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Generating Genomic Resources for Two Crustacean Species and Their Application to the Study of White Spot Disease

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Generating Genomic Resources for Two Crustacean Species and Their Application to the Study of White Spot Disease Generating genomic resources for two crustacean species and their application to the study of White Spot Disease Submitted by Bas Verbruggen To the University of Exeter as a thesis for the degree of Doctor of Philosophy in Biological Sciences, September 2016 This thesis is available for Library use on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement I certify that all material in this thesis which is not my own work has been identified and that no material has previously been submitted and approved for the award of a degree by this or any other University. Signature: ……………………………………(Bas Verbruggen) Abstract Over the last decades the crustacean aquaculture sector has been steadily growing, in order to meet global demands for its products. A major hurdle for further growth of the industry is the prevalence of viral disease epidemics that are facilitated by the intense culture conditions. A devastating virus impacting on the sector is the White Spot Syndrome Virus (WSSV), responsible for over US $ 10 billion in losses in shrimp production and trade. The Pathogenicity of WSSV is high, reaching 100 % mortality within 3-10 days in penaeid shrimps. In contrast, the European shore crab Carcinus maenas has been shown to be relatively resistant to WSSV. Uncovering the basis of this resistance could help inform on the development of strategies to mitigate the WSSV threat. C. maenas has been used widely in studies on ecotoxicology and host-pathogen interactions. However, like most aquatic crustaceans, the genomic resources available for this species are limited, impairing experimentation. Therefore, to facilitate interpretations of the exposure studies, we first produced a C. maenas transcriptome and genome scaffold assembly. We also produced a transcriptome for the European lobster (Homarus gammarus), an ecologically and commercially important crustacean species in United Kingdom waters, for use in comparing WSSV responses in this, a susceptible species, and C. maenas. For the C. maenas transcriptome assembly we isolated and pooled RNA from twelve different tissues and sequenced RNA on an Illumina HiSeq 2500 platform. After de novo assembly a transcriptome encompassing 212,427 transcripts was produced. Similar, the H. gammarus transcriptome was based on RNA from nine tissues and contained 106,498 transcripts. The transcripts were filtered and annotated using a variety of tools (including BLAST, MEGAN and RSEM) and databases (including GenBank, Gene Ontology and KEGG). The annotation rate for transcripts in both transcriptomes was around 20-25 % which appears to be common for aquatic crustacean species, as a result of the lack of well annotated gene sequences for this clade. Since it is likely that the host immune system would play an important role in WSSV infection we characterized the IMD, JAK/STAT, Toll- like receptor and other innate immune system pathways. We found a strong overlap between the immune system pathways in C. maenas and H. gammarus. In addition we investigated the sequence diversity of known WSSV interacting proteins amongst susceptible penaeid shrimp/lobster and the more resistant C. maenas. There were differences in viral receptor sequences, like Rab7, that correlate with a less efficient infection by WSSV. Page | 1 To produce the genome scaffold assembly for C. maenas we isolated DNA from muscle tissue and produced both paired-end and mate pair libraries for processing on the Illumina HiSeq 2500 platform. A de novo draft genome assembly consisting of 338,980 scaffolds and covering 362 Mb (36 % of estimated genome size) was produced, using SOAP-denovo2 coupled with the BESST scaffolding system. The generated assembly was highly fragmented due to the presence of repetitive areas in the C. maenas genome. Using a combination of ab initio predictors, RNA-sequencing data from the transcriptome datasets and curated C. maenas sequences we produced a model encompassing 10,355 genes. The gene model for C. maenas Dscam, a gene potentially involved in (pan)crustacean immune memory, was investigated in greater detail as manual curation can improve on the results of ab initio predictors. The scaffold containing C. maenas Dscam was fragmented, thus only contained the latter exons of the gene. The assembled draft genome and transcriptomes for C. maenas and H. gammarus are valuable molecular resources for studies involving these and other aquatic crustacean species. To uncover the basis of their resistance to WSSV, we infected C. maenas with WSSV and measured mRNA and miRNA expression for 7 time points spread over a period of 28 days, using