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Taxonomic and Functional Characterization of Biopolymer-Degrading Microbial Communities in the Intestinal Tract of Beavers

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Taxonomic and Functional Characterization of Biopolymer-Degrading Microbial Communities in the Intestinal Tract of Beavers TAXONOMIC AND FUNCTIONAL CHARACTERIZATION OF BIOPOLYMER-DEGRADING MICROBIAL COMMUNITIES IN THE INTESTINAL TRACT OF BEAVERS Dissertation For the award of the degree “Doctor rerum naturalium (Dr. rer. nat.)” of the Georg-August-Universität Göttingen within the doctoral program in Biology of the Georg-August University School of Science (GAUSS) submitted by Rahadian Pratama from Bogor, Indonesia Göttingen, 2019 Thesis committee Prof. Dr. Rolf Daniel, Department of Genomics and Applied Microbiology, Institute of Microbiology and Genetics, Georg-August-Universität Göttingen PD Dr. Michael Hoppert, Department of General Microbiology, Institute of Microbiology and Genetics, Georg-August-Universität Göttingen Examination board Reviewer: Prof. Dr. Rolf Daniel, Department of Genomics and Applied Microbiology, Institute of Microbiology and Genetics, Georg-August- Universität Göttingen Second reviewer: PD Dr. Michael Hoppert, Department of General Microbiology, Institute of Microbiology and Genetics, Georg-August-Universität Göttingen Further member of the examination board Prof. Dr. Stefanie Pöggeler, Department of Genetics of Eukaryotic Microorganisms, Institute of Microbiology and Genetics, Georg-August-Universität Göttingen Prof. Dr. Gerhard Braus, Department of Molecular Microbiology and Genetics, Institute of Microbiology and Genetics, Georg-August-Universität Göttingen Prof. Dr. Fabian Commichau, Department of General Microbiology, Institute of Microbiology and Genetics, Georg-August-Universität Göttingen PD Dr. Christian Roos, Primate Genetics Laboratory, German Primate Center Date of the oral examination: 2nd May 2019 2 Praise to Allah SWT and his messenger Muhammad SAW. To my mother who always believe in me, and my family for their support 3 Table of Contents 1. INTRODUCTION ............................................................................................................................................. 5 1.1. LIGNOCELLULOSE ................................................................................................................................. 7 1.2. LIGNOCELLULOSE BIODEGRADATION .................................................................................................. 8 1.2.1. Enzymes facilitate lignocellulosic biomass degradation ............................................................. 9 1.2.2. CAZy database encompassing various known and novel CAZymes ......................................... 10 1.3. HERBIVOROUS GUT AS SOURCE OF CELLULOLYTIC MICROORGANISMS AND ENZYMES ................... 12 1.3.1. Eurasian beaver gut microbiome as a source of potentially new lignocellulases .................... 13 1.4. AIM OF THE STUDY .............................................................................................................................. 15 2. MATERIALS AND METHODS .................................................................................................................... 16 2.1. MATERIALS ......................................................................................................................................... 16 2.1.1. Beavers gastrointestinal tract ..................................................................................................... 16 2.1.2. Primers ........................................................................................................................................ 16 2.2. METHODS ............................................................................................................................................ 17 2.2.1. Pretreatment of samples for direct metagenomic sequencing .................................................. 17 2.2.2. DNA extraction and nucleic acid purification .......................................................................... 17 2.2.3. Amplification and sequencing of bacterial 16S rRNA genes .................................................... 18 2.2.4. Direct sequencing of beaver gut metagenomes ......................................................................... 18 2.2.5. 16S rRNA bacterial community structure and diversity analysis ............................................. 19 2.2.6. Comparison of herbivorous gut bacterial communities ............................................................ 19 2.2.7. Metagenome reads quality filtering and assembly .................................................................... 21 2.2.8. Metagenome-derived microbial diversity of castor fiber gut ..................................................... 21 2.2.9. Metagenome annotation and functional analysis ..................................................................... 21 2.2.10. Cloning of a novel cellulase gene derived from the gut metagenome and its expression in E.coli ..................................................................................................................................................... 22 2.2.11. Preparation and purification of cellulase BC33........................................................................ 23 2.2.12. BC33 activity assays ................................................................................................................... 23 2.2.13. BC33 phylogenetic analysis and structure prediction ............................................................... 24 3. RESULTS AND DISCUSSION ...................................................................................................................... 25 3.1. DIVERSITY AND COMPOSITION OF THE EURASIAN BEAVER GUT BACTERIAL COMMUNITY .............. 25 3.1.1. Diversity of intestinal bacterial communities ............................................................................ 25 3.1.2. The Eurasian beaver gut bacterial community is dominated by Firmicutes and Actinobacteria ..................................................................................................................................................... 27 3.1.3. Potential functional capabilities of the beaver gut microbiome ............................................... 31 3.1.4. Eurasian beaver gut microbiome in comparison with North American beavers, herbivorous animals, and humans ................................................................................................................................... 32 3.2. METAGENOMIC ANALYSIS OF THE EURASIAN BEAVER GUT BACTERIAL COMMUNITY REVEALS NOVEL CELLULASE ........................................................................................................................................... 36 3.2.1. Bacterial community structure derived from metagenome sequences ..................................... 36 3.2.2. Metabolic potential derived from the metagenome of subadult beavers ................................... 38 3.2.3. The gut microbiome of the beaver as reservoir for genes encoding of carbohydrate-active enzymes (CAZymes) ..................................................................................................................................... 41 3.3. ANALYSIS OF BEAVER CELLULASE CANDIDATE 33 (BC33) – A NEW GH5 FAMILY CELLULASE ....... 48 3.3.1. The phylogenetic tree and structure of BC33 ............................................................................ 50 3.3.2. Enzymatic assay of overexpressed BC33 protein ...................................................................... 52 3.3.3. Substrate specificity and kinetics of recombinant BC33 ........................................................... 53 4. GENERAL DISCUSSION .............................................................................................................................. 55 4.1. METAGENOME-GUIDED DISCOVERY OF NEW CELLULASE FROM EURASIAN BEAVER GUT MICROBIOME .................................................................................................................................................... 56 5. SUMMARY ...................................................................................................................................................... 62 6. REFERENCES ................................................................................................................................................ 64 7. APPENDICES ................................................................................................................................................. 82 4 1. INTRODUCTION 1.1.World energy consumption trend and the use of bioethanol The economic status of the country and the welfare of its citizen are strongly influenced by energy resources and their utilization. Barnes and Floor (1996) mentioned that the energy demand of a country is determined by its economic development and vice versa. The Statistical Review of World Energy showed that most of Europe’s energy consumption comes from fossil fuel (oil, natural gas, and coal) (Figure 1. 1). The oil consumption was 49% in 2005 and 48% in 2017, followed by natural gas and coal, with hardly any change (BP, 2018). 900 800 700 600 500 Oil 400 Gas 300 Coal 200 Biofuel 100 Energy Energy consumption 0 Million Million tonnesoil equivalent 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 Year Figure 1. 1 Energy consumption in Europe by fuel type per year basis. Source: BP (2018) Fossil fuels are mainly used for transportation (Wi et al., 2015). The fuel combustion from vehicles releases carbon dioxide (CO2) as well as toxic particles, causing serious health problems, especially for children, which are most vulnerable (Perera, 2017). CO2 and other
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