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Physiology and enzymology of lignocellulose digestion in the shipworm Lyrodus pedicellatus Giovanna Pesante PhD University of York Biology September 2018 1 Abstract Shipworms are marine bivalve molluscs, known for their wood boring abilities. They use modified shells to bore into and grind wood, which is then digested. The shipworm’s ability to feed on lignocellulose is dependent on the presence of endosymbiotic bacteria that live in the animal’s gills inside specialized eukaryotic cells called bacteriocytes. These bacteria provide the animal with hydrolytic enzymes for wood digestion, which are translocated from the gills to the caecum, the main site of wood digestion. Unlike other lignocellulose degrading organisms, which harbour symbiotic microbes in their digestive tract, the shipworm caecum hosts only few bacteria but contains a large amount of carbohydrate active enzymes (CAZymes) of both endogenous and bacterial origin. This study investigates the anatomical, physiological and molecular basis of wood digestion in the shipworm Lyrodus pedicellatus. A combination of meta-transcriptomics, meta- proteomics and microscopic studies of the shipworm digestive organs was used, coupled with recombinant production and characterisation of some of the most expressed lignocellulolytic enzymes. This multidisciplinary analysis revealed how two structures, the food groove (a mucus stream utilised by filter feeding molluscs to transport food particles from the gills to the digestive system) and the crystalline style (a rotating structure hosted in the stomach involved in extra-cellular digestion) have been co-opted in shipworms to translocate bacteria and their enzymes from the gills to the caecum, to facilitate wood digestion. The transcriptomic and proteomic results indicate that bacterial lignocellulolytic enzymes are expressed in the gills, while the endogenous enzymes are mainly produced by the digestive glands, with complementary CAZy classes being expressed by the bacteria and the shipworms, indicating a subdivision of roles. Five bacterial CAZymes were recombinantly expressed and characterised, showing activity on cellulose, galacto-glucomannan and xylan. This study provides new insights into the mechanisms of wood digestion in shipworms, which may have biotechnological relevance. 2 List of contents Abstract 2 List of contents 3 List of tables 9 List of figures 10 Acknowledgments 14 Declaration 17 Chapter 1: General introduction 18 1.1 Biofuels and the plant cell wall 18 1.1.1 The need for biofuels 18 1.1.2 First- and second-generation biofuels 19 1.1.3 Lignocellulosic biomass 20 1.1.4 Cell wall composition 21 1.1.4.1 Cellulose 21 1.1.4.2 Hemicellulose 22 1.1.4.3 Pectins 23 1.1.4.4 Lignin 24 1.1.4.5 Structural proteins 25 1.1.5 Lignocellulolytic enzymes 25 1.2 Degradation of lignocellulose in nature 26 1.2.1 Prokaryotes and Archaea 27 1.2.2 Fungi 28 1.2.3 Protista 29 1.2.4 Terrestrial invertebrates 30 1.2.5 Marine invertebrates 32 1.2.6 Vertebrates 33 1.3 The wood boring bivalves 34 1.3.1 Distribution, ecological role and economic impact of the Teredinidae 34 1.3.2 Xylotrophy versus filter feeding 36 1.3.3 The symbiosis between shipworms and bacteria 39 1.3.4 The transport of the bacterial enzymes 42 1.3.5 The shipworm Lyrodus pedicellatus 43 3 1.3.5.1 Classification and distribution 43 1.3.5.2 General overview and ecology 49 1.3.5.3 Reproduction 47 1.3.5.4 Digestive system anatomy 48 1.4 Aims of the project 55 Chapter 2: Materials and methods 57 2.1 Animal cultures 57 2.1.1 Specimens acquisition and culturing 57 2.1.2 Wood preparation and compositional analysis 58 2.1.2.1 Hemicellulose content 58 2.1.2.2 Crystalline cellulose content 59 2.1.2.3 Lignin content 59 2.1.2.4 Silica content 60 2.1.2.5 Ash content 60 2.1.2.6 High-Performance Anion-Exchange Chromatography (HPAEC) 60 2.1.3 Specimen extraction and dissection 61 2.1.4 Morphological and molecular species identification 61 2.2 Microscopy 62 2.2.1 In vivo staining with x-cellobiose 62 2.2.2 Light microscopy 62 2.2.3 Transmission electron microscopy 62 2.2.4 Immunogold labelling 63 2.2.4.1 Fixing, embedding and sectioning 63 2.2.4.2 Antibodies production and purification 64 2.2.5 Scanning electron microscopy 65 2.3 Transcriptomic analysis 66 2.3.1 RNA extraction, clean up, depletion and quantification 66 2.3.2 cDNA library preparation and RNA sequencing 66 2.3.3 Contig assembly and transcriptome analysis 67 2.4 Proteomic analysis 68 2.4.1 Organs dissection and preparation 68 2.4.2 Liquid Chromatography-tandem Mass Spectrometry (LC-MS/MS) analysis 68 2.4.3 Proteomic analysis 69 4 2.4.4 Protein identification by MALDI/TOF-TOF tandem mass spectrometry 69 2.5 Molecular biology techniques 70 2.5.1 cDNA production 70 2.5.2 Polymerase chain reaction (PCR) 70 2.5.3 3’ and 5’ Rapid Amplification