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The Relation Between the Supramolecular Structure of Cellulose and Its Hydrolysability

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The Relation Between the Supramolecular Structure of Cellulose and Its Hydrolysability THESIS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY The relation between the supramolecular structure of cellulose and its hydrolysability AUSRA PECIULYTE Department of Biology and Biological Engineering CHALMERS UNIVERSITY OF TECHNOLOGY Gothenburg, Sweden 2015 The relation between the supramolecular structure of cellulose and its hydrolysability AUSRA PECIULYTE ISBN 978‐91‐7597‐301‐2 ©AUSRA PECIULYTE, 2015 Doktorsavhandlingar vid Chalmers tekniska högskola. Ny serie nr 3982 ISSN 0346‐718X Division of Industrial Biotechnology Department of Biology and Biological Engineering Chalmers University of Technology SE‐412 96 Gothenburg Sweden Telephone + 46 (0)31‐772 1000 Cover: Illustration of supramolecular structure of cellulose. Printed by Chalmers Reproservice Gothenburg, Sweden 2015 ii The relation between the supramolecular structure of cellulose and its hydrolysability AUSRA PECIULYTE Division of Industrial Biotechnology Department of Biology and Biological Engineering Chalmers University of Technology ABSTRACT The liberation of fermentable sugars from cellulosic biomass during enzymatic hydrolysis is often incomplete. One of the factors limiting the efficiency of enzymatic hydrolysis is the structural properties of cellulose. The aim of the work presented in this thesis was to increase our understanding of the relation between enzymatic hydrolysis and the structural properties of cellulosic substrates. The enzymatic hydrolysis of a number of cellulosic substrates derived from softwood preparations used in the pulp and paper industry, as well as model substrates, were studied. The differences in cellulosic substrates before and after enzymatic hydrolysis are described on the nanometre scale in terms of their supramolecular structure, i.e. the lateral dimensions of fibrils and fibril aggregates, the accessible surface area, the crystallinity and porosity, using solid-state nuclear magnetic resonance spectroscopy. The substrates were imaged and structural changes in the cellulosic substrates were characterized in real time on the micrometre scale in terms of their molecular density, ordering and autofluorescence, employing nonlinear optical microscopy. A strong correlation was found between the average pore size and the specific surface area of the starting material and the enzymatic conversion yield. The overall degree of crystallinity and the lateral dimensions of the fibrils increased in some samples as a result of hydrolysis. Avicel had a higher carbon–hydrogen bond density and a different pattern of ordered structures than the never-dried pulp fibres, possibly reflecting the collapse of the macromolecular structures during drying and rewetting. Monitoring of the substrates during enzymatic hydrolysis revealed substrate- characteristic hydrolysis pattern. The response of the most widely studied filamentous fungus for cellulase production, Trichoderma reesei, to cellulosic substrates with different supramolecular structures was studied. Substantial differences were found in the profile of the enzymes produced, despite the fact that there were only minor differences in the chemical composition of the cellulose-rich substrates. Culture filtrates from five filamentous fungi cultivations were evaluated regarding their ability to improve saccharification of the industrial cellulase cocktail Celluclast 1.5L. It was demonstrated that supplementing commercial cocktails with enzymes from carefully selected fungi can result in significantly more efficient saccharification of biomass. Keywords: CARS, Cellulases, Cellulose I, SHG, CP/MAS 13C-NMR, Imaging, MPEF, Secretomics, Trichoderma reesei iii List of publications This thesis is based on the work described in the following papers: Paper I: Peciulyte A, Karlström K, Larsson P T and Olsson L. Impact of the supramolecular structure of cellulose on the efficiency of enzymatic hydrolysis. Biotechnol. Biofuels 2015; 8:56. Paper II: Peciulyte A*, Kiskis J*, Larsson P T, Olsson L and Enejder A. Visualization of structural changes in cellulosic substrates during enzymatic hydrolysis using multimodal nonlinear microscopy Submitted Paper III: Peciulyte A, Anasontzis G E, Karlström K, Larsson P T and Olsson L. Morphology and enzyme production of Trichoderma reesei Rut C-30 are affected by the physical and structural characteristics of cellulosic substrates. Fungal Genet. Biol. 2014; 72:64-72. Paper IV: Peciulyte A, Pisano M, de Vries R P and Olsson L. Hydrolytic potential of different fungal crude extracts to enhance a commercial enzyme cocktail Submitted * These authors contributed equally to the study Published paper not included in this thesis Aldaeus, F, Larsson, K, Srndovic, J S, Kubat, M, Karlström, K, Peciulyte, A, Olsson, L, Larsson, P