SpringerLink
Log in

Effect of Carbonyl Inhibitors and Their H2O2 Detoxification on Lactic Acid Fermentation

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Biomass degradation compounds significantly inhibit biochemical conversion of biomass prehydrolysates to biofuels and chemicals, such as lactic acid. To characterize the structure-activity relationship of carbonyl inhibition on lactic acid fermentation, we examined effects of eight carbonyl compounds (furfural, 5-hydroxymethyl furfural, vanillin, syringaldehyde, 4-hydroxybenzaldehyde, phthalaldehyde, benzoic acid, and pyrogallol aldehyde) and creosol on lactic acid production by Lactobacillus delbrueckii. Pyrogallol aldehyde reduced the cell growth rate by 35 % at 1.0 mM and inhibited lactic acid production completely at 2.0 mM. By correlating the molecular descriptors to the inhibition constants in lactic acid fermentation, we found a good relationship between the hydrophobicity (Log P) of aldehydes and their inhibition constants in fermentation. The inhibitory effect of carbonyl inhibitors appeared to correlate with their thiol reactivity as well. In addition, we found that H2O2 detoxified pyrogallol aldehyde and phthalaldehyde inhibitory activity. H2O2 detoxification was applied to real biomass prehydrolysates in lactic acid fermentation.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  1. Boguta, A. M., Bringel, F., Martinussen, J. and Jensen, P. R. (2014). Screening of lactic acid bacteria for their potential as microbial cell factories for bioconversion of lignocellulosic feedstocks. Microb Cell Fact, 13

  2. Chen, S. F., Mowery, R. A., Castleberry, V. A., van Walsum, G. P., & Chambliss, C. K. (2006). High-performance liquid chromatography method for simultaneous determination of aliphatic acid, aromatic acid and neutral degradation products in biomass pretreatment hydrolysates. Journal of Chromatography A, 1104, 54–61.

    Article  CAS  Google Scholar 

  3. Nichols, N. N., Sharma, L. N., Mowery, R. A., Chambliss, C. K., van Walsum, G. P., Dien, B. S., & Iten, L. B. (2008). Fungal metabolism of fermentation inhibitors present in corn stover dilute acid hydrolysate. Enzyme and Microbial Technology, 42, 624–630.

    Article  CAS  Google Scholar 

  4. Olsson, L., & HahnHagerdal, B. (1996). Fermentation of lignocellulosic hydrolysates for ethanol production. Enzyme and Microbial Technology, 18, 312–331.

    Article  CAS  Google Scholar 

  5. Cao, D. X., Tu, M. B., **e, R., Li, J., Wu, Y. N., & Adhikari, S. (2014). Inhibitory activity of carbonyl compounds on alcoholic fermentation by saccharomyces cerevisiae. Journal of Agricultural and Food Chemistry, 62, 918–926.

    Article  CAS  Google Scholar 

  6. Franden, M. A., Pilath, H. M., Mohagheghi, A., Pienkos, P. T., and Zhang, M. (2013). Inhibition of growth of Zymomonas mobilis by model compounds found in lignocellulosic hydrolysates. Biotechnol Biofuels, 6

  7. Zaldivar, J., & Ingram, L. O. (1999). Effect of organic acids on the growth and fermentation of ethanologenic Escherichia coli LY01. Biotechnology and Bioengineering, 66, 203–210.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  9. Zaldivar, J., Martinez, A., & Ingram, L. O. (2000). Effect of alcohol compounds found in hemicellulose hydrolysate on the growth and fermentation of ethanologenic Escherichia coli. Biotechnology and Bioengineering, 68, 524–530.

    Article  CAS  Google Scholar 

  10. Larsson, S., Quintana-Sainz, A., Reimann, A., Nilvebrant, N. O., & Jonsson, L. J. (2000). Influence of lignocellulose-derived aromatic compounds on oxygen-limited growth and ethanolic fermentation by Saccharomyces cerevisiae. Applied Biochemistry and Biotechnology, 84–6, 617–632.