of cDNA Ends (RACE) 72 2.5.4 DNA purification 72 2.5.5 Nucleic acids quantification 72 2.5.6 Nucleic acid agarose gel electrophoresis 73 2.5.7 StrataClone subcloning 73 2.5.8 Colony screening 74 2.5.9 Plasmid DNA extraction 75 2.5.10 DNA sequencing (Sanger sequencing) 75 2.5.11 In-Fusion HD cloning 76 2.6 Recombinant protein expression 76 2.6.1 Transformation of chemically competent cells 76 2.6.2 Expression systems 77 2.6.2.1 E. coli cytoplasmic expression system 77 2.6.2.2 E. coli periplasmic expression system 78 2.6.2.3 Baculovirus mediated insect cell expression system 79 2.6.3 Bacterial cells expression 80 2.6.4 Insect cells expression 81 2.6.5 Sodium Dodecyl Sulphate Polyacrylamide Gel Electrophoresis (SDS-PAGE) 82 2.6.6 Schiff’s fuchsin-sulfite glycoprotein stain 83 2.6.7 Western blot analysis 83 2.6.8 Protein quantification (Bradford assay) 84 2.6.9 Protein concentration 84 2.6.10 Media 84 2.6.10.1 Lysogeny Broth 85 2.6.10.2 Super Optimal Broth with Catabolite repression 85 2.6.10.3 Auto-induction medium 85 2.6.10.4 M9 minimal medium 85 2.7 Protein purification 86 2.7.1 Affinity chromatography 86 5 2.7.2 Gel filtration 87 2.7.3 Thermal shift assay 87 2.8 Enzyme activity assays 88 2.8.1 DNS (3,5-dinitrosalicylic acid) reducing sugars assay 88 2.8.2 Heat maps 89 2.8.3 Polysaccharide analysis using carbohydrate gel electrophoresis (PACE) 90 2.8.4 Product identification by MALDI/TOF-TOF tandem mass spectrometry 90 2.8.5 Substrates 91 Chapter 3: Anatomy and physiology of the digestive organs of Lyrodus pedicellatus 92 3.1 Introduction 92 3.2 Aims of the chapter 93 3.3 Gills and food groove 94 3.3.1 Investigation of gills and food groove 94 3.3.1.1 Microscopy and in vivo assays of the gills and food groove 94 3.3.1.2 Immunogold labelling of the gills and food groove 99 3.3.1.3 In vitro activity assay of the gills 101 3.4 Caecum 103 3.4.1 The wood-degrading properties of the caecum 103 3.4.2 Investigation of the lignocellulolytic activities of the caecum 105 3.4.2.1 Transmission electron microscopy of the caecum 105 3.4.2.2 Compositional analysis of wood versus frass 108 3.4.2.3 In vitro activity assay of the caecum fluids 111 3.4.2.4 Caecum protein identification 113 3.5 Digestive glands 117 3.5.1 Investigation of the digestive glands 117 3.5.1.1 Microscopy of the digestive glands 117 3.5.1.2 In vitro activity assay of the digestive glands 122 3.6 Crystalline style 123 3.6.1 Investigation of crystalline style and its sac 123 3.6.1.1 Light and electron microscopy of the crystalline style and its sac 123 3.6.1.2 Proteins of the crystalline style 128 3.6.1.3 Enzymatic activities of the crystalline style 131 3.7 Discussion 134 6 Chapter 4: Transcriptomic and proteomic analysis of the digestive organs of Lyrodus pedicellatus 140 4.1 Introduction 140 4.2 Aims of the chapter 141 4.3 Transcriptomic analysis of digestive glands, caecum, gills and crystalline style sac 142 4.3.1 Sequencing of RNA from the digestive glands, caecum and gills 142 4.3.2 Sequencing of RNA from crystalline style sac 143 4.3.3 Analysis of the transcriptome of digestive glands, caecum, gills and crystalline style sac 144 4.4 The role of the caecum in sugar transport 153 4.5 Analysis of the proteome of digestive glands, caecum, gills and crystalline style 154 4.5.1 The non-CAZy proteins of the crystalline style 165 4.6 The role of the digestive glands and caecum in immunity 169 4.7 Discussion 173 Chapter 5: Heterologous expression and characterisation of endogenous and bacterial lignocellulolytic enzymes from Lyrodus pedicellatus 180 5.1 Introduction 180 5.2 Aims of the chapter 182 5.3 Target enzymes selection and cloning 182 5.4 The bacterial LpsGH5_8 187 5.4.1 Sequence analysis and cloning 187 5.4.2 Expression 189 5.4.3 Activity assays 192 5.4.3.1 Activity against polysaccharides 192 5.4.3.2 Heat maps 195 5.4.3.3 Polysaccharide analysis using carbohydrate gel electrophoresis 196 5.5 The bacterial LpsGH134a and LpsGH134b 197 5.5.1 Sequence analysis and cloning 197 5.5.2 Expression 200 5.5.3 Activity assays 202 5.5.3.1 Activity against polysaccharides 202 5.5.3.2 Heat maps 204 7 5.5.3.3 Polysaccharide analysis using carbohydrate gel electrophoresis 205 5.6 The bacterial LpsGH11 206 5.6.1 Sequence analysis and cloning 206 5.6.2 Expression 208 5.6.3 Activity assays 211 5.6.3.1 Activity against polysaccharides 211 5.6.3.2 Polysaccharide analysis using carbohydrate gel electrophoresis 212 5.7 The bacterial LpsAA10 213 5.7.1 Sequence analysis and cloning 213 5.7.2 Expression 215 5.7.3 Activity assays 217 5.7.3.1 MALDI/TOF-TOF tandem mass spectroscopy 217 5.8 Discussion 219 Chapter 6: Final discussion 224 6.1 General discussion 224 6.2 Future work 229 Appendices 231 Appendix A 232 Appendix B 234 Appendix C 235 List of abbreviations and symbols 238 References 242 Publications arising from this work 270 8 List of tables Table 1.1.
