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Isolation and Characterization of Cellulase-Producing Microorganisms in The Isolation and Characterization of Cellulase-Producing Microorganisms in the Red Sea Dissertation by Siham Kamal Fatani In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy King Abdullah University of Science and Technology, Thuwal, Kingdom of Saudi Arabia September, 2019 2 Examination Committee Page The Dissertation of Siham Fatani is Examined by the Committee Members Committee Chairperson: Prof. Takashi Gojobori Committee Members: Prof. Vladimir Bajic, Prof. Susana Agusti, Prof. Shugo Watabe 3 © September, 2019 Siham Kamal Fatani All Rights Reserved 4 ACKNOWLEDGMENTS This work is a consequence of great help and guidance from many people; faculty, family and friends. I am really happy to have these people by my side while undertaking my PhD Dissertation. First, I would like to express my profound gratitude and respect to my supervisor, Prof. Takashi Gojobori, Distinguished Professor of Bioscience and Associate Director of Computational Bioscience Research Center for his professional guidance, and regular encouragement and motivation at various stages of this work. I would also like to thank Dr. Katsuhiko Mineta for his support and advice during my research. Moreover, I would like to express my deepest appreciation to Dr. Yoshimoto Saito for his assistance and suggestions throughout my project. I also appreciate Mr. Mohammad Al-Arawi for his support and technical advice and without them this work would not have been possible for me to complete. In addition, I would like to thank my committee members, Prof. Vladimir Bajic, Prof. Susana Agusti and Prof. Shugo Watabe for giving their time to review my Ph.D. thesis and for offering their insight and suggestions. Finally, I would like to thank my family who always encourage me to continue for higher education and push me to do my best during my Ph.D. and my KAUSTian friends who made the five-years journey in KAUST really enjoyable and the CGG lab member who always support me. 5 ABSTRACT Isolation and Characterization of Cellulase-Producing Microorganisms in the Red Sea Siham Kamal Fatani Cellulase-producing microorganisms are considered as a key player in various environments to degrade the plant biomass and were isolated from various environment like soils, mangroves and oceans. The Red Sea has a unique environment in terms of high seawater temperature, high salinity and low nutrients. This study aims of examining if the Red Sea is a potential resource for cellulase-producing microorganisms and cellulase genes. First, I investigated types of microbial cellulase genes in the Red Sea based on public metagenomic datasets. The analysis revealed 3,383 microbial cellulase were more abundant in shallow depth than in deep seawater, and were classified into 16 sub-GH orthologous groups. These results suggest that the Red Sea environment is potentially an excellent gene resource of microbial cellulases due to its high diversity. Next, cellulase-producing microorganisms were isolated and screened from the Red Sea. Three bacterial and one fungal strain were successfully obtained. The MLTS analysis showed that the three bacterial strains belong to Bacillus paralichiniformis. The 18S rRNA of fungal strain showed 99% similarity to Aspergillus ustus and the enzymatic assay of the four strains showed high cellulase activity. These results suggest that these four isolates secreted active cellulases. Next, I tried to identify cellulase genes actually working during their cellulolysis by conducting comparative transcriptome analysis of the candidate genes and identified cellulase genes that are highly expressed during cellulolysis. To my knowledge, it is the first attempt to find out cellulase genes functioning during their cellulolysis among distinct cellulases on genomes of microorganisms. The results showed that 6 although all the candidate genes were upregulated in general, a limited number of cellulase genes were highly expressed, which are highly expected to have a crucial role in cellulolysis. I also identified operon structures composed of genes including cellulases. This will provide us with the information to elucidate the cellular mechanisms occurring along with the cellulolysis in bacterial strains. We can expect that the Red Sea is a potential resource for new cellulase genes applicable for the industry. These information can be significantly useful for the bio-prospecting research of microbial cellulases in the Red Sea. 7 Table of Contents Examination Committee Page ................................................................................................ 2 ACKNOWLEDGMENTS ............................................................................................................ 4 ABSTRACT ............................................................................................................................. 5 LIST OF ABBREVIATIONS ........................................................................................................ 9 LIST OF FIGURES .................................................................................................................. 11 LIST OF TABLES .................................................................................................................... 12 Chapter 1. General Introduction ........................................................................................... 13 1.1. Cellulose and Cellulases ................................................................................................................... 13 1.2. Cellulase-Producing Microorganisms .............................................................................................. 14 1.3. Carbohydrate-Active Enzymes Database (CAZy) ............................................................................. 15 1.4. The Red Sea Metagenome ............................................................................................................... 16 1.5. The Aim of This Study ...................................................................................................................... 17 Chapter 2. A Survey of the Red Sea Metagenome for Cellulase-Producing Microorganisms ... 18 2.1. Introduction ..................................................................................................................................... 18 2.2. Material and Methods ..................................................................................................................... 21 2.2.1. Collection and Analysis of the Red Sea Metagenomes ................................................................ 21 2.2.2. Hierarchical Clustering Analysis .................................................................................................... 23 2.3. Results and Discussion ..................................................................................................................... 23 2.3.1 Relative Abundance and Composition of Cellulase Orthologues in the Red Sea .......................... 23 2.3.2 Hierarchical Clustering Analysis of Cellulase Orthologous Composition in Red Sea Metagenomes ................................................................................................................................................................ 30 2.4. Conclusion ....................................................................................................................................... 31 Chapter 3. Isolation, Screening, and Characterization of Cellulase-Producing Microorganisms from the Red Sea ................................................................................................................. 32 3.1. Introduction ..................................................................................................................................... 32 3.2. Material and Methods ..................................................................................................................... 33 3.2.1 Collection of Samples from the Red Sea ....................................................................................... 33 3.2.2 Isolation and Screening of Cellulase-Producing Microorganisms ................................................. 34 3.2.3 Taxonomy Identification ................................................................................................................ 35 3.2.4 DNA Preparation for Whole Genome Sequencing of Bacterial Isolates ........................................ 36 8 3.2.5 De novo Assembly of the Genome Sequencing Data .................................................................... 37 3.2.6 Genome Annotation ...................................................................................................................... 37 3.2.7 Multilocus Sequence Typing (MLST) Analysis of Bacterial Isolates ............................................... 38 3.2.8 Preparation of Extracellular Cellulase Enzymes ............................................................................ 40 3.2.9 Measuring the Cellulase Activity ................................................................................................... 41 3.3. Results and Discussion ..................................................................................................................... 42 3.3.1 Isolation of Cellulase-Producing Microorganisms from the Red Sea Samples .............................. 42 3.3.2. Taxonomic Identification of Cellulase-Active Strains ................................................................... 45 3.3.3 Whole Genome Sequencing and
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