    Article  Google Scholar 

  11. Chan, K., & O’Brien, P. J. (2008). Structure-activity relationships for hepatocyte toxicity and electrophilic reactivity of alpha, beta-unsaturated esters, acrylates and methacrylates. Journal of Applied Toxicology, 28, 1004–1015.

    Article  CAS  Google Scholar 

  12. Schultz, T. W., Yarbrough, J. W., & Johnson, E. L. (2005). Structure-activity relationships for reactivity of carbonyl-containing compounds with glutathione. Sar and Qsar in Environmental Research, 16, 313–322.

    Article  CAS  Google Scholar 

  13. Schwobel, J. A. H., Wondrousch, D., Koleva, Y. K., Madden, J. C., Cronin, M. T. D., & Schuurmann, G. (2010). Prediction of Michael-type acceptor reactivity toward glutathione. Chemical Research in Toxicology, 23, 1576–1585.

    Article  CAS  Google Scholar 

  14. Schwobel, J. A. H., Koleva, Y. K., Enoch, S. J., Bajot, F., Hewitt, M., Madden, J. C., Roberts, D. W., Schutz, T. W., & Cronin, M. T. D. (2011). Measurement and estimation of electrophilic reactivity for predictive toxicology. Chemistry Review, 111, 2562–2596.

    Article  CAS  Google Scholar 

  15. Zhang, D. X., Ong, Y. L., Li, Z., & Wu, J. C. (2013). Biological detoxification of furfural and 5-hydroxyl methyl furfural in hydrolysate of oil palm empty fruit bunch by Enterobacter sp FDS8. Biochemical Engineering Journal, 72, 77–82.

    Article  CAS  Google Scholar 

  16. Shuler, M. L., & Kargi, F. (2002). Bioprocess engineering (2nd ed.). Upper Saddle River: Prentice Hall.

    Google Scholar 

  17. Ling, L. S., Mohamad, R., Rahim, R. A., Wan, H. Y., & Bin Ariff, A. (2006). Improved production of live cells of Lactobacillus rhamnosus by continuous cultivation using glucose-yeast extract medium. Journal of Microbiology, 44, 439–446.

    CAS  Google Scholar 

  18. Bohme, A., Thaens, D., Paschke, A., & Schuurmann, G. (2009). Kinetic glutathione chemoassay to quantify thiol reactivity of organic electrophiles-application to alpha, beta-unsaturated ketones, acrylates, and propiolates. Chemical Research in Toxicology, 22, 742–750.

    Article  CAS  Google Scholar 

  19. Freidig, A. P., Verhaar, H. J. M., & Hermens, J. L. M. (1999). Quantitative structure-property relationships for the chemical reactivity of acrylates and methacrylates. Environmental Toxicology and Chemistry, 18, 1133–1139.

    CAS  Google Scholar 

  20. Parr, R. G., Von Szentpaly, L., & Liu, S. B. (1999). Electrophilicity index. Journal of the American Chemical Society, 121, 1922–1924.

    Article  CAS  Google Scholar 

  21. **e, R., Tu, M. B., Wu, Y. N., & Taylor, S. (2012). Reducing sugars facilitated carbonyl condensation in detoxification of carbonyl aldehyde model compounds for bioethanol fermentation. RSC Advances, 2, 7699–7707.

    Article  CAS  Google Scholar 

  22. Ezeji, T., Qureshi, N., & Blaschek, H. P. (2007). Butanol production from agricultural residues: impact of degradation products on Clostridium beijerinckii growth and butanol fermentation. Biotechnology and Bioengineering, 97, 1460–1469.

    Article  CAS  Google Scholar 

  23. Palmqvist, E., Almeida, J. S., & Hahn-Hagerdal, B. (1999). Influence of furfural on anaerobic glycolytic kinetics of Saccharomyces cerevisiae in batch culture. Biotechnology and Bioengineering, 62, 447–454.

    Article  CAS  Google Scholar 

  24. Wahlbom, C. F., & Hahn-Hagerdal, B. (2002). Furfural, 5-hydroxymethyl furfural, and acetoin act as external electron acceptors during anaerobic fermentation of xylose in recombinant Saccharomyces cerevisiae. Biotechnology and Bioengineering, 78, 172–178.