RNA-Seq and miRNA-Seq. The resistance of C. maenas to WSSV infection was confirmed by the fact that no mortalities occurred. In these animals replicating WSSV was latent and detected only after 7 days, and this occurred in five of out 28 infected crabs only. Differential expression of transcripts and miRNAs were identified for each time point. In the first 12 hours post exposure we observed decreased expression of important regulators in endocytosis. Since it is established that WSSV enters the host cells through endocytosis and that interactions between the viral protein VP28 and Rab7 are important in successful infection, it is likely that changes in this process could impact WSSV infection success. Additionally we observed an increased expression of transcripts involved in RNA interference pathways across many time points, indicating a longer term response to initial viral exposure. miRNA sequencing showed several miRNAs that were differentially expressed. The most striking finding was a novel C. maenas miRNA that we found to be significantly downregulated in every WSSV infected individual, suggesting that it may play an important role in mediating the response of the host to the virus. In silico target prediction pointed to the involvement of this miRNA in endocytosis regulation. Taken together we hypothesize that C. maenas resistance to WSSV involves obstruction of viral entry by endocytosis, a process probably regulated through miRNAs, resulting in inefficient uptake of virions. Page | 2 Page | 3 Acknowledgements First of all I would like to thank my supervisors Dr. Ronny van Aerle, Dr. Eduarda Santos and Professor Charles Tyler for their continued support over the course of my PhD. Ronny did a great job at introducing me to the world of sequencing and bioinformatics. I was definitely not the only one that was sad to see him leave the University of Exeter. But even at his new job at Cefas he found time to help me out when I was stuck (or caused the server to break down). His relentless optimism makes working with him a pleasure. After Ronny’s departure Eduarda and Charles really came through as supervisors and both in their own way have filled the gap that Ronny left. I am also grateful for the long hours they have put in reading and editing my writing. Dr. Lisa Bickley was instrumental to the work presented in this thesis. I’m very grateful for the countless hours she spent in the lab making sure we had top notch sequencing libraries to work with. She was also a great companion on several conference trips. I would also like to give big thanks to the people at Cefas. Dr. Kelly Bateman did lots of experimental work for this project. Dr. Grant Stentiford’s passion for aquatic crustacea and the world outside the University is highly contagious. Finally I’m grateful to David for helping out fixing problems on the server. I’d like to thank Konrad Paszkiewicz, Karen Moore and Audrey Farbos of the Exeter Sequencing Service for processing our samples and providing access to the zeus computer cluster. I would like to thank all my colleagues from lab 201. In particular Aoife Parsons for managing to sit next to me for four years, being supportive and sharing the ups and downs of PhD life. Rhys for making my desk look tidy. Jenny for getting me away from my desk on coffee breaks and Lauren for providing entertainment on bioinformatics courses. A shout out to all my friends. Damian Rumble and Lewis Elliot for introducing me to life in the UK and sharing the PhD experience with me. Martijn, Geert, Giovanni, Floris and Marloes for our holiday trips and Halve Liter Woensdagen whenever I was back in the Netherlands. In particular I would like to thank Lauren Hitchman for her support and wisdom. I could not have finished this PhD without her. Finally I would like to thank my parents for their continued support and encouragement over the years. Page | 4 Contents Research Papers and Author’s Declaration ...................................................................... 7 List of General Abbreviations ............................................................................................ 8 Chapter 1: General Introduction ...................................................................................... 12 1.1 Crustacean Aquaculture ............................................................................................ 13 1.2 Next generation sequencing technology and applications .......................................... 18 1.3 Bio-informatics of de novo transcriptome assembly ................................................... 23 1.4 Research undertaken in this thesis ............................................................................ 41 1.5 References ................................................................................................................ 45 Chapter 2: Molecular Mechanisms
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