Novel enzymes for the degradation of cellulose

The bulk terrestrial biomass resource in a future bio-economy will be lignocellulosic biomass, which is recalcitrant and challenging to process. Enzymatic conversion of polysaccharides in the lignocellulosic biomass will be a key technology in future biorefineries and this technology is currently the subject of intensive research. We describe recent developments in enzyme technology for conversion of cellulose, the most abundant, homogeneous and recalcitrant polysaccharide in lignocellulosic biomass. In particular, we focus on a recently discovered new type of enzymes currently classified as CBM33 and GH61 that catalyze oxidative cleavage of polysaccharides. These enzymes promote the efficiency of classical hydrolytic enzymes (cellulases) by acting on the surfaces of the insoluble substrate, where they introduce chain breaks in the polysaccharide chains, without the need of first “extracting” these chains from their crystalline matrix.

[1]  K. Eriksson,et al.  Cellobiose dehydrogenase enhances Phanerochaete chrysosporium cellobiohydrolase I activity by relieving product inhibition. , 1998, European journal of biochemistry.

[2]  T. Hayakawa,et al.  Increased baculovirus susceptibility of armyworm larvae feeding on transgenic rice plants expressing an entomopoxvirus gene , 1999, Nature Biotechnology.

[3]  V. Eijsink,et al.  An Oxidative Enzyme Boosting the Enzymatic Conversion of Recalcitrant Polysaccharides , 2010, Science.

[4]  Christopher H. Chang,et al.  The energy landscape for the interaction of the family 1 carbohydrate-binding module and the cellulose surface is altered by hydrolyzed glycosidic bonds. , 2009, The journal of physical chemistry. B.

[5]  P. B. Pope,et al.  Metagenomics of the Svalbard Reindeer Rumen Microbiome Reveals Abundance of Polysaccharide Utilization Loci , 2012, PloS one.

[6]  M. Bunzel.  Chemistry and occurrence of hydroxycinnamate oligomers , 2010, Phytochemistry Reviews.

[7]  A. Mackenzie,et al.  Cleavage of cellulose by a CBM33 protein , 2011, Protein science : a publication of the Protein Society.

[8]  L. Lo Leggio,et al.  Stimulation of lignocellulosic biomass hydrolysis by proteins of glycoside hydrolase family 61: structure and function of a large, enigmatic family. , 2010, Biochemistry.

[9]  L. Viikari,et al.  Synergistic action of xylanase and mannanase improves the total hydrolysis of softwood. , 2011, Bioresource technology.

[10]  K. Brown,et al.  Cloning, expression, and characterization of a cellobiose dehydrogenase from Thielavia terrestris induced under cellulose growth conditions. , 2012, Biochimica et biophysica acta.

[11]  B. Synstad,et al.  The Non-catalytic Chitin-binding Protein CBP21 from Serratia marcescens Is Essential for Chitin Degradation*♦ , 2005, Journal of Biological Chemistry.

[12]  J. Eyzaguirre,et al.  Action of xylan deacetylating enzymes on monoacetyl derivatives of 4-nitrophenyl glycosides of β-D-xylopyranose and α-L-arabinofuranose. , 2011, Journal of biotechnology.

[13]  Rajai H. Atalla,et al.  Influence of hemicelluloses on the aggregation patterns of bacterial cellulose , 1995 .

[14]  A. Meyer,et al.  Evaluation of Minimal Trichoderma reesei Cellulase Mixtures on Differently Pretreated Barley Straw Substrates , 2007, Biotechnology progress.

[15]  P. Fairley.  Introduction: Next generation biofuels , 2011, Nature.

[16]  Brandi L. Cantarel,et al.  The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics , 2008, Nucleic Acids Res..

[17]  D J Cosgrove,et al.  Molecular cloning and sequence analysis of expansins--a highly conserved, multigene family of proteins that mediate cell wall extension in plants. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[18]  V. Eijsink,et al.  Crystal Structure and Binding Properties of the Serratia marcescens Chitin-binding Protein CBP 21 * , 2005 .

[19]  Piotr Oleskowicz-Popiel,et al.  The challenge of enzyme cost in the production of lignocellulosic biofuels. , 2012, Biotechnology and bioengineering.

