Skip to main content
SpringerLink
Log in

Effects of lignocellulose-derived inhibitors on growth and succinic acid accumulation by Corynebacterium glutamicum

  • Research Paper
  • Published:
Biotechnology and Bioprocess Engineering Aims and scope Submit manuscript

Abstract

Succinic acid production by genetically engineered C. glutamicum from lignocellulosic biomass requires the hydrolysis of carbohydrate polymers into fermentable syrup. A variety of toxic compounds are produced such as aldehydes and organic acids, while the hydrolysis of hemicellulose with dilute acid. In this study, we have investigated the toxicity of representative aldehydes (furfural, 5-hydroxymethylfurfural, syringaldehyde, and vanillin) and organic acids (ferulic, 4-hydroxybenzic, vanillic, protocatechuic acid) on growth and succinic acid accumulation of C. glutamicum NC-1. In the presence of various inhibitors of growth experiment, furfural, 5- hydroxymethylfurfural appeared less toxic to growth of C. glutamicum NC-1, syringaldehyde almost completely inhibitor growth of C. glutamicum NC-1, vanillin has inhibited the growth of 67%, of organic acids, only ferulic appeared toxic to growth of C. glutamicum NC-1. Of succinic acid accumulation experiment under oxygen deprivation, all the organic acids compounds showed little inhibition on the glocuse consumption and succinic acid accumulation of C. glutamicum NC-1, but furfural, 5- hydroxymethylfurfural and vanillic have decreased the production of succinic acid. In addition, the actual inhibitor mixtures from the acid hydrolysate of corn cobs have reduced the accumulation of succinic acid. Across further research showed, a reason of succinic acid yield decrease was the malic enzyme activity was inhibited.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Wang, C., H. L. Zhang, H. Cai, Z. H. Zhou, Y. L. Chen, Y. L. Chen, and P. K. Ouyang (2014) Succinic acid production from corn cob hydrolysates by genetically Engineered Corynebacterium glutamicum. Appl. Biochem. Biotechnol. 172: 340–350.

    Article  CAS  Google Scholar 

  2. Ji, X. J., H. Huang, J. Du, J. G. Zhu, L. J. Ren, S. Li, and Z. K. Nie (2009) Development of an industrial medium for economical 2,3-butanediol production through co-fermentation of glucose and xylose by Klebsiella oxytoca. Bioresour. Technol. 100: 5214–5218.

    Article  CAS  Google Scholar 

  3. Dorado, M. P., S. K. Lin, A., Du, C. Y. Koutinas, R. H. Wang, and C. Webb (2009) Cereal-based biorefinery development: Utilisation of wheat milling by-products for the production of succinic acid. J. Biotechnol. 143: 51–59.

    Article  CAS  Google Scholar 

  4. Gray, K. A., L. Zhao, and M. Emptage (2006) Current opinion in chemical biology. Bioethanol. Curr. Opin. Chem. Biol. 10: 141–146.

    Article  CAS  Google Scholar 

  5. Vertès, A. A., M. Inui, and H. Yukawa (2008) Technological options for biological fuel ethanol. J. Mol. Microbiol. Biotechnol. 15: 16–30.

    Article  Google Scholar 

  6. Sakai, S., Y. Tsuchida, H. Nakamoto, S. Okino, O. Ichihashi, H. Kawaguchi, T. Watanabe, M. Inui, and H. Yukawa (2007) Effect of lignocellulose-derived inhibitors on growth of and ethanol production by growth-arrested Corynebacterium glutamicum R. Appl. Environ. Microbiol. 73: 2349–2353.

    Article  CAS  Google Scholar 

  7. Huang, C., H. Wu, Q. P. Liu, Y. Y. Li, and M. H. Zong (2011) Effects of Aldehydes on the Growth and Lipid Accumulation of Oleaginous Yeast Trichosporon fermentans. J. Agricul. Food Chem. 59: 4606–4613.

    Article  CAS  Google Scholar 

  8. Hong, H. S. (2007) Systems approaches to succinic acid-producing microorganisms. Biotechnol. Bioproc. Eng. 12: 73–79.

    Article  CAS  Google Scholar 

  9. Lin, C. S. K., R. Luque, J. H. Clark, C. Webb, and C. Y Du (2012) Wheat-based biorefining strategy for fermentative production and chemical transformations of succinic acid. Biofuels Bioproducts & Bioref. Biofpr. 6: 88–104.

