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Virulence of Flavobacterium Psychrophilum, Antimicrobial Treatment and Intestinal Microbiota of Rainbow Trout Oncorhynchus Mykiss

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Virulence of Flavobacterium Psychrophilum, Antimicrobial Treatment and Intestinal Microbiota of Rainbow Trout Oncorhynchus Mykiss Virulence of Flavobacterium psychrophilum, Antimicrobial Treatment and Intestinal Microbiota of Rainbow Trout Oncorhynchus mykiss by Maureen Jarau A Thesis presented to The University of Guelph In partial fulfilment of requirements for the degree of Doctor of Philosophy in Pathobiology Guelph, Ontario, Canada © Maureen Jarau, September, 2018 ABSTRACT VIRULENCE OF FLAVOBACTERIUM PSYCHROPHILUM, ANTIMICROBIAL TREATMENT AND INTESTINAL MICROBIOTA OF RAINBOW TROUT ONCORHYNCHUS MYKISS Maureen Jarau Advisors: University of Guelph, 2018 Dr. J. S. Lumsden Dr. J. I. MacInnes Flavobacterium psychrophilum, the aetiologic agent of bacterial cold-water disease (BCWD), is responsible for significant economic losses in rainbow trout Oncorhynchus mykiss aquaculture. This thesis provides insights into the a) virulence potential of F. psychrophilum isolates from Ontario in rainbow trout, b) efficacy of oral treatment in controlling F. psychrophilum infection and c) impact of prophylactic treatment on the intestinal microbiota and subsequent susceptibility to BCWD. Following a preliminary infection trial, a broad range (0 to 63% mortality) of virulence was observed for 21 Ontario F. psychrophilum isolates. The virulent isolate FPG101 produced significant mortality (p < 0.05) at the infection dose of 108 cfu fish-1 compared to the control group. Plate counting rather than the rpoC qPCR assay was found to be more sensitive for detection of splenic F. psychrophilum. A minimum inhibitory concentration test showed little variation in the antimicrobial susceptibility of six virulent isolates of F. psychrophilum. One F. psychrophilum isolate with moderate susceptibility to erythromycin (FPG101) and another isolate with low susceptibility to erythromycin (FPG105) were used in an experimental infection trial. Relative to untreated controls, erythromycin treatment significantly (p < 0.05) reduced mortality of rainbow trout infected with FPG101. Erythromycin treatment was more effective than florfenicol treatment at splenic bacterial clearance during infection period. Furthermore, using Illumina Miseq sequencing, five bacterial phyla (Proteobacteria, Tenericutes, Spirochaetes, Fusobacteria and Firmicutes) plus “unclassified Bacteria” were identified as major constituents of the intestinal microbiota in rainbow trout throughout the experimental trial period. Before prophylactic oral treatment, Tenericutes and Proteobacteria were the most abundant phyla; Mycoplasma was the most abundant genus. No significant change was observed in the relative abundance of intestinal bacterial phyla after 10-day oral treatment with erythromycin. In contrast, oral treatment with florfenicol significantly increased (p < 0.05) Proteobacteria; Sphingomonas was the most abundant bacterial genus. Neither treatment increased the susceptibility of fish to subsequent F. psychrophilum infection. ACKNOWLEDGEMENTS I would like to express my infinite gratitude to my advisors, Dr. John Lumsden and Dr. Janet MacInnes, for their guidance, moral support, patience and generosity that they have extended towards me from the very beginning of my studies. Without their contributions and supervision, this thesis would simply not have happened. I would also like to thank my advisory committee, Dr. Roselynn Stevenson, who also has played an important role in assisting my success as a PhD candidate. I would like to thank the financial supporters of my program, the Ontario Veterinary College (OVC) Scholarship, the research funding from the Natural Sciences and Engineering Research Council (NSERC), and the Ontario Ministry of Agriculture, Food, and Rural Affairs (OMAFRA) awarded to Dr. John Lumsden in support of my PhD research. I would like to extend my personal gratitude to the members of Fish Pathology Laboratory (Lumsden’s laboratory), past and present, for their support and friendship: Paul Huber, Dr. Elena Contador, Dr. Lowia Al-Housinee, Dr. Ehab Misk, Jessica Grice, Ryan Horricks, Dr. Juan-Ting Liu, Dr. Jaramar Balmori-Cedeño, Paige Vroom, Dr. Doran Kirkbright and Ryan Eagleson. Many thanks to Donna Kangas, Karla De Uslar, Cathy Bernardi and Marni Stryuk, for their administrative supports. I also would like to express my special gratitude to the staff of Hagen Aqualab of University of Guelph, especially Matthew Cornish and Mike Davis, for their technical assistance and support during my experimental infection trial. Thank you also to Jeffery Gross from the Advanced Analytic Centre, for his technical expertise and assistance with MiSeq Illumina sequencing. iv Last but not least, I would like to express my appreciation to my family for their unconditional love and support on this journey. I would like to thank my best friend, Dr. Jacklyn Ng for her continuous support, understanding and friendship. I would like to give my special thanks to my boyfriend, Dr. Mark Gosselink, who has been very supportive in every possible way, with all the love, encouragement, patience and understanding throughout this thesis. Thank you for your love, support and friendship through it all. v DECLARATION OF WORK PERFORMED All work in this thesis was performed by myself, with the following exceptions: 1. The 16S rRNA partial sequencing (Chapter 2) was done by the Animal Health Laboratory, University of Guelph (Guelph, Ontario). 