[20]  A. Koivula,et al.  Cellulose-binding domains promote hydrolysis of different sites on crystalline cellulose. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[21]  M. Penttilä,et al.  Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. , 2002, European journal of biochemistry.

[22]  David K. Johnson,et al.  Effects of alkaline or liquid-ammonia treatment on crystalline cellulose: changes in crystalline structure and effects on enzymatic digestibility , 2011, Biotechnology for biofuels.

[23]  C. Felby,et al.  Production and effect of aldonic acids during enzymatic hydrolysis of lignocellulose at high dry matter content , 2012, Biotechnology for Biofuels.

[24]  D. Haltrich,et al.  Cellobiose dehydrogenase--a flavocytochrome from wood-degrading, phytopathogenic and saprotropic fungi. , 2006, Current protein & peptide science.

[25]  A. Salamov,et al.  The Plant Cell Wall–Decomposing Machinery Underlies the Functional Diversity of Forest Fungi , 2011, Science.

[26]  G. Phillips,et al.  Restructuring the crystalline cellulose hydrogen bond network enhances its depolymerization rate. , 2011, Journal of the American Chemical Society.

[27]  D. Wilson,et al.  Synergistic interactions in cellulose hydrolysis , 2012 .

[28]  E. Reese,et al.  THE BIOLOGICAL DEGRADATION OF SOLUBLE CELLULOSE DERIVATIVES AND ITS RELATIONSHIP TO THE MECHANISM OF CELLULOSE HYDROLYSIS , 1950, Journal of bacteriology.

[29]  André Faaij,et al.  Production of advanced biofuels. , 2006 .

[30]  Sandy Merino,et al.  Progress and challenges in enzyme development for biomass utilization. , 2007, Advances in biochemical engineering/biotechnology.

[31]  V. T. Forsyth,et al.  Nanostructure of cellulose microfibrils in spruce wood , 2011, Proceedings of the National Academy of Sciences.

[32]  S. Clarke,et al.  A Novel 3-Methylhistidine Modification of Yeast Ribosomal Protein Rpl3 Is Dependent upon the YIL110W Methyltransferase* , 2010, The Journal of Biological Chemistry.

[33]  Harry Brumer,et al.  How the walls come crumbling down: recent structural biochemistry of plant polysaccharide degradation. , 2008, Current opinion in plant biology.

[34]  L. Skibsted,et al.  Identification and quantification of radical reaction intermediates by electron spin resonance spectrometry of laccase-catalyzed oxidation of wood fibers from beech (Fagus sylvatica) , 1997, Applied Microbiology and Biotechnology.

[35]  J. Ståhlberg,et al.  The Putative Endoglucanase PcGH61D from Phanerochaete chrysosporium Is a Metal-Dependent Oxidative Enzyme that Cleaves Cellulose , 2011, PloS one.

[36]  J. Büchs,et al.  How recombinant swollenin from Kluyveromyces lactis affects cellulosic substrates and accelerates their hydrolysis , 2011, Biotechnology for biofuels.

[37]  C. Divne,et al.  The heme domain of cellobiose oxidoreductase: a one-electron reducing system. , 2003, Biochimica et biophysica acta.

[38]  M. Sandgren,et al.  The first structure of a glycoside hydrolase family 61 member, Cel61B from Hypocrea jecorina, at 1.6 A resolution. , 2008, Journal of molecular biology.

[39]  K. Miyamoto,et al.  Disintegration of the peritrophic membrane of silkworm larvae due to spindles of an entomopoxvirus. , 2003, Journal of invertebrate pathology.

[40]  José C del Río,et al.  Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. , 2005, International microbiology : the official journal of the Spanish Society for Microbiology.

[41]  Bruce E Dale,et al.  Deconstruction of lignocellulosic biomass to fuels and chemicals. , 2011, Annual review of chemical and biomolecular engineering.

[42]  H. Gilbert,et al.  Carbohydrate-binding modules promote the enzymatic deconstruction of intact plant cell walls by targeting and proximity effects , 2010, Proceedings of the National Academy of Sciences.

[43]  Staffan Persson,et al.  Toward a Systems Approach to Understanding Plant Cell Walls , 2004, Science.

