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Characterizing the Bacterial Fish Pathogen Flavobacterium Columnare, and Some Factors Affecting Its Pathogenicity

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Characterizing the Bacterial Fish Pathogen Flavobacterium Columnare, and Some Factors Affecting Its Pathogenicity JYVÄSKYLÄ STUDIES IN BIOLOGICAL AND ENVIRONMENTAL SCIENCE 206 Heidi Kunttu Characterizing the Bacterial Fish Pathogen Flavobacterium columnare, and Some Factors Affecting its Pathogenicity JYVÄSKYLÄ STUDIES IN BIOLOGICAL AND ENVIRONMENTAL SCIENCE 206 Heidi Kunttu Characterizing the Bacterial Fish Pathogen Flavobacterium columnare, and Some Factors Affecting its Pathogenicity Esitetään Jyväskylän yliopiston matemaattis-luonnontieteellisen tiedekunnan suostumuksella julkisesti tarkastettavaksi yliopiston Ylistönrinteellä, salissa YAA303 toukokuun 8. päivänä 2010 kello 12. Academic dissertation to be publicly discussed, by permission of the Faculty of Mathematics and Science of the University of Jyväskylä, in Ylistönrinne, hall YAA303, on May 8, 2010 at 12 o'clock noon. UNIVERSITY OF JYVÄSKYLÄ JYVÄSKYLÄ 2010 Characterizing the Bacterial Fish Pathogen Flavobacterium columnare, and Some Factors Affecting its Pathogenicity JYVÄSKYLÄ STUDIES IN BIOLOGICAL AND ENVIRONMENTAL SCIENCE 206 Heidi Kunttu Characterizing the Bacterial Fish Pathogen Flavobacterium columnare, and Some Factors Affecting its Pathogenicity UNIVERSITY OF JYVÄSKYLÄ JYVÄSKYLÄ 2010 Editor Timo Marjomäki Department of Biological and Environmental Science, University of Jyväskylä Pekka Olsbo Publishing Unit, University Library of Jyväskylä Jyväskylä Studies in Biological and Environmental Science Editorial Board Jari Haimi, Anssi Lensu, Timo Marjomäki, Varpu Marjomäki Department of Biological and Environmental Science, University of Jyväskylä Cover pictures by Heidi Kunttu URN:ISBN:978-951-39-3867-3 ISBN 978-951-39-3867-3 (PDF) ISBN 978-951-39-3853-6 (nid.) ISSN 1456-9701 Copyright © 2010 , by University of Jyväskylä Jyväskylä University Printing House, Jyväskylä 2010 ABSTRACT Kunttu, Heidi Characterizing the bacterial fish pathogen Flavobacterium columnare, and some factors affecting its pathogenicity Jyväskylä: University of Jyväskylä, 2010, 69 p. (Jyväskylä Studies in Biological and Environmental Science ISSN 1456-9701; 206) ISBN 978-951-39-3867-3 (PDF), 978-951-39-3853-6 (nid.) Yhteenveto: Kalapatogeeni Flavobacterium columnare -bakteerin ominaisuuksia ja patogeenisuuteen vaikuttavia tekijöitä Diss. Flavobacterium columnare is a bacterial pathogen of fresh water fish causing lethal columnaris disease worldwide. At Finnish fish farms, columnaris disease has occurred since the early 1980s, and is a serious problem in salmonid farming in Finland. Currently, the only effective treatment is with antibiotics. Factors related to the pathogenicity of F. columnare, transmission of columnaris disease and the immunity of salmonids to columnaris infections are poorly known. F. columnare strains isolated from Finnish fish farms were characterized geno- and phenotypically, virulence and transmission experiments were conducted, and the efficacy of two immunostimulants against columnaris infections in rainbow trout (Oncorhynchus mykiss Walbaum) fingerlings was evaluated. Finnish F. columnare strains constituted a genetically homogeneous group that differed from strains isolated from other parts of the world and tolerated narrower pH and salinity ranges than F. columnare type strain (NCIMB 2248T). Finnish strains could be divided into seven genetic groups, which can co-occur during the same outbreak at fish farms. Among the genetic groups, four colony types were formed. Formation of rhizoid colonies is suggested to be a prerequisite for virulence of F. columnare. Colony types may have a role in the infection process and persistence of F. columnare at fish farms. The bacterium was able to survive in fresh water and also as a saprophyte, and to use saprophytism as a transmission strategy. These properties, together with co- occurrence of different genetic groups, may promote the continuous nature of outbreaks at fish farms and lead to development of highly virulent F. columnare strains. Immunostimulation was effective in boosting innate immune defence parameters of rainbow trout, but was inefficient in protecting fish against F. columnare infections. This suggests that antibody-mediated immunity is also essential in protecting fish from columnaris disease. Keywords: Colony type; columnaris disease; Flavobacterium columnare; immunostimulation; saprophytism; transmission; virulence. Heidi Kunttu, University of Jyväskylä, Department of Biological and Environmental Science, P.O. Box 35, FI-40014 University of Jyväskylä, Finland Author’s address Heidi Kunttu Department of Biological and Environmental Science P.O. Box 35 FI-40014 University of Jyväskylä Finland [email protected] Supervisors Professor E. Tellervo Valtonen Department of