2. The antimicrobial residue analyses of fish and feed samples (Chapters 3 and 4) were performed by Eurofins Analytical Laboratories Inc. (New Orleans, Louisiana). 3. MiSeq Illumina Next-generation sequencing (NGS) (Chapter 4) was done at the Advanced Analysis Centre- Genomics Facility at the University of Guelph (Guelph, Ontario). vi TABLE OF CONTENTS ABSTRACT ................................................................................................................................... ii ACKNOWLEDGEMENTS ........................................................................................................ iv DECLARATION OF WORK PERFORMED .......................................................................... vi TABLE OF CONTENTS ........................................................................................................... vii LIST OF TABLES ........................................................................................................................ x LIST OF FIGURES ..................................................................................................................... xi LIST OF SYMBOLS AND ABBREVIATIONS ...................................................................... xv CHAPTER 1: Literature Review ................................................................................................ 1 1.1 General Introduction ....................................................................................................... 1 1.2 Flavobacterium psychrophilum ....................................................................................... 2 1.2.1 Initial discovery of F. psychrophilum ......................................................................... 2 1.2.2 Taxonomy and classification ....................................................................................... 3 1.2.3 Growth, phenotypic and biochemical characteristics .................................................. 4 1.2.4 Genomic characteristics .............................................................................................. 6 1.2.5 Virulence factors ......................................................................................................... 8 1.3 Disease Associated with Flavobacterium psychrophilum ............................................ 12 1.3.1 Bacterial cold-water disease (BCWD) ...................................................................... 13 1.3.2 Rainbow trout fry syndrome (RTFS) ........................................................................ 14 1.4 Clinical Signs and Pathology of F. psychrophilum Infection ..................................... 14 1.5 Diagnosis of F. psychrophilum Infections .................................................................... 17 1.5.1 Primary isolation and identification .......................................................................... 17 1.5.2 Serodiagnosis ............................................................................................................ 18 1.5.3 Molecular techniques ................................................................................................ 19 1.6 Prevention, Control and Treatment ............................................................................. 20 1.6.1 Management practices ............................................................................................... 20 1.6.2 Vaccine development ................................................................................................ 21 1.6.3 Antimicrobial therapy ............................................................................................... 22 vii 1.6.4 Disinfection ............................................................................................................... 24 1.7 Microbiota in Fish Intestines ........................................................................................ 25 1.8 Rationale, Hypotheses and Objectives ......................................................................... 26 CHAPTER 2: Virulence of Flavobacterium psychrophilum Isolates in Rainbow Trout Oncorhynchus Mykiss (Walbaum) ............................................................................................. 29 2.1
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