期刊论文详细信息
Biotechnology for Biofuels
Effects of lignin modification on wheat straw cell wall deconstruction by Phanerochaete chrysosporium
Jijiao Zeng1  Deepak Singh1  Difeng Gao1  Shulin Chen1 
[1] Department of Biological Systems Engineering, Bioprocessing and Bioproduct Engineering Laboratory (BBEL), Washington State University, L.J. Smith 213, Pullman 99163, Washington, USA
关键词: Cellulase enzyme lignin;    Milled wood lignin;    Inter-unit linkages;    Solid-state NMR;    Cellulase absorption;    Lignin-carbohydrate complex;    White rot fungi;    Lignin degradation;    NMR;   
Others  :  1084239
DOI  :  10.1186/s13068-014-0161-3
 received in 2014-05-10, accepted in 2014-10-16,  发布年份 2014
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【 摘 要 】

Background

A key focus in sustainable biofuel research is to develop cost-effective and energy-saving approaches to increase saccharification of lignocellulosic biomass. Numerous efforts have been made to identify critical issues in cellulose hydrolysis. Aerobic fungal species are an integral part of the carbon cycle, equip the hydrolytic enzyme consortium, and provide a gateway for understanding the systematic degradation of lignin, hemicelluloses, and cellulose. This study attempts to reveal the complex biological degradation process of lignocellulosic biomass by Phanerochaete chrysosporium in order to provide new knowledge for the development of energy-efficient biorefineries.

Results

In this study, we evaluated the performance of a fungal biodegradation model, Phanerochaete chrysosporium, in wheat straw through comprehensive analysis. We isolated milled straw lignin and cellulase enzyme-treated lignin from fungal-spent wheat straw to determine structural integrity and cellulase absorption isotherms. The results indicated that P. chrysosporium increased the total lignin content in residual biomass and also increased the cellulase adsorption kinetics in the resulting lignin. The binding strength increased from 117.4 mL/g to 208.7 mL/g in milled wood lignin and from 65.3 mL/g to 102.4 mL/g in cellulase enzyme lignin. A detailed structural dissection showed a reduction in the syringyl lignin/guaiacyl lignin ratio and the hydroxycinnamate/lignin ratio as predominant changes in fungi-spent lignin by heteronuclear single quantum coherence spectroscopy.

Conclusion

P. chrysosporium shows a preference for degradation of phenolic terminals without significantly destroying other lignin components to unzip carbohydrate polymers. This is an important step in fungal growth on wheat straw. The phenolics presumably locate at the terminal region of the lignin moiety and/or link with hemicellulose to form the lignin-carbohydrate complex. Findings may inform the development of a biomass hydrolytic enzyme combination to enhance lignocellulosic biomass hydrolysis and modify the targets in plant cell walls.