[44]  J. Saddler,et al.  Cellulose accessibility limits the effectiveness of minimum cellulase loading on the efficient hydrolysis of pretreated lignocellulosic substrates , 2011, Biotechnology for biofuels.

[45]  W. Mabee,et al.  Substrate pretreatment: the key to effective enzymatic hydrolysis of lignocellulosics? , 2007, Advances in biochemical engineering/biotechnology.

[46]  C. Hori,et al.  Effects of xylan and starch on secretome of the basidiomycete Phanerochaete chrysosporium grown on cellulose. , 2011, FEMS microbiology letters.

[47]  A. Darke,et al.  Structural aspects of the interaction of mannan-based polysaccharides with bacterial cellulose , 1998 .

[48]  Tracy Palmer,et al.  The complex extracellular biology of Streptomyces. , 2010, FEMS microbiology reviews.

[49]  Markus Pauly,et al.  Cell-wall carbohydrates and their modification as a resource for biofuels. , 2008, The Plant journal : for cell and molecular biology.

[50]  E. Birney,et al.  Pfam: the protein families database , 2013, Nucleic Acids Res..

[51]  B Henrissat,et al.  A classification of glycosyl hydrolases based on amino acid sequence similarities. , 1991, The Biochemical journal.

[52]  Jamie H. D. Cate,et al.  Structural basis for substrate targeting and catalysis by fungal polysaccharide monooxygenases. , 2012, Structure.

[53]  Feng Xu,et al.  Oxidoreductive Cellulose Depolymerization by the Enzymes Cellobiose Dehydrogenase and Glycoside Hydrolase 61 , 2011, Applied and Environmental Microbiology.

[54]  J. O. Baker,et al.  Cellobiohydrolase Hydrolyzes Crystalline Cellulose on Hydrophobic Faces , 2011, The Journal of Biological Chemistry.

[55]  G. Walker.  125th Anniversary Review: Fuel Alcohol: Current Production and Future Challenges , 2011 .

[56]  Tuula T. Teeri,et al.  The roles and function of cellulose-binding domains , 1997 .

[57]  T. Koshijima,et al.  Ester linkages between lignin and glucuronoxylan in a lignin-carbohydrate complex from beech (Fagus crenata) wood , 1988, Wood Science and Technology.

[58]  S. Tringe,et al.  Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen , 2011, Science.

[59]  G. Fincher,et al.  Xyloglucan xyloglucosyl transferases from barley (Hordeum vulgare L.) bind oligomeric and polymeric xyloglucan molecules in their acceptor binding sites. , 2010, Biochimica et biophysica acta.

[60]  L. Lo Leggio,et al.  Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components , 2011, Proceedings of the National Academy of Sciences.

[61]  V. Eijsink,et al.  Towards new enzymes for biofuels: lessons from chitinase research. , 2008, Trends in biotechnology.

[62]  R. Parthasarathi,et al.  Insights into hydrogen bonding and stacking interactions in cellulose. , 2011, The journal of physical chemistry. A.

[63]  Clare McCabe,et al.  Multiple Functions of Aromatic-Carbohydrate Interactions in a Processive Cellulase Examined with Molecular Simulation* , 2011, The Journal of Biological Chemistry.

[64]  A. Margolles,et al.  Lactobacillus plantarum Extracellular Chitin-Binding Protein and Its Role in the Interaction between Chitin, Caco-2 Cells, and Mucin , 2010, Applied and Environmental Microbiology.

[65]  Richard A Dixon,et al.  Lignin modification improves fermentable sugar yields for biofuel production , 2007, Nature Biotechnology.

[66]  J. Heider,et al.  Microbial degradation of aromatic compounds — from one strategy to four , 2011, Nature Reviews Microbiology.

[67]  D. Bolam,et al.  Carbohydrate-binding modules: fine-tuning polysaccharide recognition. , 2004, The Biochemical journal.

[68]  S. Gåseidnes,et al.  Characterization of the chitinolytic machinery of Enterococcus faecalis V583 and high-resolution structure of its oxidative CBM33 enzyme. , 2012, Journal of molecular biology.

[69]  V. Eijsink,et al.  Measuring processivity. , 2012, Methods in enzymology.

[70]  D. Argyropoulos,et al.  Microwave-assisted lignin isolation using the enzymatic mild acidolysis (EMAL) protocol. , 2008, Journal of agricultural and food chemistry.

