Abstract
The recalcitrance bottleneck of lignocellulosic materials presents a major challenge for biorefineries, including second-generation biofuel production. Because of their abundance in the northern hemisphere, softwoods, such as Norway spruce, are of major interest as a potential feedstock for biorefineries. In nature, softwoods are primarily degraded by basidiomycetous fungi causing brown rot. These fungi employ a non-enzymatic oxidative system to depolymerize wood cell wall components prior to depolymerization by a limited set of hydrolytic and oxidative enzymes. Here, it is shown that Norway spruce pretreated with two species of brown-rot fungi yielded more than 250% increase in glucose release when treated with a commercial enzyme cocktail and that there is a good correlation between mass loss and the degree of digestibility. A series of experiments was performed aimed at mimicking the brown-rot pretreatment, using a modified version of the Fenton reaction. A small increase in digestibility after pretreatment was shown where the aim was to generate reactive oxygen species within the wood cell wall matrix. Further experiments were performed to assess the possibility of performing pretreatment and saccharification in a single system, and the results indicated the need for a complete separation of oxidative pretreatment and saccharification. A more severe pretreatment was also completed, which interestingly did not yield a more digestible material. It was concluded that a biomimicking approach to pretreatment of softwoods using brown-rot fungal mechanisms is possible, but that there are additional factors of the system that need to be known and optimized before serious advances can be made to compete with already existing pretreatment methods.
Similar content being viewed by others
References
Agger JW et al (2014) Discovery of LPMO activity on hemicelluloses shows the importance of oxidative processes in plant cell wall degradation. Proc Natl Acad Sci USA 111(17):6287–6292
Arantes V, Goodell B (2014) Current understanding of brown-rot fungal biodegradation mechanisms: a review. In: Schultz TP, Goodell B, Nicholas DD (eds) Deterioration and protection of sustainable biomaterials. ACS Publications. Washington, DC, USA, pp 3–21
Arantes V, Qian Y, Milagres AM, Jellison J, Goodell B (2009) Effect of pH and oxalic acid on the reduction of Fe3+ by a biomimetic chelator and on Fe3+ desorption/adsorption onto wood: Implications for brown-rot decay. Int Biodeterior Biodegrad 63:478–483
Arantes V, Jellison J, Goodell B (2012) Peculiarities of brown-rot fungi and biochemical Fenton reaction with regard to their potential as a model for bioprocessing biomass. Appl Microbiol Biotechnol 94:323–338
Baldrian P, Valášková V (2008) Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol Rev 32:501–521
Bissaro B et al (2017) Oxidative cleavage of polysaccharides by monocopper enzymes depends on H2O2. Nat Chem Biol 13:1123
Chen Y, Stevens MA, Zhu Y, Holmes J, Xu H (2013) Understanding of alkaline pretreatment parameters for corn stover enzymatic saccharification. Biotechnol Biofuels 6(1):8
Couturier M et al (2018) Lytic xylan oxidases from wood-decay fungi unlock biomass degradation. Nat Chem Biol 14(3):306–310
Cowling EB (1961) Comparative biochemistry of the decay of sweetgum sapwood by white-rot and brown-rot fungi, vol 1258. US Department of Agriculture, Washington
Curling SF, Clausen CA, Winandy JE (2002) Relationships between mechanical properties, weight loss, and chemical composition of wood during incipient brown-rot decay. For Prod J 52:34
Eastwood DC et al (2011) The plant cell wall–decomposing machinery underlies the functional diversity of forest fungi. Science 333:762–765
Evans CS, Gallagher IM, Atkey PT, Wood DA (1991) Localisation of degradative enzymes in white-rot decay of lignocellulose. Biodegradation 2:93–106
Filley TR, Cody GD, Goodell B, Jellison J, Noser C, Ostrofsky A (2002) Lignin demethylation and polysaccharide decomposition in spruce sapwood degraded by brown rot fungi. Org Geochem 33(2):111–124
Floudas D et al (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719
Flournoy DS, Kirk TK, Highley T (1991) Wood decay by brown-rot fungi: changes in pore structure and cell wall volume Holzforschung. Int J Biol Chem Phys Technol Wood 45:383–388
Goodell B, Nakamura M, Jellison J (2014) The chelator mediated Fenton system in the brown rot fungi: details of the mechanism, and reasons why it has been ineffective as a biomimetic treatment in some biomass applications: a review. In: Jermer J (ed) Proceedings IRG/WP, St. George, Utah. USA, 2014. IRG/WP, p 8
Goodell B et al (2017) Modification of the nanostructure of lignocellulose cell walls via a non-enzymatic lignocellulose deconstruction system in brown rot wood-decay fungi. Biotechnol Biofuels 10:179. https://doi.org/10.1186/s13068-017-0865-2
Green F, Highley TL (1997) Mechanism of brown-rot decay: paradigm or paradox. Int Biodeterior Biodegrad 39:113–124
Hastrup ACS, Howell C, Jensen B, Green F III (2011) Non-enzymatic depolymerization of cotton cellulose by fungal mimicking metabolites. Int Biodeterior Biodegrad 65(3):553–559
He Y-C et al (2015) Enhancement of enzymatic saccharification of corn stover with sequential Fenton pretreatment and dilute NaOH extraction. Biores Technol 193:324–330