【 授权许可】

   
2014 Zeng et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Chundawat SPS, Beckham GT, Himmel ME, Dale BE: Deconstruction of lignocellulosic biomass to fuels and chemicals. Annu Rev Chem Biomol Eng 2011, 2:121-145.
  • [2]Bonawitz ND, Chapple C: The genetics of lignin biosynthesis: connecting genotype to phenotype. Annu Rev Genet 2010, 44:337-363.
  • [3]Chundawat SPS, Donohoe BS, Da Costa SL, Elder T, Agarwal UP, Lu F, Ralph J, Himmel ME, Balan V, Dale BE: Multi-scale visualization and characterization of lignocellulosic plant cell wall deconstruction during thermochemical pretreatment. Energy Environ Sci 2011, 4:973-984.
  • [4]Grabber JH, Ralph J, Lapierre C, Barrière Y: Genetic and molecular basis of grass cell-wall degradability. I. Lignin-cell wall matrix interactions. C R Biol 2004, 327:455-465.
  • [5]Evtuguin DV, Amado FML: Application of electrospray ionization mass spectrometry to the elucidation of the primary structure of lignin. Macromol Biosci 2003, 3:339-343.
  • [6]Kim H, Ralph J, Akiyama T: Solution-state 2D NMR of ball-milled plant cell wall gels in DMSO-d6. Bio Energy Res 2008, 1:56-66.
  • [7]Kumar R, Wyman CE: Cellulase adsorption and relationship to features of corn stover solids produced by leading pretreatments. Biotechnol Bioeng 2009, 103:252-267.
  • [8]Tu M, Pan X, Saddler JN: Adsorption of cellulase on cellulolytic enzyme lignin from lodgepole pine. J Agric Food Chem 2009, 57:7771-7778.
  • [9]Ding S-Y, Liu Y-S, Zeng Y, Himmel ME, Baker JO, Bayer EA: How does plant cell wall nanoscale architecture correlate with enzymatic digestibility? Science 2012, 338:1055-1060.
  • [10]Studer MH, DeMartini JD, Davis MF, Sykes RW, Davison B, Keller M, Tuskan GA, Wyman CE: Lignin content in natural Populus variants affects sugar release. Proc Natl Acad Sci 2011, 108:6300-6305.
  • [11]Rollin JA, Zhu Z, Sathitsuksanoh N, Zhang YHP: Increasing cellulose accessibility is more important than removing lignin: a comparison of cellulose solvent-based lignocellulose fractionation and soaking in aqueous ammonia. Biotechnol Bioeng 2011, 108:22-30.
  • [12]Martinez D, Larrondo LF, Putnam N, Gelpke MDS, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F: Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP 78. Nat Biotechnol 2004, 22:695-700.
  • [13]Kirk TK, Higuchi T, Chang HM: Lignin biodegradation: microbiology, chemistry, and potential applications. CRC Press, Inc, Boca Raton, FL; 1980.
  • [14]Hatakka A: Biodegradation of Lignin. Wiley-VCH, WeinHeim, Germany; 2001.
  • [15]Geib SM, Filley TR, Hatcher PG, Hoover K, Carlson JE, Del Mar J-GM, Nakagawa-Izumi A, Sleighter RL, Tien M: Lignin degradation in wood-feeding insects. Proc Natl Acad Sci 2008, 105:12932-12937.
  • [16]Kirk TK, Farrell RL: Enzymatic “ combustion”: the microbial degradation of lignin. Annu Rev Microbiol 1987, 41:465-501.
  • [17]Ten Have R, Teunissen PJM: Oxidative mechanisms involved in lignin degradation by white-rot fungi. Chem Rev 2001, 101:3397-3414.
  • [18]Tien M, Kirk T: Lignin-degrading enzyme from the hymenomycete Phanerochaete chrysosporium Burds. Science 1983, 221:661.
  • [19]Tien M, Kirk TK: Lignin-degrading enzyme from Phanerochaete chrysosporium: purification, characterization, and catalytic properties of a unique H2O2-requiring oxygenase. Proc Natl Acad Sci 1984, 81:2280-2284.
  • [20]Hammel KE: Organopollutant degradation by ligninolytic fungi. Enzyme Microb Technol 1989, 11:776-777.
  • [21]Martinez AT, Speranza M, Ruiz-Duenas FJ, Ferreira P, Camarero S, Guillen F, Martinez MJ, Gutierrez A, Del Rio JC: Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Int Microbiol 2005, 8:195-204.
  • [22]Hildén L, Johansson G, Pettersson G, Li J, Ljungquist P, Henriksson G: Do the extracellular enzymes cellobiose dehydrogenase and manganese peroxidase form a pathway in lignin biodegradation? FEBS Lett 2000, 477:79-83.
  • [23]Singh D, Zeng J, Laskar DD, Deobald L, Hiscox WC, Chen S: Investigation of wheat straw biodegradation by Phanerochaete chrysosporium. Biomass Bioenergy 2011, 35:1030-1040.
  • [24]Chen S, Zhang X, Singh D, Yu H, Yang X: Biological pretreatment of lignocellulosics: potential, progress and challenges. Biofuels 2010, 1:177-199.
