A critical appraisal of viral taxonomy

263 Pages·1983·19.734 MB·English

by  Matthews, Richard Ellis Ford

Critical Appraisal
Viral Taxonomy
Editor
R. E. F. Matthews, Ph.D.
Professor of Microbiology
University of Auckland
Auckland, New Zealand
Boca Raton London New York
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Library of Congress in Publication Data
Main entry under title:
A Critical appraisal of viral taxonomy.
Bibliography: p.
Includes index.
1. Virology—Classification. I. Matthews,
R. E. F. (Richard Ellis Ford), 1921-
[DNLM: 1. Viruses—Classification. QW. 15 C934]
QR394.C74 1983 576’ .64’012 82-17795
ISBN 0-8493-5648-2.
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PREFACE
By the early 1960s many hundreds of viruses had been found infecting vertebrates,
invertebrates, plants, and bacteria. The classification and nomenclature of these agents were
in a chaotic state. At a Microbiology Congress in Moscow in 1966 the International Com-
mittee for Nomenclature of Viruses was launched. Many problems were encountered, par-
ticularly in the early years, but steady progress was made. By 1981, 54 virus families and
groups, with a total of 1372 member viruses, had been delineated and had received formal
international approval. In spite of this progress many problems remain for the future.
The overall aim of this volume is to review critically the current state of, and future
prospects for developments in viral taxonomy. Most of the contributors have recently had
substantial periods of service on the Executive Committee and subcommittees of the Inter-
national Committee on Taxonomy of Viruses (ICTV) as follows:
H. -W. Ackermann (3 years as vice-chairman and 6 years as chairman of the Bacterial
Virus Subcommittee); J. G. Atherton (6 years as chairman of the Code and Data subcom-
mittee); K. W. Buck (6 Years as a member of the Fungal Virus subcommittee and 1 year
as chairman); R. I. B. Francki (3 years as a member of the Plant Virus subcommittee and
6 years as chairman); J. F. Longworth (3 years as a member of Executive Committee and
the Invertebrate Virus subcommittee); R. E. F. Matthews (6 years as President of the ICTV);
F. A. Murphy (3 years as vice-chairman and 6 years as chairman of the Vertebrate Virus
subcommittee). Chairmen of subcommittees were also ex officio members of the Executive
Committee.
All these workers except K. W. Buck and J. F. Longworth retired from the ICTV Executive
Committee in August 1981. It should be stressed that the views express in each chapter are
those of the individual author. They are not necessarily shared either by the editor, or by
the ICTV.
In the first chapter I have outlined the historical development of the subject, emphasizing
the difficulties along the way and the extent to which these have been overcome. The chapter
concludes with a summary of the state of viral taxonomy at August 1981. Chapters 2 to 6
consider past, present, and future problems that are particularly relevant for the taxonomy
of viruses infecting vertebrates, plants, bacteria, invertebrates, and fungi. In Chapter 7, J.
A. Dodds gives a brief account of the structure and biology of the new viruses and virus-
like particles being found in eukaryotic algae and in protozoa. The taxonomy of these agents
poses significant problems. Chapter 8 summarizes the progress that has been made in
developing a universal system for the collection, and computer-based storage and retrieval
of virus data. Last, Chapter 9 outlines my personal views on the future prospects for viral
taxonomy, with particular emphasis on the difficult problems associated with the delineation
and naming of virus species.
I wish to thank all the contributors for their ready cooperation in the production of this
volume. I thank particularly the following colleagues who read and commented upon parts
or all of the manuscripts for my own contributions: H. -W. Ackermann, A. R. Bellamy,
D. W. Dye, F. Fenner, R. I. B. Francki, A. J. Gibbs, B. D. Harrison, D. W. Kingsbury,
J. F. Longworth, J. Maurin, F. A. Murphy. H. G. Pereira, and P. Wildy.
THE EDITOR
Richard E. F. Matthews, Ph.D., Sc.D., is Professor Microbiology and Head of the
Department of Cell Biology in the University of Auckland, Auckland, New Zealand. He
received an M.Sc. degree in Botany from the University of New Zealand in 1941 and a
Ph.D. from the University of Cambridge, England in 1948, followed by the Sc.D. in 1964.
He has published 130 research papers mainly in the field of plant virology, together with
two books in this field. From 1974 to 1981 he was President of the International Committee
for Taxonomy of Viruses and was editor of two reports for the committee published in 1979
and 1982. He was made a life member of the organization in 1981. He is a member of the
Society for General Microbiology and the Biochemical Society of London. He is a Fellow
of the New Zealand Institute of Chemists and the Royal Society of New Zealand. In 1974
he was elected a Fellow of the Royal Society of London.
