Origin and evolution of viruses

530 Pages·2008·7.287 MB·English

by  Esteban Domingo, Colin R. Parrish, John J. Holland

Contributors
Raul Andino A. Bosch
Department of Microbiology and Enteric Virus Laboratory, Department of
Immunology, University of California, Microbiology, University of Barcelona, UB
Mission Bay, Genentech Hall, 600 16th Street, Barcelona, Spain
Suite S572E, Box 2280, San Francisco, CA
94143-2280, USA
J.J. Bull
Section of Integrative Biology, Institute
Jamie J. Arnold for Cellular and Molecular Biology,
Department of Biochemistry and Molecular Center for Computational Biology and
Biology, The Pennsylvania State University, Bioinformatics, University of Texas, 1
201 Althouse Laboratory, University Park, University Station c0930, Austin,
PA 16802, USA TX 78712, USA
John W. Barrett M. Buti
Biotherapeutics Research Group, Robarts Liver Unit, Hospital Universitari,
Research Institute, London, ON N6G, Vall d’ Hebron, Barcelona, Spain
Canada
Craig E. Cameron
Hans-Ulrich Bernard Department of Biochemistry and Molecular
Department of Molecular Biology and Biology, The Pennsylvania State University,
Biochemsitry, University of California, Irvine, 201 Althouse Laboratory, University Park, PA
Sprague Hall, Irvine, CA 92697, USA 16802, USA
Christof K. Biebricher José-Antonio Daròs
Max-Planck Institute for Biophysical Instituto de Biología Molecular y Celular de
Chemistry D-37070, Gottingen, Plantas (CSIC-UPV), Campus UPV, 46022
Germany Valencia, Spain
Sebastian Bonhoeffer Andrew J. Davison
Institute of Integrative Biology, ETH Zürich, MRC Virology Unit, Institute of Virology,
ETH Zentrum, CHN K12.1, Universitaetsstr. University of Glasgow, Church Street,
16, CH-8092 Zurich, Switzerland Glasgow G11 5JR, UK
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viii
CONTRIBUTORS
Aidan Dolan Derek Gatherer
MRC Virology Unit, Institute of Virology, MRC Virology Unit, Institute of Virology,
University of Glasgow, Church Street, University of Glasgow, Church Street,
Glasgow G11 5JR, UK Glasgow G11 5JR, UK
Esteban Domingo Adrian Gibbs
Centro de Biología Molecular 7 Hutt Street, Yarralumla, ACT 2600,
“ Severo Ochoa ” (CSIC-UAM), Universidad Australia
Autónoma de Madrid, Cantoblanco, 28049
Madrid, Spain Mark Gibbs
and Centro de Investigación Biomedica en School of Botany and Zoology, Faculty of
Red de Enfermedades Hepáticas y Digestivas Science, Australian National University,
(CIBERehd) Canberra, A.C.T. 0200, Australia
Núria Duran-Vila Warner C. Greene
Institut Valenciano de Investigaciones Gladstone Institute of Virology and
Agrarias (IVIA), 46113 Moncada, Valencia, Immunology, 1650 Owens Street, San
Spain Francisco, CA 94158, USA
Santiago F. Elena Kathryn A. Hanley
Instituto de Biología Molecular y Celular Department of Biology, New Mexico State
de Plantas (CSIC-UPV), Campus UPV, CPI, University, Las Cruces, NM 88003, USA
46022 Valencia, Spain
Roger W. Hendrix
Cristina Escarmís Department of Biological Sciences and
Centro de Biología Molecular Pittsburgh Bacteriophage Institute,
“ Severo Ochoa ” (CSIC-UAM), Universidad University of Pittsburgh, Pittsburgh,
Autónoma de Madrid, Cantoblanco, 28049 PA 15260, USA
Madrid, Spain
Mónica Herrera
J.I. Esteban Centro de Biología Molecular “ Severo
Liver Unit, Department of Medicine, Hospital Ochoa ” (CSIC-UAM), Universidad
Universitari Vall d’ Hebron, Pg Vall D ’ Autónoma de Madrid, Cantoblanco,
Hebron 119–129, 08035 Barcelona, Spain 28049 Madrid, Spain
and Centro de Investigación Biomedica en
Red de Enfermedades Hepáticas y Digestiuas Karin Hoelzer
(CIBERehd) Baker Institute for Animal Health,
Department of Microbiology and
Richard Flores Immunology, College of Veterinary
Instituto de Biología Molecular y Celular Medicine, Cornell University, Ithaca,
de Plantas (CSIC-UPV), Campus UPV, CPI, NY 14853, USA
46022 Valencia, Spain
John J. Holland
Fernando García-Arenal Division of Biology and Institute for
Centro de Biotecnologia y Genómica de Molecular Genetics, University of California
Plantas, E.T.S.I. Agrónomos, Universidad at San Diego, 9500 Gilman Drive, La Jolla,
Politécnica de Madrid, 28040 Madrid, Spain California 92093-0116, USA