  • [25]Zeng J, Singh D, Laskar D, Chen S: Deconstruction of native wheat straw lignin by Streptomyces viridosporus T7A. Int J Environ Sci Technol 2012, 10:165-174.
  • [26]Renganathan V, Usha S, Lindenburg F: Cellobiose-oxidizing enzymes from the lignocellulose-degrading basidiomycete Phanerochaete chrysosporium: interaction with microcrystalline cellulose. Appl Microbiol Biotechnol 1990, 32:609-613.
  • [27]Bao W, Renganathan V: Cellobiose oxidase of Phanerochaete chrysosporium enhances crystalline cellulose degradation by cellulases. FEBS Lett 1992, 302:77-80.
  • [28]Adav SS, Ravindran A, Sze SK: Quantitative proteomic analysis of lignocellulolytic enzymes by Phanerochaete chrysosporium on different lignocellulosic biomass. J Proteomics 2011, 75:1493-1504.
  • [29]Manavalan A, Adav SS, Sze SK: iTRAQ-based quantitative secretome analysis of Phanerochaete chrysosporium. J Proteomics 2011, 75:642-654.
  • [30]Jeoh T, Ishizawa CI, Davis MF, Himmel ME, Adney WS, Johnson DK: Cellulase digestibility of pretreated biomass is limited by cellulose accessibility. Biotechnol Bioeng 2007, 98:112-122.
  • [31]Nakagame S, Chandra RP, Kadla JF, Saddler JN: The isolation, characterization and effect of lignin isolated from steam pretreated Douglas-fir on the enzymatic hydrolysis of cellulose. Bioresour Technol 2011, 102:4507-4517.
  • [32]Nakagame S, Chandra RP, Kadla JF, Saddler JN: Enhanceing the enzymatic hydrolysis of lignocellulosic biomass by increasing the carboxylic acid content of the associated lignin. Biotechnol Bioeng 2010, 108:538-548.
  • [33]Min D-y, Yang C, Chiang V, Jameel H, Chang H-m: The influence of lignin-carbohydrate complexes on the cellulase-mediated saccharification II: transgenic hybrid poplars (Populus nigra L. and Populus maximowiczii A.). Fuel 2014, 116:56-62.
  • [34]Palonen H, Valtion Teknillinen T: Role of lignin in the enzymatic hydrolysis of lignocellulose.PhD thesis. Otameida Espoo: VTT Technical Research Centre of Finland; 2004.
  • [35]Sewalt VJH, Glasser WG, Beauchemin KA: Lignin impact on fiber degradation. 3. Reversal of inhibition of enzymatic hydrolysis by chemical modification of lignin and by additives. J Agric Food Chem 1997, 45:1823-1828.
  • [36]Notenboom V, Boraston AB, Kilburn DG, Rose DR: Crystal structures of the family 9 carbohydrate-binding module from Thermotoga maritima xylanase 10A in native and ligand-bound forms. Biochemistry 2001, 40:6248-6256.
  • [37]Zeng J, Helms GL, Gao X, Chen S: Quantification of wheat straw lignin structure by comprehensive NMR analysis.J Agric Food Chem 2013, 61:
  • [38]Kim H, Ralph J: A gel-state 2D-NMR method for plant cell wall profiling and analysis: a model study with the amorphous cellulose and xylan from ball-milled cotton linters. RSC Advances 2014, 4:7549-7560.
  • [39]Li H, Pu Y, Kumar R, Ragauskas AJ, Wyman CE: Investigation of lignin deposition on cellulose during hydrothermal pretreatment, its effect on cellulose hydrolysis, and underlying mechanisms. Biotechnol Bioeng 2014, 111:485-492.
  • [40]Ragnar M, Lindgren CT, Nilvebrant NO: pKa-values of guaiacyl and syringyl phenols related to lignin. J Wood Chem Technol 2000, 20:277-305.
  • [41]Kishimoto T, Chiba W, Saito K, Fukushima K, Uraki Y, Ubukata M: Influence of syringyl to guaiacyl ratio on the structure of natural and synthetic lignins. J Agric Food Chem 2009, 58:895-901.
  • [42]Zhou C, Li Q, Chiang VL, Lucia LA, Griffis DP: Chemical and spatial differentiation of syringyl and guaiacyl lignins in poplar wood via time-of-flight secondary ion mass spectrometry. Anal Chem 2011, 83:7020-7026.
  • [43]Yan L, Li W, Yang J, Zhu Q: Direct visualization of straw cell walls by AFM. Macromol Biosci 2004, 4:112-118.
  • [44]Río Andrade JC, Rencoret Pazo J, Prinsen P, Martínez Ferrer AT, Ralph J, Gutiérrez Suarez A: Structural characterization of wheat straw lignin as revealed by analytical pyrolysis, 2D-NMR, and reductive cleavage methods. J Agric Food Chem 2012, 60:5922-5935.
  • [45]Zeng J, Singh D, Chen S: Biological pretreatment of wheat straw by Phanerochaete chrysosporium supplemented with inorganic salts. Bioresour Technol 2011, 102:3206-3214.
