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Using a grass substrate to compare decay among two clades of brown rot fungi

  • Bioenergy and biofuels
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Abstract

Interest in the mechanisms of wood-degrading fungi has grown in tandem with lignocellulose bioconversion efforts, yet many potential biomass feedstocks are non-woody. Using corn stover (Zea mays) as a substrate, we tracked degradative capacities among brown rot fungi from the Antrodia clade, including Postia placenta, the first brown rot fungus to have its genome sequenced. Decay dynamics were compared against Gloeophyllum trabeum from the Gloeophyllum clade. Weight loss induced by P. placenta (6.2 %) and five other Antrodia clade isolates (average 7.4 %) on corn stalk after 12 weeks demonstrated inefficiency among these fungi, relative to decay induced by G. trabeum (44.4 %). Using aspen (Populus sp.) as a woody substrate resulted in, on average, a fourfold increase in weight loss induced by Antrodia clade fungi, while G. trabeum results matched those on stover. The sequence and trajectories of chemical constituent losses differed as a function of substrate but not fungal clade. Instead, chemical data suggest that characters unique to stover limit decay by the Antrodia clade, rather than disparities in growth rate or extractives toxicity. High p-coumaryl lignin content, lacking the methoxy groups characteristically cleaved during brown rot, is among potential rate-distinguishing characters in grasses. This ineptitude among Antrodia clade fungi on grasses was supported by meta-analysis of other unrelated studies using grass substrates. Concerning application, results expose a problem if adopting the strategy of the model decay fungus P. placenta to treat corn stover, a widely available plant feedstock. Overall, the results insinuate phylogenetically distinct modes of brown rot and demonstrate the benefit of using non-woody substrates to probe wood degradation mechanisms.

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References

  • Antai SP, Crawford DL (1982) Degradation of extract-free lignocelluloses by Coriolus versicolor and Poria placenta. Eur J Appl Microbiol Biotechnol 14:165–168

    Article  CAS  Google Scholar 

  • 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(2):323–338

    Article  PubMed  CAS  Google Scholar 

  • Arora DS (1995) Biodelignification of wheat straw by different fungal associations. Biodegradation 6:57–60

    Article  CAS  Google Scholar 

  • Buckeridge MS, Rayon C, Urbanowicz B, Tiné MAS, Carpita NC (2004) Mixed linkage (1→3), (1→4) –β-D-glucans of grasses. Cereal Chem 81(1):115–127

    Article  CAS  Google Scholar 

  • Chen SF, Mowery RA, Scarlata CJ, Chambliss CK (2007) Compositional analysis of water-soluble materials in corn stover. J Agric Food Chem 55(15):5912–5918

    Article  PubMed  CAS  Google Scholar 

  • Chen B, Gui F, Xie B, Deng Y, Sun X, Lin M, Tao Y, Li S (2013) Composition and expression of genes encoding carbohydrate enzymes in the straw-degrading mushroom Volvariella volvacea. PLoS One 8(3):e58780

    Article  PubMed  CAS  Google Scholar 

  • Clausen CA, Green F III, Woodward BM, Evans JW, DeGroot RC (2000) Correlation between oxalic acid production and copper tolerance in Wolfiporia cocos. Int Biodeterior Biodegrad 46:69–76

    Article  CAS  Google Scholar 

  • Cowling EB (1961) Comparative biochemistry of the decay of sweetgum sapwood by white-rot and brown-rot fungi. USDA Tech Bull 1258:1–79

    Google Scholar 

  • Daniel G, Volc J, Filonova L, Plíhal O, Kubátová E, Halada P (2007) Characteristics of Gloeophyllum trabeum alcohol oxidase, an extracellular source of H2O2 in brown rot decay of wood. Appl Environ Microbiol 73(19):6241–6253

    Article  PubMed  CAS  Google Scholar 

  • De Groot RC, Evans JW, Forsyth CM, Morrell JJ (1998) Soil-contact decay tests using small blocks - a procedural analysis (FPL-RP-113). USDA Forest Service, Forest Prod Lab, Madison, WI

