Skip to main content

Advertisement

SpringerLink
Log in

Value Adding of Poplar Hemicellulosic Prehydrolyzates: Laccase Production by Botryosphaeria rhodina MAMB-05 and Its Application in the Detoxification of Prehydrolyzates

  • Published:
BioEnergy Research Aims and scope Submit manuscript

Abstract

Fast-growing hybrid poplar species are attractive as feedstocks for the production of bio-based chemicals including biofuels. Pretreatment makes cellulose accessible to enzymatic hydrolysis, producing hemicellulose and lignin as major co-products. Poplar woodchips pretreated hydrothermally in an experimental industrial pilot-plant generated two prehydrolyzate streams; purge-condensate collected from cooking the woodchips and press-filtrate collected after the fiber explosion step. Both prehydrolyzates contain hemicellulose sugars (pentoses, hexoses, oligosaccharides), acetic acid, and degradation products from hemicellulose and lignin (furanic and phenolic compounds, respectively). Purge prehydrolyzate was highly diluted, of low sugar content and high biochemical/chemical oxygen demand, and constituted a process waste that was addressed for value-adding through production of enzymes by fermentation. Wood-decay fungi were screened for laccases on purge prehydrolyzate, with Botryosphaeria rhodina producing highest titers. B. rhodina detoxified the prehydrolyzate but at expense of sugar consumption. Adding xylose and glycerol to purge did not inhibit fungal growth or impede laccase production. Phenolics in the purge had inducing effect on enhancing laccase titers. Laccase production was optimized by Box-Behnken-(33)-factorial design varying the concentration of xylose in the purge, together with adding copper as laccase inducer and glycerol to increase the level of fermentable substrate, resulting in optimal enzyme titers (36.37 ± 3.52U/mL; validated). The crude laccase preparation was employed to detoxify the more concentrated press prehydrolyzate, reducing the overall content of phenolics by ∼30 %. Chromatographic (high-performance liquid chromatography-ultraviolet, gas chromatography/mass spectrometry) analysis identified various phenolic compounds present in the press prehydrolyzate following laccase treatment, and in the presence of the mediator, ABTS, the phenolics content decreased further.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Sannigrahi P, Ragauskas AJ, Tuskan GA (2010) Poplar as a feedstock for biofuels: a review of compositional characteristics. Biofuels Bioprod Bioref 4:209–226

    Article  CAS  Google Scholar 

  2. Taherzadeh MJ, Karimi K (2007) Acid-based hydrolysis processes for ethanol from lignocellulosic materials: a review. Bioresources 2:472–499

    CAS  Google Scholar 

  3. Saha BC (2003) Hemicellulose bioconversion. J Ind Microbiol Biotechnol 30:279–291

    Article  CAS  PubMed  Google Scholar 

  4. Zhang X, Tu M, Paice MG (2011) Routes to potential bioproducts from lignocellulosic biomass, lignin and hemicelluloses. Bioenerg Res 4:246–257

    Article  Google Scholar 

  5. Werpy T, Petersen G (2004) Top value added chemicals from biomass. Volume I: results of screening for potential candidates from sugars and synthesis gas. Pacific Northwest National Laboratory, National Renewable Energy Laboratory, Office of Biomass Program, U.S. Department of Energy (DOE), Oak Ridge, TN (USA)

  6. Wen S, Liu L, Nie KL, Deng L, Tan TW, Fang W (2013) Enhanced fumaric acid production by fermentation of xylose using a modified strain of Rhizopus arrhizus. Bioresources 8:2186–2194

    Article  CAS  Google Scholar 

  7. Massen N, Panakova M, Wierckx N, Geiser E, Zimmermann M, Bölker M, Klinner U, Blank LM (2014) Influence of carbon and nitrogen concentration on itaconic acid production by the smut fungus Ustilago maydis. Eng Life Sci 14:129–134

    Article  Google Scholar 

  8. Pu Y, Hu F, Huang F, Davison BH, Ragauskas AJ (2013) Assessing the molecular structure basis for biomass recalcitrance during dilute acid and hydrothermal pretreatments. Biotechnol Biofuels 6:15