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ix
CONTRIBUTORS
Edward C. Holmes Colin R. Parrish
Center for Infectious Disease Dynamics, Baker Institute for Animal Health,
Department of Biology, The Pennsylvania Department of Microbiology and
State University, University Park, PA Immunology, College of Veterinary Medicine,
16802, USA Cornell University, Ithaca, NY 14853, USA
R. Jardí Celia Perales
Biochemistry Department, Hospital Centro de Biología Molecular “ Severo
Universitari Vall d’ Hebron, Barcelona, Spain Ochoa ” (CSIC-UAM), Universidad Autónoma
and Centro de Investigación Biomedica en de Madrid, Cantoblanco, 28049 Madrid, Spain
Red de Enfermedades Hepáticas y Digestivas and Centro de Investigación Biomedica en
(CIBERehd) Red de Enfermedades Hepáticas y Digestivas
(CIBERehd)
M. Martell
Liver Unit, Hospital Universitari, Vall d’
J. Quer
Hebron, Barcelona, Spain
Liver Unit, Department of Medicine, Hospital
Universitari Vall d’ Hebron, Barcelona, Spain
Grant McFadden
and Centro de Investigación Biomedica en
Department of Molecular Genetics and
Red de Enfermedades Hepáticas y Digestivas
Microbiology, College of Medicine,
(CIBERehd)
University of Florida, 1600 SW Archer Road,
ARB Rm R4-295, POB 100266, Gainesville,
F. Rodriguez
FL 32610, USA
Biochemistry Department, Hospital
Universitari Vall d’ Hebron, Barcelona, Spain
Duncan J. McGeoch
and Centro de Investigación Biomedica en
MRC Virology Unit, Institute of Virology,
Red de Enfermedades Hepáticas y Digestivas
University of Glasgow, Church Street,
(CIBERehd)
Glasgow G11 5JR, UK
Marilyn J. Roossinck
Luis Menéndez-Arias
The Samuel Roberts Noble Foundation, Plant
Centro de Biología Molecular “ Severo
Biology Division, 2510 Sam Noble Parkway,
Ochoa ” (CSIC-UAM), Universidad
P.O. Box 2180, Ardmore, OK 73402, USA
Autónoma de Madrid, Cantoblanco,
28049 Madrid, Spain
R. Sannjuán
Institut Cavanilles de Biodiversitat i Biologia
Viktor Müller
Evolutiva, Universitat de València, Valencia,
Institute of Biology, Eötvös Loránd University,
Spain
Pázmány P.s. 1/C, 1117 Budapest, Hungary
Isabel S. Novella Mario L. Santiago
Department of Medical Microbiology and Gladstone Institute of Virology and
Immunology, University of Toledo, College of Immunology, 1650 Owens Street,
Medicine, Toledo 43614, Spain San Francisco, CA 94158, USA
Kazusato Ohshima Peter Schuster
Laboratory of Plant Virology, Faculty of Institute of Theoretical Chemistry, University
Agriculture, Saga University, 1-banchi, of Vienna, Währingstrasse 17, A-1090 Vienna,
Honjo-machi, Saga 840-8502, Japan Austria
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CONTRIBUTORS
Edgar E. Sevilla-Reyes Luis P. Villareal
MRC Virology Unit, Institute of Virology, Center for Virus Research, Irvine Research
University of Glasgow, Church Street, Unit on Animal Viruses, Department of
Glasgow G11 5JR, UK Molecular Biology and Biochemistry,
University of California, Irvine, 2332
McGaugh Hall, Irvine, CA 92697, USA
Eric Smidansky
Department of Biochemistry and Molecular
Simon Wain-Hobson
Biology, The Pennsylvania State University,
Pasteur Institute, 28 rue du Dr. Roux, 75724
201 Althouse Laboratory, University Park,
Paris Cedex 15, France
PA 16802, USA
Scott C. Weaver
Peter F. Stadler
Center for Tropical Diseases and Department
Bioinformatics Group, Department of
of Pathology, University of Texas
Computer Science and Interdisciplinary
Medical Branch, 301 University Boulevard,
Center of Bioinformatics, University of
Galveston, TX 77555-0609, USA
Leipzig, Härtelstrasse 16–18, D-04107
Leipzig, Germany
C.O. Wilke
Section of Integrative Biology, Institute for
Ronald Van Rij Cellular and Molecular Biology, Center for
Hubrecht Institute, Uppsalalaan 8, 3584 CT Computational Biology and Bioinformatics,
Utrecht, The Netherlands University of Texas, Austin,TX 78712, USA
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Preface to the Second
Edition
A second, updated edition of a scientifi c book individual viral populations consist of clouds
is a good sign that the fi rst edition was well of related variants rather than defi ned genomic
accepted, and that the book contents respond nucleotide sequences in the classical sense. This
