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Matthew J. Gray V. Gregory Chinchar Editors Ranaviruses Lethal Pathogens of Ectothermic Vertebrates Ranaviruses Matthew J. Gray • V. Gregory Chinchar Editors Ranaviruses Lethal Pathogens of Ectothermic Vertebrates Editors Matthew J. Gray V. Gregory Chinchar Center for Wildlife Health Department of Microbiology Department of Forest, Wildlife, and Fisheries University of Mississippi Medical Center University of Tennessee Jackson , MS , USA Knoxville , TN , USA ISBN 978-3-319-13754-4 ISBN 978-3-319-13755-1 (eBook) DOI 10.1007/978-3-319-13755-1 Library of Congress Control Number: 2015935731 Springer Cham Heidelberg New York Dordrecht London © The Editor(s) (if applicable) and the Author(s) 2015 . The book is published with open access at SpringerLink.com Open Access This book is distributed under the terms of the Creative Commons Attribution Noncommercial License, which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited. All commercial rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifi cally the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfi lms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specifi c statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. Printed on acid-free paper Springer International Publishing AG Switzerland is part of Springer Science+Business Media (www.springer.com) Ranaviruses are a group of emerging pathogens responsible for mass die-offs of amphibians, fi sh, and reptiles in captive and wild populations across the globe. Global commerce of ectothermic vertebrate species and stressors may be contributing to emergence of these pathogens. Photo credits ( clockwise from top left ) : Matthew Allender, Nathaniel Wheelwright, Matthew Neimiller, Jonathan Kolby, Yi Geng, Yi Geng, Jonathan Kolby, and Rolando Mazzoni. Artwork by Jeanne Jones. v Contents Introduction: History and Future of Ranaviruses ....................................... 1 Matthew J. Gray and V. Gregory Chinchar Distribution and Host Range of Ranaviruses ............................................... 9 Amanda L. J. Duffus , Thomas B. Waltzek , Anke C. Stöhr , Matthew C. Allender , Michael Gotesman , Richard J. Whittington , Paul Hick , Megan K. Hines , and Rachel E. Marschang Ranavirus Taxonomy and Phylogeny ............................................................ 59 James K. Jancovich , Natalie K. Steckler , and Thomas B. Waltzek Ranavirus Ecology and Evolution: from Epidemiology to Extinction ....... 71 Jesse L. Brunner , Andrew Storfer , Matthew J. Gray , and Jason T. Hoverman Ranavirus Replication: Molecular, Cellular, and Immunological Events ............................................................................. 105 James K. Jancovich , Qiwei Qin , Qi-Ya Zhang , and V. Gregory Chinchar Ranavirus Host Immunity and Immune Evasion ........................................ 141 Leon Grayfer , Eva-Stina Edholm , Francisco De Jesús Andino , V. Gregory Chinchar , and Jacques Robert Comparative Pathology of Ranaviruses and Diagnostic Techniques ......... 171 Debra L. Miller , Allan P. Pessier , Paul Hick , and Richard J. Whittington Design and Analysis of Ranavirus Studies: Surveillance and Assessing Risk .......................................................................................... 209 Matthew J. Gray , Jesse L. Brunner , Julia E. Earl , and Ellen Ariel Index ................................................................................................................. 241 vii Contributors Matthew C. Allender Department of Comparative Biosciences, College of Veterinary Medicine , University of Illinois , Urbana , IL , USA Francisco De Jesús Andino Department of Microbiology and Immunology , University of Rochester Medical Center , Rochester , NY , USA Ellen Ariel College of Public Health, Medical and Veterinary Sciences, James Cook University , Townsville , QLD , Australia Jesse L. Brunner School of Biological Sciences , Washington State University , Pullman , WA , USA V. Gregory Chinchar Department of Microbiology , University of Mississippi Medical Center , Jackson , MS , USA Amanda L. J. Duffus Department of Biology , Gordon State College , Barnesville , GA , USA Julia E. Earl National Institute for Mathematical and Biological Synthesis, University of Tennessee , Knoxville , TN , USA Eva-Stina Edholm Department of