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Clark TA, Mackie KL (1984) Fermentation inhibitors in wood hydrolysates derived from the softwood Pinus radiata. J Chem Technol Biotechnol 34:101–110

    Article  Google Scholar 

  10. Jönsson LJ, Alriksson B, Nilvebrant N-O (2013) Bioconversion of lignocellulose: inhibitors and detoxification. Biotechnol Biofuels 6:16

    Article  PubMed Central  PubMed  Google Scholar 

  11. Messerschmidt A (1997) Multi-copper oxidases. World Scientific, Singapore

    Book  Google Scholar 

  12. Arora DS, Sharama RK (2010) Ligninolytic fungal laccases and their biotechnological applications. Appl Biochem Biotechnol 160:1760–1788

    Article  CAS  Google Scholar 

  13. Madhavi V, Lele SS (2009) Laccase: properties and applications. Bioresources 4:1694–1717

    Google Scholar 

  14. Giese EC, Dekker RFH, Barbosa AM (2008) Orange baggase as substrate for the production of pectinase and laccase by Botryosphaeria rhodina MAMB-05 in submerged and solid state fermentation. Bioresources 3:335–345

    CAS  Google Scholar 

  15. Gómez J, Pazos M, Couto SR, Sanromán MA (2005) Chestnut shell and barley bran as potential substrates for laccase production by Coriolopsis rigida under solid-state conditions. J Food Eng 68:315–319

    Article  Google Scholar 

  16. Meza JC, Auria R, Lomascolo A, Sigoillot J-C, Casalot L (2007) Role of ethanol on growth, laccase production and protease activity in Pycnoporus cinnabarinus ss3. Enzym Microb Technol 41:162–168

    Article  CAS  Google Scholar 

  17. Dekker RFH, Barbosa AM, Sargent K (2002) The effect of lignin-related compounds on the growth and production of laccases by the ascomycete, Botryosphaeria sp. Enzym Microb Technol 30:374–380

    Article  CAS  Google Scholar 

  18. Dekker RFH, Barbosa AM, Giese EC, Godoy SDS, Covizzi LG (2007) Influence of nutrients on enhancing laccase production by Botryosphaeria rhodina MAMB-05. Int Microbiol 10:177–185

    CAS  PubMed  Google Scholar 

  19. Sluiter A, Hames B, Ruiz R, Scarlata C, Sluiter J, Templeton D (2008) Determination of ash in biomass. Laboratory Analytical Procedure (LAP). Technical Report NREL/TP-510-42622. National Renewable Energy Laboratory, Golden, Colorado

  20. Sluiter A, Hames B, Ruiz R, Scarlata C, Sluiter J, Templeton D, Crocker D (2012) Determination of structural carbohydrates and lignin in biomass. Laboratory Analytical Procedure (LAP). Technical Report NREL/TP-510-42618. National Renewable Energy Laboratory, Golden, Colorado

  21. Barbosa AM, Dekker RFH, ST. Hardy GE (1996) Veratryl alcohol as an inducer of laccase by an ascomycete, Botryosphaeria sp., when screened on the polymeric dye, poly R-478. Lett Appl Microbiol 23:93–96

    Article  CAS  Google Scholar 

  22. Vogel HJ (1956) A convenient growth medium for Neurospora crassa (medium N). Microbial Genet Bull 13:42–43

    Google Scholar 

  23. Hill T, Lewicki P (2006) Experimental design (industrial DOE). In: Statistics: methods and applications: a comprehensive reference for science, industry, and data mining, 1st edn. StatSoft Inc., Tulsa, OK, USA, pp 179–226. ISBN 1-884233-59-7

    Google Scholar 

  24. STATISTICA (2009) StatSoft Inc. http://www.statsoft.com

  25. Kiefer K, Herwehe K (1996) Use of BSTFA silylating reagent to prepare volatile derivatives for GC. Report SUPELCO 15(4):1–5

    Google Scholar 

  26. Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic–phosphotungstic acid reagents. Amer J Enol Viticult 16:144–153