  • Eastwood DC, Floudas D, Binder M, Majcherczyk A, Schneider P, Aerts A, Asiegbu FO, Baker SE, Barry K, Bendiksby M, Blumentritt M, Coutinho PM, Cullen D, de Vries RP, Gathman A, Goodell B, Henrissat B, Ihrmark K, Kauserud H, Kohler A, LaButti K, Lapidus A, Lavin JL, Lee Y-H, Lindquist E, Lilly W, Lucas S, Morin E, Murat C, Oguiza JA, Park J, Pisabarro AG, Riley R, Rosling A, Salamov A, Schmidt O, Schmutz J, Skrede I, Stenlid J, Wiebenga A, Xie X, Kües U, Hibbett DS, Hoffmeister D, Högberg N, Martin F, Grigoriev IV, Watkinson SC (2011) The plant cell wall-decomposing machinery underlies the functional diversity of forest fungi. Science 333:762–765

    Article  PubMed  CAS  Google Scholar 

  • Eslyn WE, Highley TL (1976) Decay resistance and susceptibility of sapwood of fifteen tree species. Phytopathology 66:1010–1017

    Article  Google Scholar 

  • European Standard EN-113 (1996) Wood preservatives—method of test for determining the protective effectiveness against wood destroying basidiomycetes—determination of the toxic values. European Committee for Standardization, Brussels

    Google Scholar 

  • Fengel D, Wegener G (1984) Wood: chemistry, ultrastructure, reactions. Walter de Gruyter, New York

    Google Scholar 

  • Filley TR, Cody GD, Goodell B, Jellison J, Noser C, Ostrofsky A (2001) Lignin demethylation and polysaccharide decomposition in spruce sapwood degraded by brown rot fungi. Org Geochem 33:111–124

    Article  Google Scholar 

  • Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martinez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM, de Vries RP, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Górecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens JA, Kallen N, Kersten P, Kohler A, Kües U, Kumar TKA, Kuo A, LaButti K, Larrondo LF, Lindquist E, Ling A, Lombard V, Lucas S, Lundell T, Martin R, McLaughlin DJ, Morgenstern I, Morin E, Murat C, Nagy LG, Nolan M, Ohm RA, Patyshakuliyeva A, Rokas A, Ruiz-Dueñas FJ, Sabat G, Salamov A, Samejima M, Schmutz J, Slot JC, St. John F, Stenlid J, Sun H, Sun S, Syed K, Tsang A, Wiebenga A, Young D, Pisabarro A, Eastwood DC, Martin F, Cullen D, Grigoriev IV, Hibbett DS (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336(6089):1715–1719

    Article  PubMed  CAS  Google Scholar 

  • Fry SC (1989) The structure and function of xyloglucan. J Exp Bot 40(1):1–11

    Article  CAS  Google Scholar 

  • Gao Z, Mori T, Kondo R (2012) The pretreatment of corn stover with Gloeophyllum trabeum KU-41 for enzymatic hydrolysis. Biotechnol Biofuels 5(1):1–11

    Google Scholar 

  • Gilbertson R, Ryvarden L (1988) North American polypores. Lubrecht and Cramer, New York

    Google Scholar 

  • Goodell B, Jellison J, Liu J, Daniel G, Paszczynski A, Fekete F, Krishnamurthy S, Jun L, Xu G (1997) Low molecular weight chelators and phenolic compounds isolated from wood decay fungi and their role in the fungal biodegradation of wood. J Biotechnol 53:133–162

    Article  CAS  Google Scholar 

  • Han G, Cheng W, Manning M, Eloy P (2012) Performance of zinc borate-treated oriented structural straw board against mold fungi, decay fungi, and termites—a preliminary trial. BioResources 7(3):2986–2995

    Google Scholar 

  • Hatakka AI (1983) Pretreatment of wheat straw by white-rot fungi for enzymic saccharification of cellulose. Eur J Appl Microbiol Biotechnol 18(6):350–357

    Article  CAS  Google Scholar 

  • Hibbett DS, Donoghue MJ (2001) Analysis of character correlations among wood decay mechanisms, mating systems, and substrate ranges in homobasidiomycetes. Syst Biol 50(2):215–242

    Article  PubMed  CAS  Google Scholar 

  • Highley TL (1978) How moisture and pit aspiration affect decay of wood by white-rot and brown-rot fungi. Mater Org 13:197–206

    Google Scholar 

  • Hoskinson RL, Karlen DL, Birrell SJ, Radtke CW, Wilhelm WW (2007) Engineering, nutrient removal, and feedstock conversion evaluations of four corn stover harvest scenarios. Biomass Bioenergy 31(2):126–136

    Article  CAS  Google Scholar 

  • Irwin D, Leathers TD, Greene RV, Wilson DB (2003) Corn fiber hydrolysis by Thermobifida fusca extracellular enzymes. Appl Microbiol Biotechnol 61(4):352–358