    Article  CAS  Google Scholar 

  10. Cheng, K. K., X. B. Zhao, J. Zeng, and J. A. Zhang (2012) Biotechnological production of succinic acid: Current state and perspectives. Biofuels Bioprod. Bioref. 6: 302–318.

    Article  CAS  Google Scholar 

  11. Beauprez, J. J., M. De Mery, and W. K. Soetaert (2010) Microbial succinic acid production: Natural versus metabolic engineered producers. Proc. Biochem. 45: 1103–1114.

    Article  CAS  Google Scholar 

  12. Werpy, T., J. Frye, and J. Holladay (2006) Succinic acid-a model building block for chemical production from renewable resources. pp. 367–379. In: Birgit Kamm, Patrik R. Gruber, and Michael Kamm (eds.). Biorefineries-Industrial Processes and Products: Status Quo and Future Directions. Wiley-VCH, Weinheim.

    Google Scholar 

  13. Cukalovic, A. and C. V. Stevens (2008) Feasibility of production methods for succinic acid derivatives: A marriage of renewable resources and chemical technology. Biofuels Bioprod. Bioref. 2: 505–529.

    Article  CAS  Google Scholar 

  14. Zeikus, G. J., M. K. Jain, and P. Elankovan (1999) Biotechnology of succinic acid production and markets for derived industrial products. Appl. Microbiol. Biotechnol. 51: 545–552.

    Article  CAS  Google Scholar 

  15. Okino, S., R. Noburyu, M. Suda, T. Jojima, M. Inui, and H. Yukawa (2008) An efficient succinic acid production process in a metabolically engjneered Corynebacterium glutamicum strain. Appl. Microbiol. Biotechnol. 81: 459–464.

    Article  CAS  Google Scholar 

  16. Alvira, P., E. Tomas-Pejo, M. Ballesteros, and M. J. Negro (2010) Pretreatment technologies for an efficient bioethanol production process based on enzymatic hydrolysis: A review. Bioresource Technology. 101: 4851–4861.

    Article  CAS  Google Scholar 

  17. Almeida, J. R. M., T. Modig, A. Petersson, B. Hähn-Hägerdal, G. Lidén, and M. F. Gorwa-Grauslund (2007) Increasrd tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae. J. Chem. Technol. Biotechnol. 82: 340–349.

    Article  CAS  Google Scholar 

  18. Palmqvist, E., J. S. Almeida, and B. Hahn-Hägerdal (1999) Influence of furfural on anaerobic glycolytic of Saccharomyces cerevisiae in batch culture. Biotechnol. Bioeng. 62: 447–454.

    Article  CAS  Google Scholar 

  19. Oliva, J., M. Negro, F. Sáez, I. Ballesteros, P. Manzanares, A. González, and M. Ballesteros (2006) Effects of acetic acid, furfural and catechol combinations on ethanol fermentation of KIuyveromyces marxianus. Proc. Biochem. 41: 1223–1228.

    Article  CAS  Google Scholar 

  20. Ausubel, F. M., R. Brent, and R. E. Kingston (1998) Short protocols in molecular biology. pp. 240–251. Science Press. Beijing, China.

    Google Scholar 

  21. Boernke, W. E., C. S. Millard, P. W. Stevens, S. N. Kakar, F. J. Stevens, and M. I. Donnelly (1995) Stringency of substrate specificity of Escherichia coli malate dehydrogenase. Acta Biochim. Biophy. 332: 43–52.

    Google Scholar 

  22. Klinke, H. B., A. B. Thomsen, and B. K. Ahring (2004) Inhibition of ethanol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass. Appl. Microbiol. Biotechnol. 66: 10–26.

    Article  CAS  Google Scholar 

  23. Boopathy, R., H. Bokang, and L. Daniels (1993) Biotransformation of furfural and 5-hydroxymethyl furfural by enteric bacteria. J. Industrial Microbiol. 11: 147–150.