CONTRIBUTORS
Hans-Wolfgang Ackermann, M. D. I. R. Holmes
Professor Department of Microbiology
Department of Microbiology University of Queensland
Faculty of Medicine St. Lucia, Queensland
Lava1 University Australia
Quebec, Canada
E. H. Jobbins
J. G. Atherton, Ph.D. Department of Microbiology
Reader in Virology University of Queensland
University of Queensland St. Lucia, Queensland
St. Lucia, Queensland Australia
Australia
John F. Longworth, M. S.
K. W. Buck, Ph.D.
Director
Reader in Fungal and Plant Virology
Entomology Division
Department of Pure and Applied Biology
Department of Scientific and Industrial
Imperial College of Science and
Research
Technology
Auckland, New Zealand
London, England
J. Allan Dodds, Ph.D. R. E. F. Matthews, Ph.D.
Associate Professor Professor of Microbiology
Department of Plant Pathology University of Auckland
University of California Auckland, New Zealand
Riverside, California
F. A. Murphy, D.V.M., Ph.D.
R. I. B. Francki, Ph.D. Professor of Microbiology
Reader in Plant Pathology College of Veterinary Medicine and
Waite Agricultural Research Institute Biomedical Sciences
University of Adelaide Colorado State University
Glen Osmond, South Australia Ft. Collins, Colorado
TABLE OF CONTENTS
Chapter 1
The History of Viral Taxonomy.. ........................................................ 1
R. E. F. Matthews
Chapter 2
Current Problems in Vertebrate Virus Taxonomy.. ...................................... 37
Frederick A. Murphy
Chapter 3
Current Problems in Plant Virus Taxonomy.. .......................................... .63
R. I. B. Francki
Chapter 4
Current Problems in Bacterial Virus Taxonomy ........................................ 105
Hans-Wolfgang Ackermann
Chapter 5
Current Problems in Insect Virus Taxonomy .......................................... .l23
John F. Longworth
Chapter 6
Current Problems in Fungal Virus Taxonomy .......................................... 139
K. W. Buck
Chapter 7
New Viruses of Eukaryotic Algae and Protozoa.. ...................................... 177
J. Allan Dodds
Chapter 8
Virus Data-Problems in Collection, Storage, and Retrieval .......................... .l89
J. G. Atherton, I. R. Holmes, and E. H. Jobbins
Chapter 9
Future Prospects for Viral Taxonomy ................................................. .219
R. E. F. Matthews
Index .................................................................................. -247
Chapter 1
THE HISTORY OF VIRAL TAXONOMY
R . E . F . Matthews
TABLE OF CONTENTS
I . Introduction ...................................................................... 2
I1 . The Period Up to 1961 ........................................................... 2
A . Individual Plant Virologists ............................................... 2
B . Individual Animal Virologists ............................................ 4
C . Attempts at International Cooperation .................................... 5
111 . The Period Leading Up to the Moscow Conference (1962-1966) ................ 8
IV . The Presidency of P . Wildy (1966-1970) ....................................... 12
V1 . The Present State of Viral Taxonomy ........................................... 22
V11 . The Rules of Viral Nomenclature. 1981 ........................................ 31
References ............................................................................... 33
2 A Critical Appraisal of Viral Taxonomy
I. INTRODUCTION
Viruses have been found in almost all the major groups of prokaryotic and eukaryotic
organisms. The number of distinct viruses that have been described cannot be ascertained
with any precision, but the total must be several thousand. There are over 2000 descriptions
of viruses infecting bacteria alone. Man has an innate desire to classify and name all of the
natural objects which he studies, and viruses are no exception. However, there are many
different possible ways of classifying and naming biological objects, and judgments must
be made that do not have a strictly scientific basis. Thus there is ample room for differences
of opinion, emotional attachment to a particular point of view, and unwillingness to com-
promise. For these reasons the development of viral taxonomy has been marked by some
stormy interludes. In this introductory chapter the development of viral taxonomy over the
past half century or so will be outlined and the state the subject had reached at the end of
the Fifth International Congress for Virology in Strasbourg, 1981, will be summarized.
The historical development can usefully be divided into four periods as follows:
1. The period up to 1961. This period was characterized by premature efforts on the part
of individual virologists to establish their particular scheme, accompanied by slow-
moving and largely ineffective international cooperation.
2. 1962-1966. In this period important events took place which led up to the meetings
held during the International Congress for Microbiology in Moscow in 1966, and to
the establishment of the International Committee on Nomenclature of Viruses (I.C.N.V.).
3. 1966-1970. The first period of I.C.N.V., under the 4-year presidency of Wildy, was
a critical one. The policy decisions made and the taxonomic work carried out laid the
foundations for further development of a universal taxonomy of viruses based on
international and interdisciplinary cooperation.
4. 1971- 198 1. This period was mainly one of development and consolidation.