    CAS  Google Scholar 

  27. APHA-AWWA-WEF (2012) Standard methods for the examination of water and wastewater, 22nd edn. American Public Health Association (APHA)-American Water Works Association (AWWA)-Water Environment Federation (WEF): Washington, DC, USA pp. 1496

  28. US-EPA (Environmental Protection Agency) Method 410.4 (1993) The determination of chemical oxygen demand by semi-automated colorimetry. J. W. O’Dell, Editor, Inorganic Chemistry Branch, Chemistry Research Division, Revision 2.0 http://www.caslab.com/EPA-Methods/PDF/EPA-Method-4104.pdf

  29. Verardo V, Arráez-Román D, Segura-Carretero A, Marconi E, Fernández-Gutiérrez A, Caboni MF (2011) Determination of free and bound phenolic compounds in buckwheat spaghetti by RP-HPLC-ESI-TOF-MS: effect of thermal processing from farm to fork. J Agric Food Chem 59:7700–7707

    Article  CAS  PubMed  Google Scholar 

  30. Matheson CD, McCollum AJ (2014) Characterising native plant resins from Australian Aboriginal artefacts using ATR-FTIR and GC/MS. J Archaeol Sci 52:116–128

    Article  CAS  Google Scholar 

  31. Salvador LD, Suganuma T, Kitahara K, Tanoue H, Ichiki M (2000) Monosaccharide composition of sweet potato fiber and cell wall polysaccharides from sweet potato, cassava, and potato analyzed by the high-performance anion exchange chromatography with pulsed amperometric detection method. J Agric Food Chem 48:3448–3454

    Article  CAS  PubMed  Google Scholar 

  32. Vasconcelos de Sá LR, de Oliveira MAL, Cammarota MC, Matos A, Ferreira-Leitão (2011) Simultaneous analysis of carbohydrates and volatile fatty acids by HPLC for monitoring fermentative biohydrogen production. Int J Hydrogen Energy 1–10

  33. US-EPA Method 3051A (2007), Microwave assisted acid digestion of sediments, sludges, soils and oils. In: Test methods for evaluating solid waste. US Environmental Protection Agency, Washington, DC, USA, 3rd edition

  34. Rao KS, Balaji T, Rao TP, Babu Y, Naidu GRK (2002) Determination of iron, cobalt, nickel, manganese, zinc, copper, cadmium and lead in human hair by inductively coupled plasma atomic emission spectrometry. Spectrochim Acta B 57:1333–1338

    Article  Google Scholar 

  35. Yang F, Hanna MA, Sun R (2012) Value-added uses for crude glycerol—a byproduct of biodiesel production. Biotechnol Biofuels 5:13

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Saldanha RL, Garcia JE, Dekker RFH, Vilas-Boas LA, Barbosa AM (2007) Genetic diversity among Botryosphaeria isolates and their correlation with cell wall-lytic enzyme production. Braz J Microbiol 38:259–264

    Article  Google Scholar 

  37. Scheller HV, Ulvskov P (2010) Hemicelluloses. Ann Rev Plant Biol 61:263–289

    Article  CAS  Google Scholar 

  38. Deutschmann R, Dekker RFH (2012) From plant biomass to bio-based chemicals: latest developments in xylan research. Biotechnol Adv 30:1627–1640

    Article  CAS  PubMed  Google Scholar 

  39. Dekker RFH, Karageorge H, Wallis AFA (1987) Pretreatment of hardwood (Eucalyptus regnans) sawdust by autohydrolysis explosion and its saccharification by Trichodermal cellulases. Biocatal Biotransfor 1:47–61

    Article  CAS  Google Scholar 

  40. Chua MGS, Wayman M (1979) Characterization of autohydrolysis aspen (Populus tremuloides) lignins. Part 1. Composition and molecular weight distribution of extracted autohydrolysis lignin. Can J Chem 57:1141–1149

    Article  CAS  Google Scholar 

  41. Leschinsky M, Webber HK, Patt R, Sixta H (2009) Formation of insoluble components during autohydrolysis of Eucalyptus globulus. Lenzinger Berichte 87:16–25

