pometto AL, Dispirito AA, Denli Y (2004) Evaluation of succinic acid continuous and repeat-batch biofilm fermentation by Actinobacillus succinogenes using plastic composite support bioreactors. Appl Microbiol Biotechnol 65:664–670. doi:10.1007/s00253-004-1634-2

    Article  CAS  Google Scholar 

  25. Lin SKC, Du C, Koutinas A et al (2008) Substrate and product inhibition kinetics in succinic acid production by Actinobacillus succinogenes. Biochem Eng J 41:128–135. doi:10.1016/j.bej.2008.03.013

    Article  CAS  Google Scholar 

  26. Guettler M, Rumler D, Jain M (1999) Actinobacillus succinogenes sp. nov., a novel succinic-acid-producing strain from the bovine rumen. Int J Syst Bacteriol 49:207–216

    Article  CAS  Google Scholar 

  27. FitzPatrick M, Champagne P, Cunningham MF, Whitney RA (2010) A biorefinery processing perspective: treatment of lignocellulosic materials for the production of value-added products. Bioresour Technol 101:8915–8922. doi:10.1016/j.biortech.2010.06.125

    Article  CAS  Google Scholar 

  28. Zhao X, Zhang L, Liu D (2012) Biomass recalcitrance. Part I: the chemical compositions and physical structures affecting the enzymatic hydrolysis of lignocellulose. Biofuels, Bioprod Biorefining 6:465–482. doi:10.1002/bbb.1331

    Article  CAS  Google Scholar 

  29. Chen X, Shekiro J, Franden MA et al (2012) The impacts of deacetylation prior to dilute acid pretreatment on the bioethanol process. Biotechnol Biofuels 5:8. doi:10.1186/1754-6834-5-8

    Article  CAS  Google Scholar 

  30. Weiss ND, Nagle NJ, Tucker MP, Elander RT (2009) High xylose yields from dilute acid pretreatment of corn stover under process-relevant conditions. Appl Biochem Biotechnol 155:418–428. doi:10.1007/s12010-008-8490-y

    Article  CAS  Google Scholar 

  31. Schell D, Farmer J (2003) Dilute-sulfuric acid pretreatment of corn stover in pilot-scale reactor. Appl Biochem Biotechnol 105:69–85

    Article  Google Scholar 

  32. Villadsen J, Nielsen J, Lidén G (2011) Bioreaction engineering principles, Third. Engineering. doi: 10.1007/978-1-4419-9688-6

  33. Cheng K-C, Demirci A, Catchmark JM (2010) Advances in biofilm reactors for production of value-added products. Appl Microbiol Biotechnol 87:445–456. doi:10.1007/s00253-010-2622-3

    Article  CAS  Google Scholar 

  34. Liu Y-P, Zheng P, Sun Z-H et al (2008) Economical succinic acid production from cane molasses by Actinobacillus succinogenes. Bioresour Technol 99:1736–1742. doi:10.1016/j.biortech.2007.03.044

    Article  CAS  Google Scholar 

  35. Xi Y, Dai W, Xu R et al (2013) Ultrasonic pretreatment and acid hydrolysis of sugarcane bagasse for succinic acid production using Actinobacillus succinogenes. Bioprocess Biosyst Eng 36:1779–1785. doi:10.1007/s00449-013-0953-z

    Article  CAS  Google Scholar 

  36. Borges ER, Pereira N (2011) Succinic acid production from sugarcane bagasse hemicellulose hydrolysate by Actinobacillus succinogenes. J Ind Microbiol Biotechnol 38:1001–1011. doi:10.1007/s10295-010-0874-7

    Article  CAS  Google Scholar 

  37. Zheng P, Dong J-J, Sun Z-H et al (2009) Fermentative production of succinic acid from straw hydrolysate by Actinobacillus succinogenes. Bioresour Technol 100:2425–2429. doi:10.1016/j.biortech.2008.11.043

    Article  CAS  Google Scholar 

  38. Liang L, Liu R, Li F et al (2013) Repetitive succinic acid production from lignocellulose hydrolysates by enhancement of ATP supply in metabolically engineered Escherichia coli. Bioresour Technol 143:405–412. doi:10.1016/j.biortech.2013.06.031