[71]  Danièle Revel,et al.  IPCC Special Report on Renewable Energy Sources and Climate Change Mitigation , 2011 .

[72]  Jamie H. D. Cate,et al.  Oxidative cleavage of cellulose by fungal copper-dependent polysaccharide monooxygenases. , 2012, Journal of the American Chemical Society.

[73]  S. Sze,et al.  Quantitative proteomic analysis of lignocellulolytic enzymes by Phanerochaete chrysosporium on different lignocellulosic biomass. , 2012, Journal of proteomics.

[74]  S. Persson,et al.  Cellulose synthases and synthesis in Arabidopsis. , 2011, Molecular plant.

[75]  J.-F. Cheng,et al.  Adaptation to herbivory by the Tammar wallaby includes bacterial and glycoside hydrolase profiles different from other herbivores , 2010, Proceedings of the National Academy of Sciences.

[76]  B. Henrissat,et al.  Structures and mechanisms of glycosyl hydrolases. , 1995, Structure.

[77]  L. Holm,et al.  The Pfam protein families database , 2005, Nucleic Acids Res..

[78]  Jamie H. D. Cate,et al.  Cellobiose dehydrogenase and a copper-dependent polysaccharide monooxygenase potentiate cellulose degradation by Neurospora crassa. , 2011, ACS chemical biology.

[79]  Xiaochao Xiong,et al.  A Novel Biochemical Route for Fuels and Chemicals Production from Cellulosic Biomass , 2012, PloS one.

[80]  E. Reese.  Enzymatic Hydrolysis of Cellulose , 1956 .

[81]  J. Sugiyama,et al.  The binding specificity and affinity determinants of family 1 and family 3 cellulose binding modules , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[82]  T. Wood,et al.  Synergism Between Enzymes Involved in the Solubilization of Native Cellulose , 1979 .

[83]  Baron Peters,et al.  Molecular-level origins of biomass recalcitrance: decrystallization free energies for four common cellulose polymorphs. , 2011, The journal of physical chemistry. B.

[84]  Felix Moser,et al.  Regulation and characterization of Thermobifida fusca carbohydrate‐binding module proteins E7 and E8 , 2008, Biotechnology and bioengineering.

[85]  Jacqueline MacDonald,et al.  Transcriptomic Responses of the Softwood-Degrading White-Rot Fungus Phanerochaete carnosa during Growth on Coniferous and Deciduous Wood , 2011, Applied and Environmental Microbiology.

[86]  B. Synstad,et al.  Costs and benefits of processivity in enzymatic degradation of recalcitrant polysaccharides , 2006, Proceedings of the National Academy of Sciences.

[87]  T. Houfek,et al.  Transcriptional Regulation of Biomass-degrading Enzymes in the Filamentous Fungus Trichoderma reesei* , 2003, Journal of Biological Chemistry.

[88]  H. Koley,et al.  Intestinal Adherence of Vibrio cholerae Involves a Coordinated Interaction between Colonization Factor GbpA and Mucin , 2008, Infection and Immunity.

[89]  D. Brede,et al.  The Transcriptome of the Nosocomial Pathogen Enterococcus faecalis V583 Reveals Adaptive Responses to Growth in Blood , 2009, PloS one.

[90]  D. V. van Aalten,et al.  Crystal Structure and Binding Properties of the Serratia marcescens Chitin-binding Protein CBP21* , 2005, Journal of Biological Chemistry.

[91]  Norma H. Pawley,et al.  Exploring new strategies for cellulosic biofuels production , 2011 .

[92]  Igor Grigoriev,et al.  Comparative Transcriptome and Secretome Analysis of Wood Decay Fungi Postia placenta and Phanerochaete chrysosporium , 2010, Applied and Environmental Microbiology.

[93]  Anne S Meyer,et al.  Enzymatic xylose release from pretreated corn bran arabinoxylan: differential effects of deacetylation and deferuloylation on insoluble and soluble substrate fractions. , 2010, Journal of agricultural and food chemistry.

[94]  Michael F. Crowley,et al.  Decrystallization of Oligosaccharides from the Cellulose Iβ Surface with Molecular Simulation , 2011 .