11. THE PERIOD UP TO 196 1
From the very beginnings of virology, names have been given to viruses as they were
discovered and described. For viruses infecting animals and plants most of these names were
trivial or vernacular, and commonly included an important host or an important disease
symptom as part of the name. Bacterial viruses were commonly given code symbols such
as T1 or C16 sometimes in a quite haphazard fashion. However, some workers in this period
provided their viruses with more high-sounding names. For example d'Herelle' applied the
name Bacteriophagum intestinale to a culture of a bacterial virus (or viruses) which he
studied, but names such as this were seldom of any lasting significance.
As far as virus classification was concerned in this period, the custom developed of
grouping viruses according to the kind of host-animal, plant, or bacterial. The reasons for
this were mainly historical and practical. Most virologists worked with viruses replicating
(or thought to replicate) in only one kind of host. Doubts concerning this system arose in
the 1940s when it became apparent that some plant viruses could replicate in their insect
vectors. During the period up to 1961 attempts were made both by individuals and by
organizations to introduce more detailed systems of classification and nomenclature. I will
deal first with efforts made by individual virologists. I can find no record of any phage
worker attempting a comprehensive classification of bacterial viruses in this period.
A. Individual Plant Virologists
Johnson2 made the first approach to the problem of classifying plant viruses. He was well
aware of the problem. He wrote: "A system of nomenclature for plant viruses is greatly
needed. The present system of applying names on the basis of host attacked or symptoms
exhibited is quite inadequate for present needs." He confined his attention to a set of I l
viruses affecting tobacco and other solanaceous hosts. The separation and classification of
the viruses described was based on the symptoms (if any) produced on 10 or more different
host species, their longevity in vitro, thermal death points, lethal effects of chemicals, and
such properties as relative infectivity and length of incubation period. He suggested that
properties of the virus in vitro would be more reliable criteria than disease symptoms. He
named the viruses with the English name of the host followed by a number, e.g., Tobacco
virus 1, Tobacco virus 2, etc.
Using the same naming system, Johnson and Hoggan' compiled a descriptive key based
on five characters - modes of transmission, natural or differential hosts, longevity in vitro,
thermal death point, and distinctive or specific symptoms. About 50 viruses were identified
and placed in groups.
Smith4 outlined a scheme in which the known viruses or virus diseases were divided into
51 groups. Viruses were named and grouped according to the generic name of the host in
which they were first found. Successive members in a group were given a number. For
example, tobacco mosaic virus was Nicotiana virus 1, and there were 15 viruses in the
Nicotiana virus group. Viruses that were quite unrelated in their basic properties were given
names that might have been thought to imply that they were related. Although Smith's list
served for a time as a useful catalogue of the known plant viruses, it wzs not a classification.
Holmes' published a classification of plant viruses based primarily on host reactions and
methods of transmission. He used a Latin binomial-trinomial system of naming. For example
tobacco mosaic virus became Marmor tabaci, Holmes. His classification was based on
diseases rather than the viruses. The viruses were split into 10 families. The family Mar-
moraceae (the Mosaic group) had a single genus Marmor which included 53 of the 89
viruses considered as species by Holmes. This genus contained viruses known even at the
time to differ widely in their properties (e.g., tobacco mosaic and tomato bushy stunt viruses).
Nevertheless, the Latin binomial system appealed to a number of workers and various
modified schemes were put forward.6-'' The Holmes system received the blessing of the
Nomenclature Committee of the American Phytopathological Society. IZ Subsequently Holmes"
put forward a revised scheme which was published as a supplement in the sixth edition of
Bergey's Manual of Determinative Bacteriology, which covered all viruses. This version
still contained many groupings that were even then obviously inappropriate. These are
discussed further below in relation to animal viruses. Hansen14-lhw as the most recent and
probably the last individual plant virologist to propose a system for nomenclature and
classification. His system for deriving generic names was based on characters of the virus
particle, the diseases caused, and the methods of transmission. His system of pseudo-
Latinized names would have provided the generic names for a Latinized binomial system.
While the Holmes and similar systems received some support from plant virologists
particularly in the U.S., in the main they were ignored. Bawden17 was a leading critic of
the use of disease symptoms in classification. He made an important contribution by sug-
gesting that any permanent classification must be based on the peculiarities of the viruses
themselves and not on those of the host plants. He emphasized the importance of serological
relationships. He pointed out the widespread existence of virus strains which although closely
related on both the physical and chemical properties of the particle and serologically, may
cause markedly different diseases. He stated, "it would seem as reasonable to expect to
classify flowering plants because of their reactions to a number of viruses as it is to classify
viruses by the symptoms they produce in a given number of hosts."
Bawden" and Valleau2' made the useful, but unheeded suggestion that while well-studied
viruses might be usefully classified, little-studied entities should be placed aside in a category
equivalent to the Fungi Imperfecti. Nevertheless Bawden's published comments and criti-