    PubMed  CAS  Google Scholar 

  • Kamdem DP, Pizzi A, Jermannaud A (2002) Durability of heat-treated wood. Holz Roh Werkst 60(1):1–6

    Article  CAS  Google Scholar 

  • Kelley SS, Jellison J, Goodell B (2002) Use of NIR and pyrolysis-MBMS coupled with multivariate analysis for detecting the chemical changes associated with brown-rot biodegradation of spruce wood. FEMS Microbiol Lett 209:107–111

    Article  PubMed  CAS  Google Scholar 

  • Kerem Z, Jensen KA, Hammel KE (1999) Biodegradative mechanism of the brown rot basidiomycete Gloeophyllum trabeum: evidence for an extracellular hydroquinone-driven Fenton reaction. FEBS Lett 446(1):49–54

    Article  PubMed  CAS  Google Scholar 

  • Koenigs JW (1974) Hydrogen peroxide and iron: a proposed system for decomposition of wood by brown-rot basidiomycetes. Wood Fiber Sci 6(1):66–80

    Google Scholar 

  • Liang Y, Sun W, Zhu YG, Christie P (2007) Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environ Pollut 147:422–428

    Article  PubMed  CAS  Google Scholar 

  • Ma JF (2004) Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Sci Plant Nutr 50(1):11–18

    Article  CAS  Google Scholar 

  • Martin SB, Dale JL (1980) Biodegradation of turf thatch with wood-decay fungi. Phytopathology 70:297–301

    Article  Google Scholar 

  • Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Duenas FJ, Martinez AT, Kersten P, Hammel KE, Vanden Wymelenberg A, Gaskell J, Lindquist E, Sabat G, BonDurant SS, Larrondo LF, Canessa P, Vicuna R, Yadav J, Doddapaneni H, Subramanian V, Pisabarro AG, Lavin JL, Oguiza JA, Master E, Henrissat B, Coutinho PM, Harris P, Magnuson JK, Baker SE, Bruno K, Kenealy W, Hoegger PJ, Kües U, Ramaiya P, Lucas S, Salamov A, Shapiro H, Tu H, Chee CL, Misra M, Xie G, Teter S, Yaver D, James T, Mokrejs M, Pospisek M, Grigoriev IV, Brettin T, Rokhsar D, Berka R, Cullen D (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci U S A 106(6):1954–1959

    Article  PubMed  CAS  Google Scholar 

  • Monrroy M, Ortega I, Ramírez M, Baeza J, Freer J (2011) Structural change in wood by brown rot fungi and effect on enzymatic hydrolysis. Enzyme Microb Tech 49:472–477

    Google Scholar 

  • 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 Bioenerg 34(8):1257–1262

    Google Scholar 

  • Ritschkoff AC, Viikari L (1991) The production of extracellular hydrogen peroxide by brown-rot fungi. Mater Org 26:157–167

    CAS  Google Scholar 

  • Saha BC, Woodward J (eds) (1997) Fuels and chemicals from biomass. ACS Symp Ser 666. American Chemical Society, Washington, DC

    Google Scholar 

  • Salvachúa D, Prieto A, López-Abelairas M, Lu-Chau T, Martínez AT, Martínez MJ (2011) Fungal pretreatment: an alternative in second-generation ethanol from wheat straw. Bioresour Technol 102:7500–7506

    Article  PubMed  Google Scholar 

  • Sarker P, Bosneaga E, Auer M (2009) Plant cell walls throughout evolution: towards a molecular understanding of their design principles. J Exp Bot 60(13):3615–3635

    Article  Google Scholar 

  • Schilling JS, Norcutt A (2010) Effects of wood mixtures on deterioration by a filamentous brown-rot fungus. Wood Fiber Sci 42(2):150–157

    CAS  Google Scholar 

  • Schilling JS, Ai J, Blanchette RA, Duncan SM, Filley TR, Tschirner UW (2012) Lignocellulose modifications by brown rot fungi and their effects, as pretreatments, on cellulolysis. Bioresour Technol 116:147–154

    Article  PubMed  CAS  Google Scholar 

  • Schmidt O, Wei DS, Liese W, Wollenberg E (2011) Fungal degradation of bamboo samples. Holzforschung 65:883–888

    Article  CAS  Google Scholar 

  • Shortle WC, Dudzik KR, Smith KT (2010) Development of wood decay in wound-initiated discolored wood of eastern red cedar. Holzforschung 64:529–536