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    Short Notes 263 The Rhizome-Boring Shipworm Zachsia zenkewitschi (Bivalvia: Teredinidae) in Drifted Eelgrass Takuma Haga Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan The shipworm Zachsia zenkewitschi Bulatoff & free-swimming larval stage. Turner & Yakovlev Rjabtschikoff, 1933 lives inside the rhizomes of the (1983) observed that the larvae swam mostly near eelgrasses Phyllospadix and Zostera (Helobiales; the bottom of a culture dish in their laboratory. Zosteraceae) and has sporadic distribution records They hypothesized that in natural environments the from Primorskii Krai (=Primoriye Region) to larvae can swim only for short distances within the Siberia in the Russian Far East and in Japanese eelgrass beds and that wide dispersal might have waters (Higo et al., 1999). Its detailed distribution been achieved through long-distance transporta- and habitats have been surveyed in detail only tion of the host eelgrass by accidental drifting. locally along the coast of Vladivostok in Primoriye However, this hypothesis has not been verified to (Turner et al., 1983; Fig. 1F). In Japanese waters, date. this species has been recorded in only three cata- This report is the first documentation of Z. logues of local molluscan faunas (Fig. 1; Inaba, zenkewitschi in drifted rhizomes of eelgrass, and 1982; Kano, 1981; Kuroda & Habe, 1981). These describes the soft animal morphology of this spe- catalogues, however, did not provide information cies. on detailed collecting sites and habitats. This rare species was recently rediscovered along the coast Zachsia zenkewitschi in drift eelgrass of Miyagi Prefecture, northeast Japan (Sasaki et al., 2006; Fig.
  • TREATISE ONLINE Number 48

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    TREATISE ONLINE Number 48 Part N, Revised, Volume 1, Chapter 31: Illustrated Glossary of the Bivalvia Joseph G. Carter, Peter J. Harries, Nikolaus Malchus, André F. Sartori, Laurie C. Anderson, Rüdiger Bieler, Arthur E. Bogan, Eugene V. Coan, John C. W. Cope, Simon M. Cragg, José R. García-March, Jørgen Hylleberg, Patricia Kelley, Karl Kleemann, Jiří Kříž, Christopher McRoberts, Paula M. Mikkelsen, John Pojeta, Jr., Peter W. Skelton, Ilya Tëmkin, Thomas Yancey, and Alexandra Zieritz 2012 Lawrence, Kansas, USA ISSN 2153-4012 (online) paleo.ku.edu/treatiseonline PART N, REVISED, VOLUME 1, CHAPTER 31: ILLUSTRATED GLOSSARY OF THE BIVALVIA JOSEPH G. CARTER,1 PETER J. HARRIES,2 NIKOLAUS MALCHUS,3 ANDRÉ F. SARTORI,4 LAURIE C. ANDERSON,5 RÜDIGER BIELER,6 ARTHUR E. BOGAN,7 EUGENE V. COAN,8 JOHN C. W. COPE,9 SIMON M. CRAgg,10 JOSÉ R. GARCÍA-MARCH,11 JØRGEN HYLLEBERG,12 PATRICIA KELLEY,13 KARL KLEEMAnn,14 JIřÍ KřÍž,15 CHRISTOPHER MCROBERTS,16 PAULA M. MIKKELSEN,17 JOHN POJETA, JR.,18 PETER W. SKELTON,19 ILYA TËMKIN,20 THOMAS YAncEY,21 and ALEXANDRA ZIERITZ22 [1University of North Carolina, Chapel Hill, USA, [email protected]; 2University of South Florida, Tampa, USA, [email protected], [email protected]; 3Institut Català de Paleontologia (ICP), Catalunya, Spain, [email protected], [email protected]; 4Field Museum of Natural History, Chicago, USA, [email protected]; 5South Dakota School of Mines and Technology, Rapid City, [email protected]; 6Field Museum of Natural History, Chicago, USA, [email protected]; 7North