Himmel ME, Ding S-Y, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315:804–807
Hug SJ, Leupin O (2003) Iron-catalyzed oxidation of arsenic (III) by oxygen and by hydrogen peroxide: pH-dependent formation of oxidants in the Fenton reaction. Environ Sci Technol 37:2734–2742
Jensen KA Jr, Ryan ZC, Wymelenberg AV, Cullen D, Hammel KE (2002) An NADH: quinone oxidoreductase active during biodegradation by the brown-rot basidiomycete Gloeophyllum trabeum. Appl Environ Microbiol 68:2699–2703
Jung YH, Kim HK, Park HM, Park Y-C, Park K, Seo J-H, Kim KH (2015) Mimicking the Fenton reaction-induced wood decay by fungi for pretreatment of lignocellulose. Biores Technol 179:467–472
Kato DM, Elía N, Flythe M, Lynn BC (2014) Pretreatment of lignocellulosic biomass using Fenton chemistry. Biores Technol 162:273–278
Kirk T, Highley T (1973) Quantitative changes in structural components of conifer woods during decay by white-and brown-rot fungi. Phytopathology 63:1338–1342
Ko JK, Kim Y, Ximenes E, Ladisch MR (2015) Effect of liquid hot water pretreatment severity on properties of hardwood lignin and enzymatic hydrolysis of cellulose. Biotechnol Bioeng 112(2):252–262
Lee J-W, Kim H-Y, Koo B-W, Choi D-H, Kwon M, Choi I-G (2008) Enzymatic saccharification of biologically pretreated Pinus densiflora using enzymes from brown rot fungi. J Biosci Bioeng 106:162–167
Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 6:41
Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2013) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495
Martinez D et al (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci 106:1954–1959
Michalska K, Miazek K, Krzystek L, Ledakowicz S (2012) Influence of pretreatment with Fenton’s reagent on biogas production and methane yield from lignocellulosic biomass. Biores Technol 119:72–78
Moilanen U, Kellock M, Várnai A, Andberg M, Viikari L (2014) Mechanisms of laccase-mediator treatments improving the enzymatic hydrolysis of pre-treated spruce. Biotechnol Biofuels 7:177
Noriega OAU (2016) Sistemas oxidativos e biomiméticos aplicados à hidrólise enzimática de materiais lignocelulósicos. (Oxidative-biomimetic systems applied to enzymatic hydrolysis of lignocellulosic materials). Ph.D. University of São Paulo. Lorena Campus, Brazil
Ogner G et al (1999) The chemical analysis program of the Norwegian Forest Research Institute 2000. Internal report
Orejuela LM (2017) Lignocellulose deconstruction using glyceline and a chelator-mediated Fenton system. Ph.D., Virginia Polytechnic Institute and State University
Palmqvist E, Hahn-Hägerdal B (2000) Fermentation of lignocellulosic hydrolysates. II: inhibitors and mechanisms of inhibition. Bioresour Technol 74:25–33
Paszczynski A, Crawford R, Funk D, Goodell B (1999) De Novo synthesis of 4,5-dimethoxycatechol and 2,5-dimethoxyhydroquinone by the brown rot fungus Gloeophyllum trabeum. Appl Environ Microbiol 65:674–679
Pedersen M, Meyer AS (2010) Lignocellulose pretreatment severity–relating pH to biomatrix opening. New Biotechnol 27:739–750
Presley GN, Schilling JS (2017) Distinct growth and secretome strategies by two taxonomically-divergent brown rot fungi. Appl Environ Microbiol 83(7):e02987–16. https://doi.org/10.1128/AEM.02987-16
Prousek J (2007) Fenton chemistry in biology and medicine. Pure Appl Chem 79:2325–2338
Ray MJ, Leak DJ, Spanu PD, Murphy RJ (2010) Brown rot fungal early stage decay mechanism as a biological pretreatment for softwood biomass in biofuel production. Biomass Bioenergy 34:1257–1262
Riley R et al (2014) Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proc Natl Acad Sci 111:9923–9928
Rodrigues AC, Haven MØ, Lindedam J, Felby C, Gama M (2015) Celluclast and Cellic® CTec2: saccharification/fermentation of wheat straw, solid–liquid partition and potential of enzyme recycling by alkaline washing. Enzyme Microb Technol 79:70–77
Sluiter A, Hames B, Ruiz R, Scarlata C, Sluiter J, Templeton D, Crocker D (2008) Determination of structural carbohydrates and lignin in biomass. Lab Anal Proced 1617:1–16
Vlasenko E et al (2010) Substrate specificity of family 5, 6, 7, 9, 12, and 45 endoglucanases. Biores Technol 101(7):2405–2411
Xu G, Goodell B (2001) Mechanisms of wood degradation by brown-rot fungi: chelator-mediated cellulose degradation and binding of iron by cellulose. J Biotechnol 87:43–57
Yang H et al (2016) Cell wall targeted in planta iron accumulation enhances biomass conversion and seed iron concentration in Arabidopsis and rice. Plant Biotechnol J 14:1998–2009. https://doi.org/10.1111/pbi.12557
Yelle DJ, Ralph J, Lu F, Hammel KE (2008) Evidence for cleavage of lignin by a brown rot basidiomycete. Environ Microbiol 10(7):1844–1849
Zhang J et al (2016) Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungus Postia placenta. Proc Natl Acad Sci 113(39):10968–10973
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 Biorefin 6:465–482
Acknowledgements
This work was financed by the Research Council of Norway 243663/E50 BioMim and the Norwegian Institute for Bioeconomy Research.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hegnar, O.A., Goodell, B., Felby, C. et al. Challenges and opportunities in mimicking non-enzymatic brown-rot decay mechanisms for pretreatment of Norway spruce. Wood Sci Technol 53, 291–311 (2019). https://doi.org/10.1007/s00226-019-01076-1
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00226-019-01076-1