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Gill Disease in Finfish Aquaculture with Particular Emphasis on Amoebic Gill Disease

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Gill Disease in Finfish Aquaculture with Particular Emphasis on Amoebic Gill Disease GILL DISEASE IN FINFISH AQUACULTURE WITH PARTICULAR EMPHASIS ON AMOEBIC GILL DISEASE Jamie Kian Downes, BSc, MSc Submitted in fulfillment of the requirements of the degree of Doctor of Philosophy Supervised by Dr Eugene MacCarthy, Dr Ian O’Connor, Dr Hamish Rodger & Dr Neil Ruane Submitted to Galway/Mayo Institute of Technology August 2017 GILL DISEASE IN FINFISH AQUACULTURE WITH PARTICULAR EMPHASIS ON AMOEBIC GILL DISEASE PhD Thesis Jamie Downes Submitted in fulfillment of the requirements of the degree of Doctor of Philosophy Galway/Mayo Institute of Technology Supervised by Dr Eugene MacCarthy, Dr Ian O’Connor, Dr Hamish Rodger & Dr Neil Ruane This project is funded under the Marine Institute Research Fellowship Programme (project MEFSS/PhD/2013) in conjunction with the Galway-Mayo Institute of Technology. I Author: Jamie Kian Downes Title: Gill disease in finfish aquaculture with emphasis on amoebic gill disease Abstract Gill disease is one of the most significant challenges facing global salmon aquaculture and in terms of economic impact; amoebic gill disease (AGD) caused by the free living protozoan Neoparamoeba perurans is perhaps the most destructive. However, gill disease is often multifactorial, with numerous putative pathogens identified as potentially playing a role. AGD was first described in Irish aquaculture in 1995. Between the years 1995 and 2010, there were sporadic and relatively minor outbreaks of AGD. Since the re-emergence of the disease in 2011/2012, greater focus has been placed on gill health. This research aimed to investigate gill disease and in particular the re-emergence of AGD caused by N. perurans in Irish aquaculture. Through this it was hoped to provide the industry with the tools and information to help improve management of gill disease as well as fish health and welfare. With respect to this, Chapter 2 of this thesis details the effort to develop and validate a real-time TaqMan® PCR assay to detect Neoparamoeba perurans in Atlantic salmon gills. Furthermore, it describes the use of this assay to monitor disease progression on a marine Atlantic salmon farm in Ireland in conjunction with gross gill pathology and histopathology. As molecular diagnosis of AGD remains a high priority for much of the international salmon farming industry, Chapter 3 evaluates the suitability of currently available molecular assays in conjunction with the most appropriate non-destructive sampling methodology. In addition it compares this methodology with traditional screening methods of gill scoring and histopathology. Chapter 4 addresses the complex and multifactorial nature of gill disorders. Co-infections are common on farms and there is a lack of knowledge in relation to interactions and synergistic effects of these agents. The advances in molecular diagnostics have made it possible in Chapter 5 to identify N. perurans as the causative agent in the earliest AGD outbreaks. In addition to this, a number of other putative pathogens were also identified in these early cases of gill disease. Finally, Chapter 6 concludes the findings of this research and how they relate to the current knowledge of gill health and welfare. II Declaration I hereby declare that the results presented are to the best of my knowledge correct, and that this thesis represents my own original work, carried out during the designated research project period, and has not been taken from the work of others save and to the extent that such work has been cited and acknowledged within the text of my work. Signed: , candidate ID No. G00170432 Date: 25/08/2017 III Acknowledgement Firstly, I would like to express my sincere gratitude to my supervisors Eugene MacCarthy (GMIT), Ian O’Connor (GMIT), Hamish Rodger (Fish Vet Group) and Neil Ruane (FHU, Marine Institute) for their support, guidance and valuable advice on all aspects of the thesis. I would like to thank the Marine Institute for providing the funding and opportunity for this project as well as GMIT for facilitating the project. A special thanks to my colleagues in CSIRO, Australia, Dr. Mat Cook and Dr. Richard Taylor for their encouragement since meeting them at the first Gill health Initiative. I can’t thank them enough for arranging for me to visit their labs in Australia and for their hospitality during the visit. The bloody Mary oyster shot could be left out next time. Not forgetting Dr. Megan Rigby and Dr. Ben Maynard for their assistance with the collaboration in this study. I am very grateful to Tadaishi Yatabe, (CADMS, UC Davis) for getting involved and helping carry out analysis on the interactions of pathogens and for his advice and guidance in preparing the resulting publication. A big thank you to all members of the Fish Health Unit in the MI who I have worked with over the past 4 years. You were always there when a little bit of help or advice was needed as well as showing me the ropes when I first started. Also thank you to Kathy Henshilwood for her guidance when starting out with the molecular work. Thank you to Eve Collins for her help analysing the histology for this project but also for always being available to offer sound advice. Also, a massive thank you to Teresa Morrissey for not only helping out whenever needed, but for also helping to keep me sane through the last 4 years. Thank you to my family and friends who for the most part weren’t really sure what I was doing. But the support they provided when breaking away from the thesis was invaluable. Thank you especially to my mother Johanna, for the all the support and encouragement she has given me, not just in the last 4 years during this study but from the very beginning. I certainly wouldn’t be where I am today without her help. IV Contents Contents Legends to Figures ............................................................................................................... VIII Legend to Tables ..................................................................................................................... X Introduction ............................................................................................................................. 1 1.1 Salmon Aquaculture ...................................................................................................... 2 1.2 Gill Disease ................................................................................................................... 3 1.3 Non-infectious Gill Disorders ....................................................................................... 5 1.4 Amoebic Gill Disease .................................................................................................... 6 1.4.1 AGD in Ireland ......................................................................................................... 7 1.4.2 Pathology ................................................................................................................. 8 1.4.3 Morphology and Phylogeny ..................................................................................... 9 1.4.4 Diagnosis of AGD .................................................................................................. 10 1.4.5 Infection trials ........................................................................................................ 16 1.4.6 Treatment of AGD ................................................................................................. 18 1.4.7 Transmission Pathways .......................................................................................... 20 1.5 Multifactorial Gill Disease .......................................................................................... 23 1.6 Objectives .................................................................................................................... 26 1.7 Summary of Chapters .................................................................................................. 27 1.8 Literature Cited ........................................................................................................... 30 A longitudinal study of amoebic gill disease on a marine Atlantic salmon, Salmo salar L., farm utilising a real-time PCR assay for the detection of Neoparamoeba perurans . .... 43 2.1 Abstract ....................................................................................................................... 44 2.2 Introduction ................................................................................................................. 45 2.3 Materials and Methods ................................................................................................ 47 2.3.1 Amoeba isolates and culture: ................................................................................. 47 2.3.2 DNA extraction and conventional PCR of cultured amoebae: ............................... 48 2.3.3 Real time primer and probe design: ....................................................................... 48 2.3.4 TaqMan® real-time PCR: ...................................................................................... 49 2.3.5 Validation of reaction efficiency, sensitivity and specificity: ................................ 49 2.3.6 Reproducibility: ..................................................................................................... 50 2.3.7 Longitudinal study site and sampling details: ........................................................ 50 2.3.8 In-situ hybridisation: .............................................................................................. 51 2.3.9
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