Biological and Environmental Science P.O. Box 35 FI-40014 University of Jyväskylä Finland Docent Ilmari Jokinen Department of Biological and Environmental Science P.O. Box 35 FI-40014 University of Jyväskylä Finland Dr. Lotta-Riina Suomalainen Department of Biological and Environmental Science P.O. Box 35 FI-40014 University of Jyväskylä Finland Reviewers Docent Tom Wiklund Laboratory of Aquatic Pathobiology Åbo Akademi University BioCity, Artillerigatan 6 FI-20520 Åbo Finland Dr. Craig Shoemaker Aquatic Animal Health Research Unit United States Department of Agriculture Agricultural Research Service 990 Wire Road Auburn, AL 36832 USA Opponent Dr. Jean-François Bernardet L’institut National de la Recherche Agronomique Laboratoire de Virologie et Immunologie Domaine de Vilvert 78350 Jouy-en-Josas France CONTENTS LIST OF ORIGINAL PUBLICATIONS ABBREVIATIONS 1 INTRODUCTION ..................................................................................................... 9 1.1 Columnaris disease at fish farms ................................................................... 9 1.2 Flavobacterium columnare ................................................................................ 10 1.3 Studying the genetic diversity of bacteria ................................................... 11 1.4 Virulence factors of fish pathogenic bacteria.............................................. 13 1.5 Host immune defence versus virulence mechanisms of pathogens ....... 14 1.6 Influence of fish farming conditions on disease outbreaks ...................... 16 1.7 Curing and preventing diseases at fish farms and enhancing immune defence of fish .................................................................................. 17 2 AIMS OF THE STUDY ........................................................................................... 19 3 SUMMARY OF MATERIALS AND METHODS ................................................ 20 3.1 Bacterial strains ............................................................................................... 20 3.2 Fish and experimental setup of bath challenge (II, V) ............................... 21 3.3 Genomic analyses of Flavobacterium columnare strains (I) ......................... 22 3.4 Growth features of F. columnare strains (I) .................................................. 22 3.5 Experiments on colony morphology types formed by F. columnare strains (II, III) ................................................................................................... 22 3.5.1 Genomic analyses and whole cell proteins (II)................................ 23 3.5.2 Adhesion on polystyrene (II, III) ....................................................... 24 3.5.3 Adhesion on gill tissue of rainbow trout (II) ................................... 24 3.5.4 Inhibition of adhesion (III) ................................................................. 24 3.5.5 Choindroitin AC lyase activity (III) .................................................. 25 3.6 Saprophyte experiment (IV) .......................................................................... 25 3.7 Transmission experiment (IV) ...................................................................... 25 3.8 Survival in water (IV) ..................................................................................... 26 3.9 Immunostimulant experiments (V) .............................................................. 26 3.9.1 Trial 1: Feeding with yeast β-glucan ................................................. 26 3.9.2 Trial 2: Injection with yeast β-glucan ................................................ 27 3.9.3 Trial 3: Feeding with β-hydroxy-β-methylbutyrate (HMB) .......... 27 3.9.4 Determining the immune status of fish ............................................ 27 4 RESULTS AND DISCUSSION .............................................................................. 29 4.1 Finnish Flavobacterium columnare strains (I) ................................................ 29 4.1.1 Genetic properties ................................................................................ 29 4.1.2 Growth features ................................................................................... 31 4.2 Colony types formed by Finnish F. columnare strains (II, III) ................... 32 4.2.1 Genetic basis of differential colony formation (II) .......................... 33 4.2.2 Relationship between virulence (II), adhesion (II, III) and chondroitin AC lyase activity (III) of the colony types .................. 35 4.2.3 Inhibition of adhesion (III) ................................................................. 39 4.3 Saprophytic life style and transmission properties of F. columnare (IV) ... 40 4.4 Immunostimulation of rainbow trout against columnaris disease (V)... 42 4.4.1 Effect on immune status ..................................................................... 42 4.4.2 Protection
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