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The Pennsylvania State University The Pennsylvania State University The Graduate School Intercollege Graduate Degree Programs MULTITROPHIC INTERACTIONS CONTRIBUTE TO WOOD DIGESTION AND NUTRITIONAL ECOLOGY IN LARVAL ANOPLOPHORA GLABRIPENNIS (ASIAN LONGHORNED BEETLE) A Dissertation in Genetics by Erin D. Scully 2013 Erin D. Scully Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy December 2013 The dissertation of Erin D. Scully was reviewed and approved* by the following: Dr. Kelli Hoover Professor of Entomology Dissertation Co-Advisor Dr. John Carlson Professor of Ecosystem and Management Dissertation Co-Advisor Dr. Dawn Luthe Professor of Plant Stress Biology Dissertation Chair Dr. Scott Geib Research Entomologist, USDA-ARS-PBARC Special Committee Member Dr. David Geiser Professor of Plant Pathology Dr. Robert Paulson Professor of Veterinary and Biomedical Sciences Head of the Genetics Program *Signatures are on file in the Graduate School iii ABSTRACT The Asian longhorned beetle (Anoplophora glabripennis) is an exotic, wood-boring pest that was first detected in the northeastern United States in 1996. A. glabripennis has a broad host range and can feed and grow in the heartwood of about 25 different deciduous tree species in the US. A. glabripennis’ ability to thrive in a broad range of healthy host trees is particularly impressive considering that most other wood-boring insects with broad host ranges feed on stressed or dying trees whose woody, intractable components have been pre-digested by wood- degrading bacteria and fungi. In contrast, A. glabripennis harbors a diverse gut microbial community hypothesized to provide key enzymes for lignocellulose digestion and nutrient acquisition that help this insect overcome challenges of survival in healthy host trees. To investigate the contribution of gut microbes to digestive physiology, we surveyed the inherent digestive capabilities of A. glabripennis through midgut transcriptome sequencing, inventoried the taxonomic identity and metabolic potential of gut microbial affiliates through metagenome and metatranscriptome profiling, and analyzed the wood-degrading potential of a filamentous fungal taxon (e.g. Fusarium solani) consistently found in association with the A. glabripennis midgut using multidimensional protein identification techniques. While A. glabripennis endogenously produces a diverse array of cellulases belonging to three glycoside hydrolase families, xylanases, detoxification enzymes, and proteins involved in nitrogen and nutrient scavenging, its suite of digestive and nutrient scavenging abilities is greatly expanded through its affiliation with gut microbes. Metagenome and metatranscriptome profiling revealed that the gut community has the capacity to produce cellulases, xylanases, and enzymes involved in nitrogen- fixation and recycling, vitamin and sterol synthesis, and lignin degradation. Moreover, secretome analysis of the beetle gut isolate of F. solani was cultivated on wood chips, revealing the production of several laccases, peroxidases, and accessory enzymes previously implicated in iv lignin depolymerization, suggesting that this isolate could have lignin-degrading capabilities in the beetle gut. Both insect- and microbial- derived digestive enzymes represent novel targets that could be targeted for control of this invasive beetle. Overall, this research lays the foundation for unraveling the complex interactions between cerambycids and their gut microbes that contribute to survival in an environment devoid of easily accessible nutrients, allowing us to mine for novel biochemical pathways that could be exploited to enhance industrial cellulosic ethanol production and to develop novel targets for pest management. v TABLE OF CONTENTS List of Figures .......................................................................................................................... ix List of Tables ........................................................................................................................... xii Acknowledgements .................................................................................................................. xiv Chapter 1 Introduction ............................................................................................................. 1 Background ...................................................................................................................... 3 Nutritional Composition of Woody Tissue .............................................................. 3 Symbiosis in Xylophagous Insects ........................................................................... 4 Endogenous Enzymes of Xylophagous Insects and their Roles in Nutrient Acquisition ....................................................................................................... 5 Host Plant Resistance: Impacts on Insects and their Symbionts ............................. 7 Life History of (ALB) Anoplophora glabripennis ................................................... 9 Microbes Associated with the Midgut of Anoplophora glabripennis ...................... 10 Experiments ..................................................................................................................... 12 Chapter 2. Comparative Metagenomic Profiling Reveals Lignocellulose Degrading System in Microbial Community Associated with a Wood- Feeding Beetle .................................................................................................. 13 Chapter 3. Proteomic Analysis of Fusarium solani Isolated from the Asian Longhorned Beetle, Anoplophora glabripennis. .............................................. 14 Chapter 4. Midgut Transcriptome Profiling of Anoplophora glabripennis, a Lignocellulose-Degrading, Wood-Boring Cerambycid ................................... 15 Chapter 5. Metatranscriptome Analysis and Community Profiling of Microbes Associated with the Asian Longhorned Beetle (Anoplophora glabripennis) Midgut: Insights into Insect-Microbe Interactions and Nutritional Ecology ... 16 Supplemental Chapter: Phylogenetic Analysis of Fusarium solani Associated with the Asian Longhorned Beetle, Anoplophora glabripennis ....................... 17 Literature Cited ................................................................................................................ 17 Chapter 2 Comparative Metagenomic Profiling Reveals Lignocellulose Degrading System in Microbial Community Associated with a Wood-Feeding Beetle .................... 29 Abstract ............................................................................................................................ 29 Introduction ...................................................................................................................... 30 Methods ............................................................................................................................ 34 Preparation of Insect Cell Free DNA for Community Profiling and Shotgun Sequencing ....................................................................................................... 34 454 Amplicon Pyrosequencing to Taxonomically Identify Microbes Associated with the A. glabripennis Midgut ....................................................................... 35 Phylogenetic Binning and Functional Analysis of A. glabripennis Midgut Microbiota Using Shotgun 454 Pyrosequencing .............................................. 37 Comparisons to Other Herbivore-Related Metagenomes: ....................................... 39 Results and Discussion ..................................................................................................... 41 vi Taxonomic Classification of OTUs and Shotgun Reads .......................................... 41 Identification of Cellulose-, Hemicellulose- and Aromatic Compound- Degrading Bacterial Taxa ................................................................................. 42 Identification of Fungal Community ........................................................................ 43 Functional Profiling of Reads Generated through 454 Shotgun Sequencing ........... 45 Comparison of Functional Domains from Other Herbivore Associated Microbial Communities .................................................................................... 45 Candidate Genes for Lignin Degrading Enzymes .................................................... 48 Candidate Genes for Cellulases and Carbohydrases ................................................ 51 Candidate Genes for Xylose Utilization and Fermentation ...................................... 52 Candidate Genes for Pectin Degrading Enzymes ..................................................... 54 Candidate Genes for Nutrient Acquisition and Synthesis ........................................ 54 Candidate Genes from Fusarium ............................................................................. 59 Candidate Genes from Leuconostoc ......................................................................... 60 Conclusion ....................................................................................................................... 61 Acknowledgements .......................................................................................................... 62 Literature Cited ................................................................................................................ 64 Chapter 3 Proteomic Analysis of Fusarium solani isolated from the Asian longhorned beetle, Anoplophora glabripennis
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