    CAS  Google Scholar 

  42. Stewart JJ, Kadla JF, Mansfield SD (2006) The influence of lignin chemistry and ultrastructure on the pulping efficiency of clonal aspen (Populus tremuloides Michx.). Holzforschung 60:111–122

    Article  CAS  Google Scholar 

  43. Vasconcelos AFD, Barbosa AM, Dekker RFH, Scarminio IS, Rezende MI (2000) Optimization of laccase production by Botryosphaeria sp. in the presence of veratryl alcohol by the response-surface method. Process Biochem 35:1131–1138

    Article  CAS  Google Scholar 

  44. Dekker RFH, Barbosa AM (2001) The effects of aeration and veratryl alcohol on the production of two laccases by the ascomycete Botryosphaeria sp. Enz Microb Technol 28:81–88

    Article  CAS  Google Scholar 

  45. Andrade MM, Barbosa AM, Bofinger MR, Dekker RFH, Messias JM, Guedes CL, Zaminelli T, de Oliveira BH, de Lima VM, Dall’Antonia LH (2013) Lipase production by Botryosphaeria ribis EC-01 on soybean and castorbean meals: optimization, immobilization, and application for biodiesel production. Appl Biochem Biotechnol 170:1792–1806

    Article  CAS  PubMed  Google Scholar 

  46. Couto SR, Rodríguez A, Paterson RRM, Lima N, Teixeira JA (2006) Laccase activity from the fungus Trametes hirsute using an air-lift bioreactor. Lett Appl Microbiol 42:612–616

    CAS  Google Scholar 

  47. Alves Da Cunha MA, Barbosa AM, Giese EC, Dekker RFH (2003) The effect of carbohydrate carbon sources on the production of constitutive and inducible laccases by Botryosphaeria sp. J Basic Microbiol 43:385–392

    Article  PubMed  Google Scholar 

  48. Palmieri G, Giardina P, Bianco C, Fontanella B, Sannia G (2000) Copper induction of laccase isoenzymes in the ligninolytic fungus Pleurotus ostreatus. Appl Environ Microbiol 2000:920–924

    Article  Google Scholar 

  49. Galhaup HD (2001) Enhanced formation of laccase activity by the white-rot fungus Trametes pubescens in the presence of copper. Appl Microbiol Biotechnol 56:225–232

    Article  CAS  PubMed  Google Scholar 

  50. Lacina C, Gourene G, Spiros AN (2003) Utilization of fungi for biotreatment of raw wastewaters. Afr J Biotechnol 2:620–630

    Article  Google Scholar 

  51. Palmqvist E, Hahn-Hӓgerdal B, Szengyel Z, Zacchi G, Rèczey K (1997) Simultaneous detoxification and enzyme production of hemicellulose hydrolysates obtained after steam pretreatment. Enzym Microb Technol 20:286–293

    Article  CAS  Google Scholar 

  52. Larsson S, Reimann A, Nilvebrant N-O, Jönsson LJ (1999) Comparison of different methods for the detoxification of lignocellulose hydrolyzates of spruce. Appl Biochem Biotechnol 77:91–103

    Article  Google Scholar 

  53. Nichols NN, Sharma LN, Mowery RA, Chambliss CK, Peter van Walsum G, Dien BS, Iten LB (2008) Fungal metabolism of fermentation inhibitors present in corn stover dilute acid hydrolysate. Enzym Microb Technol 42:624–630

    Article  CAS  Google Scholar 

  54. Basha KM, Rajendran A, Thangavelu V (2010) Recent advances in the biodegradation of phenol: a review. Asian J Exp Biol Sci 1:219–234

    CAS  Google Scholar 

  55. Al-Khalid T, El-Naas MH (2012) Aerobic biodegradation of phenols: a comprehensive review. Crit Rev Environ Sci Technol 42:1631–1690

    Article  CAS  Google Scholar 

  56. Ran H, Zhang J, Gao Q, Lin Z, Bao J (2014) Analysis of biodegradation performance of furfural and 5-hydroxymethylfurfural by Amorphotheca resinae ZN1. Biotechnol Biofuels 7:51