    Article  CAS  Google Scholar 

  39. Qureshi N, Annous BA, Ezeji TC et al (2005) Biofilm reactors for industrial bioconversion processes: employing potential of enhanced reaction rates. Microb Cell Fact 4:24. doi:10.1186/1475-2859-4-24

    Article  CAS  Google Scholar 

  40. Brink HG, Nicol W (2014) Succinic acid production with Actinobacillus succinogenes: rate and yield analysis of chemostat and biofilm cultures. Microb Cell Fact 13:111. doi:10.1186/s12934-014-0111-6

    Article  CAS  Google Scholar 

  41. Corona-González RI, Bories A, González-Álvarez V, Pelayo-Ortiz C (2008) Kinetic study of succinic acid production by Actinobacillus succinogenes ZT-130. Process Biochem 43:1047–1053. doi:10.1016/j.procbio.2008.05.011

    Article  CAS  Google Scholar 

  42. McKinlay JB, Shachar-Hill Y, Zeikus JG, Vieille C (2007) Determining Actinobacillus succinogenes metabolic pathways and fluxes by NMR and GC-MS analyses of 13C-labeled metabolic product isotopomers. Metab Eng 9:177–192. doi:10.1016/j.ymben.2006.10.006

    Article  CAS  Google Scholar 

  43. McKinlay JB, Vieille C (2008) 13C-metabolic flux analysis of Actinobacillus succinogenes fermentative metabolism at different NaHCO3 and H2 concentrations. Metab Eng 10:55–68. doi:10.1016/j.ymben.2007.08.004

    Article  CAS  Google Scholar 

  44. McKinlay JB, Laivenieks M, Schindler BD et al (2010) A genomic perspective on the potential of Actinobacillus succinogenes for industrial succinate production. BMC Genom 11:680. doi:10.1186/1471-2164-11-680

    Article  CAS  Google Scholar 

  45. Lu S, Eiteman MA, Altman E (2009) Effect of CO2 on succinate production in dual-phase Escherichia coli fermentations. J Biotechnol 143:213–223. doi:10.1016/j.jbiotec.2009.07.012

    Article  CAS  Google Scholar 

  46. Runquist D, Hahn-Hägerdal B, Bettiga M (2009) Increased expression of the oxidative pentose phosphate pathway and gluconeogenesis in anaerobically growing xylose-utilizing Saccharomyces cerevisiae. Microb Cell Fact 8:49. doi:10.1186/1475-2859-8-49

    Article  CAS  Google Scholar 

  47. Witteveen CFB, Busink R, van de Vondervoort P et al (1989) L-Arabinose and D-Xylose catabolism in Aspergillus niger. J Gen Microbiol 135:2163–2171

    CAS  Google Scholar 

  48. Schindler BD, Joshi RV, Vieille C (2014) Respiratory glycerol metabolism of Actinobacillus succinogenes 130Z for succinate production. J Ind Microbiol Biotechnol 41:1339–1352. doi:10.1007/s10295-014-1480-x

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The financial assistance of the National Research Foundation (NRF) towards this research is hereby acknowledged. Opinions expressed and conclusions arrived at, are those of the author and are not necessarily to be attributed to the NRF. We thank Andre Naude for his help in developing the HPLC methods.

Author information

Affiliations

  1. Department of Chemical Engineering, University of Pretoria, Lynnwood Road, Hatfield, Pretoria, 0002, South Africa

    Michael F. A. Bradfield & Willie Nicol

Authors
  1. Michael F. A. Bradfield
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Willie Nicol
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Willie Nicol.

Ethics declarations

Conflict of interest

The authors declare that no conflict of interest exists.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bradfield, M.F.A., Nicol, W. Continuous succinic acid production from xylose by Actinobacillus succinogenes . Bioprocess Biosyst Eng 39, 233–244 (2016). https://doi.org/10.1007/s00449-015-1507-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-015-1507-3

Keywords

  • Actinobacillus succinogenes
  • Continuous fermentation
  • Biofilm
  • Redox balance
  • Succinic acid
  • Xylose