Microbiology and Immunology , University of Rochester Medical Center , Rochester , NY , USA Michael Gotesman Department of Infectious Diseases and Pathology, College of Veterinary Medicine , University of Florida , Gainesville , FL , USA Matthew J. Gray Center for Wildlife Health, Department of Forestry, Wildlife and Fisheries , University of Tennessee , Knoxville , TN , USA Leon Grayfer Department of Microbiology and Immunology , University of Rochester Medical Center , Rochester , NY , USA Paul Hick Faculty of Veterinary Science , University of Sydney , Sydney , NSW , Australia ix x Contributors Megan K. Hines University of Wisconsin-Madison, School of Veterinary Medicine , Madison , WI , USA Jason T. Hoverman Department of Forestry and Natural Resources , Purdue University , West Lafayette , IN , USA James K. Jancovich Department of Biological Sciences , California State University , San Marcos , CA , USA Rachel E. Marschang Laboklin GmbH & Co. KG , Bad Kissingen , Germany Debra L. Miller Center for Wildlife Health and Department of Biomedical and Diagnostic Sciences , University of Tennessee , Knoxville , TN , USA Allan P. Pessier Institution for Conservation Research, San Diego Zoo , San Diego , CA , USA Qiwei Qin Key Laboratory of Tropical Marine Bio-Resources and Ecology , South China Sea Institute of Oceanology, Chinese Academy of Sciences , Guangzhou , China Jacques Robert Department of Microbiology and Immunology , University of Rochester Medical Center , Rochester , NY , USA Natalie K. Steckler Department of Infectious Diseases and Pathology, College of Veterinary Medicine , University of Florida , Gainesville , FL , USA Anke C. Stöhr Institute of Environmental and Animal Hygiene, University of Hohenheim , Stuttgart , Germany Andrew Storfer School of Biological Sciences , Washington State University , Pullman , WA , USA Thomas B. Waltzek Department of Infectious Diseases and Pathology, College of Veterinary Medicine , University of Florida , Gainesville , FL , USA Richard J. Whittington Faculty of Veterinary Science , University of Sydney , Sydney , NSW , Australia Qi-Ya Zhang State Key Laboratory of Freshwater Ecology and Biotechnology , Institute of Hydrobiology, Chinese Academy of Sciences , Wuhan , Hubei , China Introduction: History and Future of Ranaviruses Matthew J. Gray and V. Gregory Chinchar What a wonderful bird the frog are — When he stand he sit almost ; When he hop , he fl y almost . He ain ’ t got no sense hardly ; He ain ’ t got no tail hardly either . When he sit , he sit on what he ain ’ t got almost . Anonymous Allan Granoff (1923–2012) serendipitously isolated the fi rst ranaviruses (Granoff et al. 1966 ) while attempting to generate cell lines that would support the replication of Lucke herpesvirus. Although one of Allan’s isolates, Frog virus 3 (FV3), subsequently became the best-characterized member of both the genus ( Ranavirus ) and the family ( Iridoviridae ); the impact of that discovery was not fully appreciated at the time. FV3 was neither the fi rst iridovirus to be recognized as a pathogen of lower vertebrates or the fi rst isolated. Those honors belonged to lymphocystis disease virus (LCDV) and invertebrate iridovirus 1 (IIV1), respec- tively (Wissenberg 1965 ; Xeros 1954 ). LCDV is responsible for a generally non-life threatening, but disfi guring, disease in fi sh characterized by the appearance of wart- like growths on the skin and (rarely) internal organs, whereas IIV1 is the causative agent of latent and patent infections in crane fl y larvae. Despite its lack of primacy, FV3 was studied because, in keeping with the mission of St. Jude Hospital, it was initially thought to be linked to adenocarcinoma in frogs and thus could be a useful model of human malignancies. Furthermore, unlike LCDV and IIV1, it could be readily grown in cultured cells and was thus amenable to detailed molecular charac- terization. Although its role in tumor development was soon proven incorrect, FV3 served as a gateway into understanding the replication strategy of a heretofore poorly studied virus family. Moreover, over the next 20 years, its study led to M. J. Gray (*) Center for Wildlife Health, Department of Forestry, Wildlife and Fisheries , University of Tennessee , 274 Ellington Plant Sciences Building , Knoxville , TN 37996-4563 , USA e-mail: [email protected] V. G. Chinchar