    Article  CAS  Google Scholar 

  25. Taherzadeh, M. J., Niklasson, C., & Liden, G. (1997). Acetic acid—friend or foe in anaerobic batch conversion of glucose to ethanol by Saccharomyces cerevisiae? Chemical Engineering Science, 52, 2653–2659.

    Article  CAS  Google Scholar 

  26. Chan, K., Jensen, N., & O’Brien, P. J. (2008). Structure–activity relationships for thiol reactivity and rat or human hepatocyte toxicity induced by substituted p-benzoquinone compounds. Journal of Applied Toxicology, 28, 608–620.

    Article  CAS  Google Scholar 

  27. Cronin, M. T. D., & Schultz, T. W. (1996). Structure-toxicity relationships for phenols to Tetrahymena pyriformis. Chemosphere, 32, 1453–1468.

    Article  CAS  Google Scholar 

  28. Cronin, M. T. D., & Schultz, T. W. (2001). Development of quantitative structure-activity relationships for the toxicity of aromatic compounds to Tetrahymena pyriformis: comparative assessment of the methodologies. Chemical Research in Toxicology, 14, 1284–1295.

    Article  CAS  Google Scholar 

  29. Klinke, H. B., Thomsen, A. B., & Ahring, B. K. (2004). Inhibition of ethanol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass. Applied Microbiology and Biotechnology, 66, 10–26.

    Article  CAS  Google Scholar 

  30. Larsson, S., Reimann, A., Nilvebrant, N. O., & Jonsson, L. J. (1999). Comparison of different methods for the detoxification of lignocellulose hydrolyzates of spruce. Applied Biochemistry and Biotechnology, 77–9, 91–103.

    Article  Google Scholar 

  31. Palmqvist, E., & Hahn-Hagerdal, B. (2000). Fermentation of lignocellulosic hydrolysates. II: inhibitors and mechanisms of inhibition. Bioprocess Technology, 74, 25–33.

    CAS  Google Scholar 

  32. Leonard, R. H., & Hajny, G. J. (1945). Fermentation of wood sugars to ethyl alcohol. Industrial and Engineering Chemistry, 37, 390–395.

    Article  CAS  Google Scholar 

  33. Hodge, D. B., Andersson, C., Berglund, K. A., & Rova, U. (2009). Detoxification requirements for bioconversion of softwood dilute acid hydrolysates to succinic acid. Enzyme and Microbial Technology, 44, 309–316.

    Article  CAS  Google Scholar 

  34. Lee, J. M., Venditti, R. A., Jameel, H., & Kenealy, W. R. (2011). Detoxification of woody hydrolysates with activated carbon for bioconversion to ethanol by the thermophilic anaerobic bacterium Thermoanaerobacterium saccharolyticum. Biomass and Bioenergy, 35, 626–636.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors appreciate the financial support of this study, partially, by grants from the Auburn Univeristy (IGP and AAES) and by the National Science Foundation (NSF-CBET 1254899).

Author information

Author notes

    Authors and Affiliations

    1. Forest Products Laboratory and Center for Bioenergy and Bioproducts, Auburn University, 520 Devall Drive, Auburn, AL, 36849, USA

      **g Li, Caiqing Zhu & Maobing Tu

    2. Department of Mathematics and Statistics, Auburn University, Auburn, AL, 36849, USA

      **** Han

    3. Department of Chemistry and Biochemistry, Auburn University, Auburn, AL, 36849, USA

      Yonnie Wu

    Authors
    1. **g Li
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Caiqing Zhu
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Maobing Tu
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. **** Han
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Yonnie Wu
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Maobing Tu.

    Additional information

    **g Li and Caiqing Zhu contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Li, J., Zhu, C., Tu, M. et al. Effect of Carbonyl Inhibitors and Their H2O2 Detoxification on Lactic Acid Fermentation. Appl Biochem Biotechnol 175, 3657–3672 (2015). https://doi.org/10.1007/s12010-015-1533-2

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s12010-015-1533-2

    Keywords

    Search

    Navigation