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Characterisation of the Microbial Communities in the Gastrointestinal Tract of Wood-Eating Organisms

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Characterisation of the Microbial Communities in the Gastrointestinal Tract of Wood-Eating Organisms Characterisation of the Microbial Communities in the Gastrointestinal Tract of Wood-Eating Organisms by Caroline Marden The thesis is submitted in partial fulfilment of the requirements for the award of the degree of DOCTOR OF PHILOSOPHY of the University of Portsmouth March 2019 Abstract Wood recycling is key to biogeochemical cycling and largely driven by microorganisms, with bacteria and fungi naturally coexisting together in the environment. Terrestrial isopods Oniscus asellus and Porcellio scaber have adaptations to enable them to colonise diverse terrestrial environments and scavenge on dead and decaying organic matter that is rich in cellulose. The Amazonian catfish, Panaque nigrolineatus have physiological adaptions enabling the scraping and consumption of wood, facilitating a detritivorous dietary strategy. Substrates high in lignocellulose are difficult to degrade and as yet, it is unclear whether these organisms obtain any direct nutritional benefits from ingestion and degradation of lignocellulose. However, there are numerous systems that rely on microbial symbioses to provide energy and other nutritional benefits for host organisms via lignocellulose decomposition. Whilst previous studies on the microbial communities of O. asellus, P. scaber and P. nigrolineatus, have focused upon the bacterial populations, the presence and role of fungi in lignocellulose degradation has not yet been examined. These studies describe the bacterial and fungal communities within the gastrointestinal tracts using next generation sequencing. The hepatopancreas of O. asellus and P. scaber was predominantly colonised by one bacterial species and had more fungal diversity. The hindgut was colonised by more diverse bacterial and fungal communities. Due to the woodlouse inhabiting diverse environments, including those with heavy metal pollution, culture methods were used to detect antimicrobial resistance in the gastrointestinal tract of woodlice. The effects of diet on enteric fungal populations were examined in each gastrointestinal tract region of P. nigrolineatus and fungal species were found to vary in different regions of the gastrointestinal tract as a function of diet. This is the first study to investigate the bacterial and fungal communities within the hepatopancreas and hindgut from two species of woodlice, using the same individual woodlouse, using next generation sequencing. This is the first study to detect fungi in the digestive tract of any woodlice. This study is the first to examine the fungal community in a xylivorous fish and results support the hypothesis that diet influences fungal distribution and diversity within the gastrointestinal tract of P. nigrolineatus. This study provides new insights into the microbial communities that may have a symbiotic role involved in wood degradation in the GI tracts of wood- eating organisms. This study also highlights the need for further research into fungi inhabiting many diverse environments to give more complete and balanced information about the absence and presence of microorganisms. Declaration Whilst registered as a candidate for the above degree, I have not been registered for any other research award. The results and conclusions embodied in this thesis are the work of the named candidate and have not been submitted for any other academic award. Word Count: 36,904 Contents 1 General Introduction ................................................................................................................. 1 1.1 Biogeochemical Cycle and Lignocellulose ........................................................................ 1 1.1.1 Composition of Lignocellulose ..................................................................................... 1 1.2 Microbial Degradation of Lignocellulose .......................................................................... 7 1.2.1 Saproxylic Bacteria ....................................................................................................... 7 1.2.2 Wood Degradation by Fungi ...................................................................................... 10 1.3 Symbiosis Systems .......................................................................................................... 13 1.3.1 Bacterial and Fungal Interactions in Wood Degradation ........................................... 13 1.3.2 Animals with a Diet Rich in Cellulose ......................................................................... 14 1.3.3 Wood-Eating Catfish P. nigrolineatus ........................................................................ 17 1.3.4 The Common Woodlouse ........................................................................................... 19 1.4 Heavy Metal and Antimicrobial Resistance in the Woodlouse Gut ................................ 28 1.5 Characterising the Gut Microbiota ................................................................................. 30 1.5.1 The 16S rRNA Gene .................................................................................................... 31 1.5.2 ITS rDNA Region ......................................................................................................... 32 1.6 NGS and Microbial Ecology ............................................................................................ 33 1.7 Aims and Objectives of this Work .................................................................................. 35 2 Material and Methods ............................................................................................................. 36 2.1 Media and reagents ........................................................................................................ 36 2.2 Animal Specimen Acquisition ......................................................................................... 38 2.2.1 P. nigrolineatus Collection and Husbandry ................................................................ 38 2.2.2 O. asellus and P. scaber Collection and Husbandry ................................................... 39 2.3 Preparation for Microbial Community Analysis ............................................................. 43 2.3.1 DNA Extraction ........................................................................................................... 43 2.3.2 DNA Quantification .................................................................................................... 43 2.3.3 Polymerase Chain Reaction (PCR) .............................................................................. 44 2.3.4 Gel Electrophoresis .................................................................................................... 45 2.3.5 Confirmation of Fungi in the GI tract ......................................................................... 45 2.3.6 Sanger Sequencing ..................................................................................................... 46 2.3.7 Next Generation Sequencing ..................................................................................... 46 2.4 Bioinformatic Analysis .................................................................................................... 46 2.4.1 Data Pre-Processing ................................................................................................... 46 2.4.2 OTU Diversity Analysis ............................................................................................... 48 3 Characterisation of the Fungal Communities in the GI Tract of P. nigrolineatus ..................... 50 3.1 Introduction .................................................................................................................... 50 3.2 Aims ................................................................................................................................ 50 3.3 Preparation for Next Generation Sequencing ................................................................ 51 3.3.1 DNA Quantification .................................................................................................... 51 3.3.2 Confirmation of Fungi in Samples .............................................................................. 51 3.4 Distribution and Diversity of Fungi in the GI Tract of P. nigrolineatus ........................... 51 3.4.1 Analysis of ITS rDNA Sequences Detected in P. nigrolineatus ................................... 51 3.4.2 Alpha Diversity Analysis ............................................................................................. 52 3.4.3 Fungal Community Diversity in the GI Tract of P. nigrolineatus ................................ 54 3.5 Relative Distribution and Diversity of Fungi Based on Dietary Regimen ........................ 57 3.6 Relative Distribution and Diversity of Fungi Based on Enteric Region ........................... 60 3.7 Distribution and Diversity of Fungi in the GI Tract from ITS1 rDNA Analysis ................. 61 3.7.1 Alpha Diversity of Fungi in GI tract of P. nigrolineatus .............................................. 61 3.7.2 Fungal (ITS1 rDNA) Community Diversity in the GI Tract of P. nigrolineatus ............. 63 3.8 Discussion ....................................................................................................................... 65 4 Characterisation of the Bacterial and Fungal Communities in the Hepatopancreas from O. asellus and P. scaber ........................................................................................................................ 68 4.1 Introduction ...................................................................................................................
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