    Article  CAS  Google Scholar 

  24. Delgenes, J. P., R. Moletta, and J. M. Navarro (1996) Effects of lignocellulose degradation products on ethanol fermentations of glucose and xylose by Saccharomyces cerevisiae, Zymomonas mobilis, Pichia stipitis, and Candida shehatae. Enz. Microbial. Technol. 19: 220–225.

    Article  CAS  Google Scholar 

  25. Zaldivar, J., A. Martinez, and L. O. Ingram (1999) Effect of selected aldehydes on the growth and fermentation of ethanologenic Escherichia coli. Biotechnol. Bioeng. 65: 24–33.

    Article  CAS  Google Scholar 

  26. Zaldivar, J. and L. O. Ingram (1999) Effect of organic acids on the growth and fermentation of ethanologenic Escherichia coli LY01. Biotechnol. Bioeng. 66: 203–210.

    Article  CAS  Google Scholar 

  27. Klinke, H. B., L. Olsson, A. B. Thomsen, and B. K. Ahring (2003) Potential inhibitors from wet oxidation of wheat straw and their effect on ethanol production of Saccharomyces cerevisiae: Wet oxidation and fermentation by yeast. Biotechnol. Bioeng. 81: 738–747.

    Article  CAS  Google Scholar 

  28. Singh, N. P. and A. Khan (1995) Acetaldehyde: Genotoxicity and cytotoxicity in human lymphocytes. Mutation Res. -DNA Repair 337: 9–17.

    Article  CAS  Google Scholar 

  29. Sampaio, F. C., P. Torre, F. M. L. Passos, C. A. De Moraes, P. Perego, and A. Converti (2007) Influence of inhibitory compounds and minor sugars on xylitol production by Debaryomyces hansenii. Appl. Biochem. Biotechnol. 136: 165–181.

    Article  CAS  Google Scholar 

  30. Palmqvist, E. and B. Hahn-Hagerdal (2000) Fermentation of lignocellulosic hydrolysates. II: Inhibitors andmechanisms of inhibition. Bioresour. Technol. 74: 25–33.

    CAS  Google Scholar 

  31. Almeida, J., T. Modig, A. Petersson, B. Hahn-Hagerdal, G. Liden, and M. Gorwa-Grauslund (2007) Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae. J. Chem. Technol. Biotechnol. 82: 340–349.

    Article  CAS  Google Scholar 

  32. Palmqvist, E., J. S. Almeida, and B. Hahn-Hagerdal (1999) Influence of furfural on anaerobic glycolytic kinetics of Saccharomyces cerevisiae in batch culture. Bioresour. Technol. 62: 447–454.

    CAS  Google Scholar 

  33. Zaldivar, J., A. Martinez, and L. O. Ingram (1999) Effect of selected aldehydes on the growth and fermentation of ethanologenic Escherichia coli. Bioresour. Technol. 65: 24–33.

    CAS  Google Scholar 

  34. Sarvari Horvath, I., C. J. Franzen, M. J. Taherzadeh, C. Niklasson, and G. Liden (2003) Effects of furfural on the respiratory metabolism of Saccharomyces cerevisiae in glucose-limited chemostats. Appl. Environ. Microbiol. 69: 4076–4086.

    Article  Google Scholar 

  35. Ratledge, C. (2004) Fatty acid biosynthesis in microorganisms being used for single cell oil production. Biochimie. 86: 807–815.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Biotechnology and Pharmaceutical Engineering, Nanjing University of Technology, Nanjing, 211-816, China

    Hong-Tao Xu, Chen Wang, Zhi-Hui Zhou & Heng Cai

  2. College of Food Science and Engineering, Inner Mongolia, Agricultural University, Hohhot, 010-018, China

    Zhong-Jun Chen

Authors
  1. Hong-Tao Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhi-Hui Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhong-Jun Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Heng Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Heng Cai.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, HT., Wang, C., Zhou, ZH. et al. Effects of lignocellulose-derived inhibitors on growth and succinic acid accumulation by Corynebacterium glutamicum . Biotechnol Bioproc E 20, 744–752 (2015). https://doi.org/10.1007/s12257-015-0201-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12257-015-0201-2

Keywords

Search

Navigation