  • [46]Akin D, Sethuraman A, Morrison W, Martin S, Eriksson KEL: Microbial delignification with white rot fungi improves forage digestibility. Appl Environ Microbiol 1993, 59:4274-4282.
  • [47]Scalbert A, Monties B, Lallemand J-Y, Guittet E, Rolando C: Ether linkage between phenolic acids and lignin fractions from wheat straw. Phytochemistry 1985, 24:1359-1362.
  • [48]Ralph J, Grabber JH, Hatfield RD: Lignin-ferulate cross-links in grasses: active incorporation of ferulate polysaccharide esters into ryegrass lignins. Carbohydr Res 1995, 275:167-178.
  • [49]Lam T, Kadoya K, Iiyama K: Bonding of hydroxycinnamic acids to lignin: ferulic and p-coumaric acids are predominantly linked at the benzyl position of lignin, not the β-position, in grass cell walls. Phytochemistry 2001, 57:987-992.
  • [50]Hatakka A: Lignin-modifying enzymes from selected white-rot fungi: production and role in lignin degradation. FEMS Microbiol Rev 1994, 13:125-135.
  • [51]Cantarella M, Mucciante C, Cantarella L: Inactivating effects of lignin-derived compounds released during lignocellulosic biomass pretreatment on the endo-glucanase catalyzed hydrolysis of carboxymethylcellulose: a study in continuous stirred ultrafiltration-membrane reactor. Bioresour Technol 2014, 156:48-56.
  • [52]Bunzel M, Allerdings E, Ralph J, Steinhart H: Cross-linking of arabinoxylans via 8-8-coupled diferulates as demonstrated by isolation and identification of diarabinosyl 8-8 (cyclic)-dehydrodiferulate from maize bran. J Cereal Sci 2008, 47:29-40.
  • [53]Grabber JH, Hatfield RD, Ralph J, Zon J, Amrhein N: Ferulate cross-linking in cell walls isolated from maize cell suspensions. Phytochemistry 1995, 40:1077-1082.
  • [54]Grabber JH, Hatfield RD, Lu F, Ralph J: Coniferyl ferulate incorporation into lignin enhances the alkaline delignification and enzymatic degradation of cell walls. Biomacromolecules 2008, 9:2510-2516.
  • [55]Grabber JH, Mertens DR, Kim H, Funk C, Lu F, Ralph J: Cell wall fermentation kinetics are impacted more by lignin content and ferulate cross-linking than by lignin composition. J Sci Food Agric 2009, 89:122-129.
  • [56]Pinto PA, Dias AA, Fraga I, Marques G, Rodrigues MAM, Colaço J, Sampaio A, Bezerra RMF: Influence of ligninolytic enzymes on straw saccharification during fungal pretreatment. Bioresour Technol 2012, 111:261-267.
  • [57]Blanchette R, Otjen L, Carlson M: Lignin distribution in cell walls of birch wood decayed by white rot basidiomycetes. Phytopathology 1987, 77:684-690.
  • [58]Blanchette RA, Krueger EW, Haight JE, Akhtar M, Akin DE: Cell wall alterations in loblolly pine wood decayed by the white-rot fungus Ceriporiopsis subvermispora. J Biotechnol 1997, 53:203-213.
  • [59]Arantes V, Milagres AMF, Filley TR, Goodell B: Lignocellulosic polysaccharides and lignin degradation by wood decay fungi: the relevance of nonenzymatic Fenton-based reactions. J Ind Microbiol Biotechnol 2011, 38:541-555.
  • [60]Henriksson G, Johansson G, Pettersson G: A critical review of cellobiose dehydrogenases. J Biotechnol 2000, 78:93-113.
  • [61]Igarashi K, Samejima M, Saburi Y, Habu N, Eriksson KEL: Localization of cellobiose dehydrogenase in cellulose-grown cultures of Phanerochaete chrysosporium. Fungal Genet Biol 1997, 21:214-222.
  • [62]Henriksson G, Ander P, Pettersson B, Pettersson G: Cellobiose dehydrogenase (cellobiose oxidase) from Phanerochaete chrysosporium as a wood-degrading enzyme. Studies on cellulose, xylan and synthetic lignin. Appl Microbiol Biotechnol 1995, 42:790-796.
  • [63]Sluiter A, Hames B, Ruiz R, Scarlata C, Sluiter J, Templeton D, Crocker D: Determination of structural carbohydrates and lignin in biomass.Lab Anal Proced 2008,
  • [64]Gilardi G, Abis L, Cass AEG: Carbon-13 CP/MAS solid-state NMR and FT-IR spectroscopy of wood cell wall biodegradation. Enzyme Microb Technol 1995, 17:268-275.
  • [65]Park S, Baker JO, Himmel ME, Parilla PA, Johnson DK: Cellulose crystallinity index: measurement techniques and their impact on interpreting cellulase performance. Biotechnol Biofuels 2010, 3:1-10. BioMed Central Full Text
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