T. The supramolecular structure of cellulose-rich wood pulps can be a determinative factor for enzymatic hydrolysability. Cellulose, 2015; 22: 3991-4002. iv The author’s contributions Paper I: I designed and carried out the experimental work apart from the CP/MAS 13C-NMR analysis. I analysed the results and wrote the manuscript. Paper II: I, together with Juris Kiskis, developed the idea and designed the experimental set-up. I was responsible for the enzymatic hydrolysis part and Juris Kiskis performed the microscopy measurements. I, together with Juris Kiskis, participated in all the experiments and the measurements, analysed the data, and wrote the manuscript. Paper III: I designed and carried out the experimental work apart from the proteomic analysis; I analysed the results and wrote the manuscript. Paper IV: I designed the work, supervised Maria Pisano who performed the screening of the fungal strains, and I performed the rest of the experiments. I analysed the results and wrote the manuscript. v Preface This research was carried out according to the requirements for the degree of Doctor of Philosophy at the Department of Biology and Biological Engineering, Chalmers University of Technology, Sweden. The project was initiated in June 2011. The research was carried out under the supervision of Professor Lisbeth Olsson, Chalmers University of Technology, and Associate Professor Per Tomas Larsson, Innventia AB. Per Tomas Larsson provided expertise on high-resolution solid-state NMR and the supramolecular structure of cellulose. Lisbeth Olsson and I were responsible for the biological perspective, focusing on enzymes, fungal physiology and the enzymatic hydrolysis of cellulose. The work described in this thesis was performed in collaboration with Innventia AB. The project was funded by the Swedish Research Council (Vetenskapsrådet) under the Programme for Strategic Energy Research under grant agreement № 621-2010-3788. vi List of abbreviations AA Auxiliary activity AFM Atomic force microscopy BG β-glucosidase CARS Coherent anti-Stokes Raman scattering CAZy Carbohydrate-active enzymes CBD Cellulose-binding domain CBH Cellobiohydrolase CBM Carbohydrate-binding module CD Catalytic domain DNS Dinitrosalicylic acid DCr Degree of crystallinity EG Endoglucanase GH Glycosyl hydrolase HPAEC-PAD High-performance anion-exchange chromatography coupled with pulsed amperometric detection LC Liquid chromatography LFD Lateral fibril dimensions LFAD Lateral fibril aggregate dimensions LPMO Lytic polysaccharide monooxygenase MPEF Multiphoton excited fluorescence MS Mass spectrometry QCM-D Quartz crystal microbalance with dissipation SHG Second harmonic generation SSA Specific surface area vii Contents 1 Introduction .................................................................................................................... 1 2 History of cellulose research .......................................................................................... 7 3 Sources of cellulose and its isolation ............................................................................. 9 3.1 Sources of cellulose in nature .................................................................................. 9 3.2 Pulping processes .................................................................................................. 12 4 Cellulolytic enzymes .................................................................................................... 15 4.1 Molecular structure and mechanisms of cellulolytic enzymes .............................. 15 4.2 Molecular structure and mechanism of lytic polysaccharide monooxygenases .... 18 4.3 Classification of cellulolytic enzymes ................................................................... 19 4.4 Enzymatic hydrolysis of cellulose ......................................................................... 19 5 Cellulase production and analysis ................................................................................ 23 5.1 Cellulase producers in nature ................................................................................ 24 5.2 Trichoderma reesei ................................................................................................ 26 5.3 Influence of the insoluble carbon source on the production of cellulases in T. reesei ............................................................................................................................ 28 5.4 Secretome of T. reesei and its analysis .................................................................. 29 5.5 Microorganism morphology .................................................................................. 31 6 Cellulose composition and structure ............................................................................ 33 6.1 Native cellulose ....................................................................................................
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