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The Ecology and Glycobiology of Prymnesium Parvum

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The Ecology and Glycobiology of Prymnesium Parvum The Ecology and Glycobiology of Prymnesium parvum Ben Adam Wagstaff This thesis is submitted in fulfilment of the requirements of the degree of Doctor of Philosophy at the University of East Anglia Department of Biological Chemistry John Innes Centre Norwich September 2017 ©This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with the author and that use of any information derived there from must be in accordance with current UK Copyright Law. In addition, any quotation or extract must include full attribution. Page | 1 Abstract Prymnesium parvum is a toxin-producing haptophyte that causes harmful algal blooms (HABs) globally, leading to large scale fish kills that have severe ecological and economic implications. A HAB on the Norfolk Broads, U.K, in 2015 caused the deaths of thousands of fish. Using optical microscopy and 16S rRNA gene sequencing of water samples, P. parvum was shown to dominate the microbial community during the fish-kill. Using liquid chromatography-mass spectrometry (LC-MS), the ladder-frame polyether prymnesin-B1 was detected in natural water samples for the first time. Furthermore, prymnesin-B1 was detected in the gill tissue of a deceased pike (Exos lucius) taken from the site of the bloom; clearing up literature doubt on the biologically relevant toxins and their targets. Using microscopy, natural P. parvum populations from Hickling Broad were shown to be infected by a virus during the fish-kill. A new species of lytic virus that infects P. parvum was subsequently isolated, Prymnesium parvum DNA virus (PpDNAV-BW1). Morphological analysis and genome sequencing revealed PpDNAV-BW1 to belong to the Megaviridae family of algal viruses. We propose that viral lysis of P. parvum may act as a novel release mechanism for intracellular toxins. The sialic acid, 2-keto-3-deoxy-D-glycero-D-galacto-nononic acid (KDN) has recently been shown to be important in viral infections of microalgae. LC-MS was used to demonstrate that P. parvum contains KDN. Candidate sequences for KDN biosynthesis from P. parvum were cloned and expressed and shown to produce cytidine monophosphate-activated KDN (CMP- KDN). Using the newly characterized sequences in BLASTp analysis, we revealed that sialic acid biosynthesis is widespread amongst algae. Using bioinformatics, NDP-β-L-rhamnose biosynthesis was explored in P. parvum and across other algae. We propose that the haptophytes have acquired bacterial TDP-β-L-rhamnose biosynthetic genes from horizontal gene transfer and subsequently passed them on to some dinoflagellate species. Sugar-nucleotide profiling of two representative algae support this proposition. Page | 2 List of Contents Abstract .............................................................................................................................. 2 List of Contents ................................................................................................................... 3 List of Figures ...................................................................................................................... 7 List of Tables ..................................................................................................................... 10 List of Supplementary Material .......................................................................................... 11 Acknowledgements ........................................................................................................... 12 Declaration of Authorship ................................................................................................. 14 Abbreviations ................................................................................................................... 15 Publications Arising from this PhD ..................................................................................... 20 Author Contributions ........................................................................................................ 21 1 Thesis Introduction and Outlines ............................................................................ 23 1.1 Introduction ........................................................................................................... 24 1.1.1 Harmful algal blooms .................................................................................................. 24 1.1.2 Prymnesium parvum ................................................................................................... 25 1.1.3 Prymnesium parvum on the Norfolk Broads ............................................................... 30 1.1.4 Prymnesium parvum toxins......................................................................................... 32 1.1.5 Factors affecting growth and toxicity ......................................................................... 38 1.1.6 Current monitoring and management strategies ....................................................... 42 1.2 Objectives and outline of the thesis ........................................................................ 45 1.3 References ............................................................................................................. 47 2 Genetic and Metabolite Assessment of a Harmful Algal Bloom; Prymnesium parvum and its Toxins .................................................................................................................... 56 2.1 Abstract ................................................................................................................. 57 2.2 Introduction ........................................................................................................... 58 2.3 Results ................................................................................................................... 61 2.3.1 Study site – fish kill March 2015 ................................................................................. 61 2.3.2 Optical microscopy of water samples ......................................................................... 62 2.3.3 Genetic analysis of microbial community ................................................................... 63 2.3.4 Detection of Prymnesin-1 & -2 in P. parvum 946/6 .................................................... 65 2.3.5 Detection of Prymnesin-B1 in natural water samples and fish gills ........................... 67 2.3.6 Monitoring of P. parvum by quantitative real-time PCR ............................................ 70 2.4 Discussion .............................................................................................................. 72 2.5 Materials and Methods .......................................................................................... 75 Page | 3 2.5.1 P. parvum culture conditions ...................................................................................... 75 2.5.2 Study site – fish kill March 2015 ................................................................................. 75 2.5.3 Optical microscopy ...................................................................................................... 76 2.5.4 Genetic analysis of microbial community ................................................................... 76 2.5.5 Detection of Prymnesin-1 & -2 in P. parvum 946/6 .................................................... 76 2.5.6 Detection of Prymnesin-B1 in natural water samples and fish gills ........................... 77 2.5.7 Monitoring P. parvum by quantitative real-time PCR................................................. 78 2.6 References ............................................................................................................. 79 3 Isolation and Characterization of a Double Stranded DNA Megavirus Infecting the Toxin-Producing Haptophyte Prymnesium parvum ............................................................. 82 3.1 Abstract ................................................................................................................. 83 3.2 Introduction ........................................................................................................... 84 3.3 Results ................................................................................................................... 86 3.3.1 Optical microscopy of natural P. parvum populations ............................................... 86 3.3.2 Isolation of whole viral communities .......................................................................... 86 3.3.3 Isolation of lytic virus particles ................................................................................... 88 3.3.4 Virus morphology, host range, and infectious properties .......................................... 90 3.3.5 Genome sequencing and phylogenetic analysis ......................................................... 93 3.4 Discussion .............................................................................................................. 97 3.5 Materials and Methods ........................................................................................ 100 3.5.1 Prymnesium parvum culture conditions ................................................................... 100 3.5.2 Optical microscopy of natural P. parvum populations ............................................. 100 3.5.3 Isolation and analysis of whole viral communities ................................................... 100 3.5.4 Isolation of lytic virus particles ................................................................................
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