    Article  CAS  Google Scholar 

  • Sluiter J, Sluiter A (2010) Summative mass closure—LAP review and integration: feedstocks (NREL/TP-510-48087). National Renewable Energy Laboratory, Golden

    Google Scholar 

  • Sluiter A, Hames B, Ruiz R, Scarlata C, Sluiter J, Templeton D (2005) Determination of ash in biomass (NREL/TP-510-42622). National Renewable Energy Laboratory, Golden

    Google Scholar 

  • Sluiter A, Ruiz R, Scarlata C, Sluiter J, Templeton D (2008a) Determination of extractives in biomass (NREL/TP-510-42619). National Renewable Energy Laboratory, Golden

    Google Scholar 

  • Sluiter A, Hames B, Ruiz R, Scarlata C, Sluiter J, Templeton D, Crocker D (2008b) Determination of structural carbohydrates and lignin in biomass (NREL/TP-510-42618). National Renewable Energy Laboratory, Golden

    Google Scholar 

  • Stangerlin DM, de Melo RR, Garlet A, Gatto DA (2011) Natural durability of Eucalyptus grandis and Bambusa vugaris particleboards under accelerated fungi decay test. Cienc Rural 41(8):1369–1374

    Article  Google Scholar 

  • Suprapti S (2010) Decay resistance of five Indonesian bamboo species against fungi. J Trop For Sci 22(3):287–294

    Google Scholar 

  • Tewalt J, Schilling J (2010) Assessment of saccharification efficacy in the cellulose system of the brown rot fungus Gloeophyllum trabeum. Appl Microbiol Biotechnol 86:1785–1793

    Google Scholar 

  • Torget R, Werdene P, Himmel M, Grohmann K (1990) Dilute acid pretreatment of short rotation woody and herbaceous crops. Appl Biochem Biotechnol 24(25):115–126

    Article  Google Scholar 

  • Troya MT, Rubio F, Prieto MJ, Lorenzo D, Fernández-Cabo JL, Schöftner R (2009) Natural durability of reed (Phragmites australis) against wood decay organisms: relation to other forest species. Invest Agrar-Sist R 18(3):289–295

    Google Scholar 

  • US DOE, Perlack RB, Stokes BJ (Leads) (2011) U.S. billion-ton update: biomass supply for a bioenergy and bioproducts industry (ORNL/TM-2011/224). Oak Ridge National Laboratory, Oak Ridge, TN

  • Vaidya A, Singh, T (2012) Pre-treatment of Pinus radiata substrates by basidiomycetes fungi to enhance enzymatic hydrolysis. Biotechnol Lett 34:1263–1267

    Google Scholar 

  • Vanden Wymelenberg A, Gaskell J, Mozuch M, BonDurant SS, Sabat G, Ralph J, Skyba O, Mansfield SD, Blanchette RA, Grigoriev IV, Kersten PJ, Cullen D (2011) Significant alteration of gene expression in wood decay fungi Postia placenta and Phanerochaete chrysosporium by plant species. Appl Environ Microbiol 77(13):4499–4507

    Article  PubMed  CAS  Google Scholar 

  • Vogel J (2008) Unique aspects of the grass cell wall. Curr Opin Plant Biol 11:301–307

    Article  PubMed  CAS  Google Scholar 

  • Worrall JJ, Anagnost SE, Zabel RA (1997) Comparison of wood decay among diverse lignicolous fungi. Mycologia 89(2):199–219

    Article  Google Scholar 

  • Zabel RA, Morrell JJ (1992) Wood microbiology: decay and its prevention. Academic, San Diego

    Google Scholar 

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Acknowledgments

Funding for this research was provided by the University of Minnesota Initiative for Renewable Energy and the Environment Early Career award RC-00008-11 through the Institute on the Environment, as well as generous support from the Buckman Foundation as a departmental (BBE) fellowship. The authors would like to thank undergraduate students Ms. Heather Connelly, Ms. Audrie Ayres, and Mr. Quinn O'Leary, for their assistance with composition characterization.

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  1. Department of Bioproducts and Biosystems Engineering, University of Minnesota, 2004 Folwell Avenue, Saint Paul, MN, 55108, USA

    Justin T. Kaffenberger & Jonathan S. Schilling

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Correspondence to Jonathan S. Schilling.

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Kaffenberger, J.T., Schilling, J.S. Using a grass substrate to compare decay among two clades of brown rot fungi. Appl Microbiol Biotechnol 97, 8831–8840 (2013). https://doi.org/10.1007/s00253-013-5142-0

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