    Article  PubMed Central  PubMed  Google Scholar 

  57. Jurado M, Prieto A, Martínez-Alcalá A, Martínez AT, Martínez MJ (2009) Laccase detoxification of steam-exploded wheat straw for second-generation bioethanol. Bioresour Technol 100:6378–6384

    Article  CAS  PubMed  Google Scholar 

  58. Parawira W, Tekere M (2011) Biotechnological strategies to overcome inhibitors in lignocellulose hydrolysates for ethanol production: review. Crit Rev Biotechnol 31:20–31

    Article  CAS  PubMed  Google Scholar 

  59. Lee K-M, Kalyani D, Tiwari MK, Kim T-S, Dhiman SS, Lee J-K, Kim I-W (2012) Enhanced enzymatic hydrolysis of rice straw by removal of phenolic compounds using a novel laccase from yeast Yarrowia lipolytica. Bioresour Technol 123:636–645

    Article  CAS  PubMed  Google Scholar 

  60. Moreno AD, Ibarra D, Fernández JL, Ballesteros M (2012) Different laccase detoxification strategies for ethanol production from lignocellulosic biomass by the thermotolerant yeast Kluyvermoyces marxianus CECT 10875. Bioresour Technol 106:101–109

    Article  CAS  PubMed  Google Scholar 

  61. Alvira P, Moreno AD, Ibarra D, Sáez F, Ballesteros M (2013) Improving the fermentation performance of Saccharomyces cerevisiae by laccase during ethanol production from steam-exploded wheat straw at high-substrate loadings. Biotechnol Prog 29:74–82

    Article  CAS  PubMed  Google Scholar 

  62. Chandel AK, Kapoor RK, Singh A, Kuhad RC (2007) Detoxification of sugarcane baggase hydrolysate improves ethanol production by Candida shehate NCIM 3501. Bioresour Technol, 1947–1950

  63. Xu F, Shin W, Brown SH, Wahleithner JA, Sundaram U, Solomon EI (1996) A study of a series of recombinant fungal laccases and bilirubin oxidase that exhibit significant differences in redox potential, substrate specificity, and stability. Biochim Biophys Acta 1292:303–311

    Article  PubMed  Google Scholar 

  64. Desai SS, Nityanand C (2011) Microbial laccases and their applications: a review. Asian J Biotechnol 3:98–124

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge CRIBE (Center for Research and Innovation in the Bio-economy, Ontario, Canada) for a grant (RFH Dekker) that supported this work. Dr. Regis Benech, Dr. Stephan Brey, and Greg Santavy of Greenfield Engineering and Technology (Research and Development), Chatham (Canada), are thanked for providing the poplar prehydrolyzate samples. Dr. Rudi Deutschmann is acknowledged for providing data on the compositional analysis of the poplar woodchips. The authors gratefully acknowledge the technical expertise of Greg Kepka and Gamini Rupasingha for their assistance with the HPLC analyses.

Conflict of Interest

The authors declare that they have no competing interests.

Author information

Authors and Affiliations

  1. Biorefining Research Institute, Lakehead University, Thunder Bay, ON, P7B 5E1, Canada

    Lakmali Nilmini G. Vithanage, Aneli M. Barbosa & Robert F. H. Dekker

  2. Biorefining and Biotechnology Consultancy, Rua João Huss 200, Gleba Palhano, CEP 86050-490, Londrina, PR, Brazil

    Aneli M. Barbosa & Robert F. H. Dekker

  3. Departamento de Química-CCE, Universidade Estadual de Londrina, CEP 86050-990, Londrina, PR, Brazil

    Dionisio Borsato

Authors
  1. Lakmali Nilmini G. Vithanage
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aneli M. Barbosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dionisio Borsato
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robert F. H. Dekker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Robert F. H. Dekker.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vithanage, L.N.G., Barbosa, A.M., Borsato, D. et al. Value Adding of Poplar Hemicellulosic Prehydrolyzates: Laccase Production by Botryosphaeria rhodina MAMB-05 and Its Application in the Detoxification of Prehydrolyzates. Bioenerg. Res. 8, 657–674 (2015). https://doi.org/10.1007/s12155-014-9547-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12155-014-9547-0

Keywords

Search

Navigation