to the demands of a dynamic fi eld of activity. is carefully explored in the book from the view-
The second edition of O rigin and Evolution of points of biochemistry and of evolution. It will
Viruses tries to refl ect, as the fi rst edition did, not escape the reader that the extreme dynam-
the different molecular strategies that viruses ics of viral populations, with all its implications
use to evolve within and between hosts, and for virus evolution and pathogenesis, repre-
to provide a view of the complexities of short- sents a translation into virology of the quasi-
term and long-term evolution, with their species concept, proposed initially by Manfred
implications for viral disease. To this aim, the Eigen in an infl uential paper published 36
book includes several chapters related to gen- years ago. Quasispecies theory was further
eral concepts and tools for the study of virus developed by several of Eigen’ s colleagues, and
diversity, evolution, and pathogenesis, and some of them have contributed chapters to the
a number of chapters covering specifi c viral book. Quasispecies has represented the intro-
systems including animal, plant, and bacterial duction of concepts of complexity to virology.
viruses. We have broadened the scope of the The editors wish to highlight the relevance of
fi rst edition by including new subjects such quasispecies theory for virology, and gratefully
as phylogenetic analysis of viral genomes, the dedicate this volume to Manfred Eigen on the
enzymological bases of error-prone replica- occasion of his 80th birthday.
tion, RNA interference, and cellular functions Such a diversity of topics and viral sys-
involved in hypermutagenesis. We have main- tems would not have been possible without
tained and expanded the chapters needed to the commitment and hard work of the many
provide a historical view of how viruses might authors to whom we are deeply indebted. Our
have originated, with updated accounts of the thanks go also to Elsevier, in particular to Lisa
primitive RNA world, quasispecies dynamics, Tickner and Maureen Twaig, fi rst for taking
and how virus evolution relates to the general the initiative to propose a second edition of the
evolution of our biosphere. We hope that the book, and, second, for their careful involve-
reader will fi nd the series of chapters to be both ment in the various matters that require atten-
informative and a stimulus for further research. tion before a book can be printed.
It is now well established, and it becomes
even more transparent upon reading the book,
that the diversity of viruses, and their popula- Esteban Domingo, Colin Parrish, John Holland
tion numbers are astonishing. On top of this,
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xii
PREFACE TO THE SECOND EDITION
‘ Theory cannot remove complexity, but it
shows what kind of “ regular ” behavior can
be expected and what experiments have to be
done to get a grasp on the irregularities. ’
Manfred Eigen
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Preface to the First Edition

Viruses differ greatly in their molecular genomes. Among the retroelements, retrovi-
strategies of adaptation to the organisms ruses are transmitted as RNA-containing par-
they infect. RNA viruses utilize continu- ticles, prior to intracellular copying of their
ous genetic change as they explore sequence RNA genomes into DNA, which can be sta-
space to improve their fi tness, and thereby to bly maintained as an insert into the DNA of
adapt to the changing environment of their their hosts. The book discusses retroid agents
hosts. Variation is intimately linked to their and retroviruses, with emphasis on human
disease-causing potential. Paramount to the immunodefi ciency virus, the most thoroughly
understanding of RNA viruses is the concept scrutinized retrovirus of all. Experiments
of quasispecies, fi rst developed to describe and modeling meet to try to understand how
the early replicons thought to be components variation and adaption of this dreaded patho-
of a primitive RNA world devoid of DNA or gen lead to a collapse of the human immune
proteins. The fi rst chapter of the book deal system.
