Analysis of Spounaviruses as a Case Study for the Overdue Reclassification of Tailed Phages

Barylski, Jakub [Department of Molecular Virology, Institute of Experimental Biology, Faculty of Biology, Adam Mickiewicz University in Poznań, Collegium Biologicum - Umultowska 89, 61-614 Poznań, Poland] Enault, François [Université Clermont Auvergne, CNRS, LMGE, F-63000 Clermont-Ferrand, France] Dutilh, Bas E [Theoretical Biology and Bioinformatics, Department of Biology, Science for Life, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands] Schuller, Margo BP [Theoretical Biology and Bioinformatics, Department of Biology, Science for Life, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands] Edwards, Robert A [Department of Biology, San Diego State University, 5500 Campanile Drive, San Diego, CA 92182, USA] Gillis, Annika [UCL] Klumpp, Jochen [Institute of Food, Nutrition and Health, ETH Zurich, Schmelzbergstrasse 7, 8092 Zurich, Switzerland] Knezevic, Petar [Department of Biology and Ecology, Faculty of Sciences, University of Novi Sad, Novi Sad, Serbia] Krupovic, Mart [Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur, 25 rue du Dr. Roux, 75015 Paris, France] Kuhn, Jens H [Integrated Research Facility at Fort Detrick, Division of Clinical Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, B-8200 Research Plaza, Fort Detrick, Frederick, MD 21702, USA] Lavigne, Rob [Laboratory of Gene Technology, Department of Biosystems, KU Leuven, Kasteelpark Arenberg 21 - box 2462, 3001 Leuven, Belgium] Oksanen, Hanna M [Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, P.O. Box 56 (Viikinkaari 9B), 00014 Helsinki, Finland] Sullivan, Matthew B [Department of Microbiology, The Ohio State University, 496 W 12thAvenue, Columbus, OH 43210, USA] Jang, Ho Bin [Department of Microbiology, The Ohio State University, 496 W 12thAvenue, Columbus, OH 43210, USA] Simmonds, Peter [Nuffield Department of Medicine, University of Oxford, Peter Medawar Building, South Parks Road, Oxford OX1 3SY, UK] Aiewsakun, Pakorn [Nuffield Department of Medicine, University of Oxford, Peter Medawar Building, South Parks Road, Oxford OX1 3SY, UK] Wittmann, Johannes [Leibniz-Institut DSMZ—German Collection of Microorganisms and Cell Cultures, Inhoffenstr. 7B, 38124 Braunschweig, Germany] Tolstoy, Igor [National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, 8600 Rockville Pike, Bethesda MD 20894, USA] Brister, J Rodney [National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, 8600 Rockville Pike, Bethesda MD 20894, USA] Kropinski, Andrew M [Department of Food Science, University of Guelph, Guelph, Ontario, Canada] Adriaenssens, Evelien M [Department of Functional & Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Biosciences Building, Crown Street, Liverpool L69 7ZB, UK] et al.[show all]

Tailed bacteriophages are the most abundant and diverse viruses in the world, with genome sizes ranging from 10 kbp to over 500 kbp. Yet, due to historical reasons, all this diversity is confined to a single virus order—Caudovirales, composed of just four families: Myoviridae, Siphoviridae, Podoviridae, and the newly created Ackermannviridae family. In recent years, this morphology-based classification scheme has started to crumble under the constant flood of phage sequences, revealing that tailed phages are even more genetically diverse than once thought. This prompted us, the Bacterial and Archaeal Viruses Subcommittee of the International Committee on Taxonomy of Viruses (ICTV), to consider overall reorganization of phage taxonomy. In this study, we used a wide range of complementary methods—including comparative genomics, core genome analysis, and marker gene phylogenetics—to show that the group of Bacillus phage SPO1-related viruses previously classified into the Spounavirinae subfamily, is clearly distinct from other members of the family Myoviridae and its diversity deserves the rank of an autonomous family. Thus, we removed this group from the Myoviridae family and created the family Herelleviridae—a new taxon of the same rank. In the process of the taxon evaluation, we explored the feasibility of different demarcation criteria and critically evaluated the usefulness of our methods for phage classification. The convergence of results, drawing a consistent and comprehensive picture of a new family with associated subfamilies, regardless of method, demonstrates that the tools applied here are particularly useful in phage taxonomy. We are convinced that creation of this novel family is a crucial milestone toward much-needed reclassification in the Caudovirales order.