with theoretical concepts of self-organization, DNA viruses are likely to have coevolved
RNA-mediated catalysis and the adaptive with their hosts while the DNA world was
exploration of sequence space by RNA repli- developing. The last chapters of the book deal
cons. Likely descendants of the RNA world with the interplay between host evolution and
that we can study today are the plant-infecting DNA virus evolution, including chapters on
viroids, and the (cid:2) agent (hepatitis D), a unique the simplest and the most complex of the DNA
RNA genome associated with some cases of viral genomes known. This broad coverage of
hepatitis B infection. (cid:2) provides an example of topics would not have been possible without
a simple, bifunctional molecule that contains the contributions of many experts. We express
a viroid-like replication domain, and a mini- our most sincere gratitude to all of these
mal protein-coding domain. It may be a relic authors for having joined in the effort. The
of the type of recombinant molecules that may strong interdisciplinary fl avor of the book is
have participated in the transition to the DNA due to their different points of view. We expect
world from the RNA world. The impact of the book to take the reader on a long journey
genetic variability of pathogenic RNA viruses (in time and in concepts) from the primitive
is addressed in several chapters that cover and basic to the modern and complex.
specifi c viruses of animals and plants. While this book was in press, Professor
Retroid agents probably had an essen- Eladio Viñuela passed away on March 9, 1999.
tial role in early evolution. Not only are they Eladio was an outstanding scientist, a pioneer
widely distributed and capable of copying of Virology in Spain, and a friend. The editors
RNA into DNA, but they may also have pro- dedicate this volume to his memory.
vided regulatory elements, and promoted
genetic modifi cations for adaptation of DNA E. Domingo, R.G. Webster, J.J. Holland
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C H A P T E R
1
Early Replicons: Origin and Evolution*
Peter Schuster and Peter F. Stadler
ABSTRACT where plus–minus ( (cid:2) ) duplex formation is
avoided by the action of an RNA replicase.
RNA and protein molecules have been found Error propagation to forthcoming genera-
to be both templates for replication and spe- tions is analyzed in the absence of selective
cifi c catalysts for biochemical reactions. RNA by neutral mutants as well as for predefi ned
molecules, although very diffi cult to obtain degrees of neutrality. The concept of an error
via plausible synthetic pathways under threshold for suffi ciently precise replication
prebiotic conditions, are the only candidates and survival of populations derived from
for early replicons. Only they are obligatory the theory of molecular quasispecies is dis-
templates for replication, which can conserve cussed. Computer simulations are used to
mutations and propagate them to forthcom- model the interplay between adaptive evolu-
ing generations. RNA-based catalysts, called tion and random drift. A model of evolution
ribozymes, act with high effi ciency and spe- is proposed that allows for explicit handling
cifi city for all classes of reactions involved in of phenotypes.
the interconversion of RNA molecules such as
cleavage and template-assisted ligation. The
idea of an RNA world was conceived for a WHAT IS A REPLICON?
plausible prebiotic scenario of RNA molecules
operating upon each other and constituting Biology, and evolution in particular, are based
thereby a functional molecular organization. on reproduction or multiplication and on vari-
A theoretical account of molecular replication ation. Reproduction pure has the property of
making precise the conditions under which self-enhancement and leads to exponential
one observes parabolic, exponential, or hyper- growth. Self-enhancement in chemical reactions
bolic growth is presented. Exponential growth under isothermal conditions is tantamount to
is observed in a protein-assisted RNA world autocatalysis that, in its simplest form, corre-
sponds to a reaction mechanism of the kind:
*Dedicated to Manfred Eigen, the pioneer of molec-
ular evolution and intellectual father of quasispe- A(cid:3)Y ⎯⎯k ⎯→ 2Y, (1)
cies theory, on the occasion of his 80th birthday.
Origin and Evolution of Viruses Copyright © 2008 Elsevier Ltd
ISBN 978-0-12-374153-0 1 All rights of reproduction in any form reserved.
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2
P. SCHUSTER AND P.F. STADLER
where A is the substrate and Y the autocata- In the (improbable) case that Y (cid:4) is the only
lyst. Being just an autocatalyst is certainly not mutant of Y , the two channel frequencies add
enough for playing a role at the origin of life up to unity: Q (cid:3) Q (cid:4) (cid:6) 1. In general, there will
or in evolution. An additional c onditio sine be many mutations, Y (cid:2) Y , that give rise to
j i
qua non is the property to act as an encoded variants and conservation of probabilities
instruction for the reproduction process. It then leads to the conservation relation:
is useful to remain rather vague as far as
the nature of this instruction is concerned,
n
because there are many possible solutions ∑Q (cid:6)1 (cid:7) j(cid:6)1,…n, (4)
ij
for template action at the molecular level. In i(cid:6)1
reality the most straightforward candidates
for useful templates are heteropolymers built which expresses that a copy is either error free
from a few classes of monomers with specifi c or contains errors.
interactions. The proper physical basis for It is useful further to distinguish two classes
such interactions are charge patterns, patterns of replicons: (i) obligatory replicons and (ii)
of hydrogen bonds, space-fi lling hydrophobic optional replicons. All error copies of obliga-
interactions, and others. We may summarize tory replicons can be replicated and thus are
the fi rst paragraph by saying: “ A replicon is replicons themselves. Examples of obligatory
an entity that carries the instruction for its replicons are nucleic acid molecules under
own replication in some encoded form. ” suitable conditions (F igure 1.1 ). In Nature
Precise asexual reproduction gives rise to practically no restrictions on the initiation and
perfect inheritance. This is essentially true chain propagation of replication are known
for prokaryotes: bacteria, archaebacteria, and apart from recognition sites at replication ori-
viruses. In sexually reproducing eukaryotes, gins and a few other general requirements for
recombination introduces variation already into replication. An example of a laboratory system
the error-free reproduction process. 1 Mutation is the polymerase chain reaction (PCR), which
in the form of unprecise or error-prone repro- allows for amplifi cation of DNA templates
duction represents the universal kind of varia- with (almost) any sequence. Optional repli-
tion, which occurs in all organisms and can be cons are, for example, autocatalytically grow-
sketched by a single overall reaction step: ing oligonucleotides (v on Kiedrowski, 1986 )
and oligopeptides (L ee et al. , 1996) ( F igure 1.2 ).
A(cid:3)Y ⎯⎯k(cid:4)⎯→ Y(cid:3)Y(cid:4). (2) These oligomers lose their capability to act as

template (almost always) when a particular
Here, the mutant is denoted by Y (cid:4) . The rate nucleotide or amino acid residue is exchanged
parameters k and k (cid:4) refer to two parallel reac- for any other one. In other words, the property
tion channels. This can be indicated by replac- to be a replicon is not common feature of the
ing the two parameters with a single rate entire class of molecules but a specifi c prop-
constant and reaction (channel) frequencies: erty of certain selected molecules only.
Simple replicons certainly lack the complex-
k (cid:2) f (cid:5)Q and
k(cid:4)(cid:2) f (cid:5)Q(cid:4). (3) ity of present-day organisms and are defi ned
best as molecular entities that are capable of
replication by means of some mechanism
based on interaction with a template. Almost
1 Sexual reproduction introduces obligatory
all known replicons are oligomers or polymers
recombination into the mechanism of inheritance.
composed from a few classes of monomers.
Recombination in eukaryotes occurs during meio-
Two extreme types of replicons are distin-
sis and is a highly complex process. In this chap-
ter we are discussing primitive replication systems guished: o bligatory replicons , for which exchange
only and therefore we can dispense with any of individual monomeric units yields other rep-
detailed discussion of recombination. licons with different monomer sequences, and
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