Viruses Are Ancient Parasites that Have Influenced the Evolution of Contemporary and Archaic ...

106 Pages·2010·5.91 MB·English

by  Matti Jalasvuori

JYVÄSKYLÄ STUDIES IN BIOLOGICAL AND ENVIRONMENTAL SCIENCE
213
Matti Jalasvuori
Viruses Are Ancient Parasites that
Have Influenced the Evolution
of Contemporary and Archaic
Forms of Life
JYVÄSKYLÄ STUDIES IN BIOLOGICAL AND ENVIRONMENTAL SCIENCE 213
Matti Jalasvuori
Viruses Are Ancient Parasites
that Have Influenced the Evolution
of Contemporary and Archaic Forms of Life
Esitetään Jyväskylän yliopiston matemaattis-luonnontieteellisen tiedekunnan suostumuksella
julkisesti tarkastettavaksi yliopiston Ylistönrinteellä, salissa YAA303
syyskuun 24. 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 September 24, 2010 at 12 o'clock noon.
UNIVERSITY OF JYVÄSKYLÄ
JYVÄSKYLÄ 2010
Viruses Are Ancient Parasites
that Have Influenced the Evolution
of Contemporary and Archaic Forms of Life
JYVÄSKYLÄ STUDIES IN BIOLOGICAL AND ENVIRONMENTAL SCIENCE 213
Matti Jalasvuori
Viruses Are Ancient Parasites
that Have Influenced the Evolution
of Contemporary and Archaic Forms of Life
UNIVERSITY OF JYVÄSKYLÄ
JYVÄSKYLÄ 2010
Editor
Varpu Marjomäki
Department of Biological and Environmental Science, University of Jyväskylä
Pekka Olsbo, Sini Rainivaara
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
URN:ISBN:978-951-39-4035-5
ISBN 978-951-39-4035-5 (PDF)
ISBN 978-951-39-3996-0 (nid.)
ISSN 1456-9701
Copyright © 2 0 1 0 , by University of Jyväskylä
Jyväskylä University Printing House, Jyväskylä 2010
Ymmärrän aineen synnyn, sen hitaan kiertokulun
alkuräjähdyksestä tähtiin ja eläviin olentoihin, mutta siinä
ei ole kaikki. Aina välillä on hyvä polvistua vesirajaan ja
katsella merta sekä tähtiä, outoja ajatuksia mielessään
liikutellen. Ei kannata uskoa mihinkään, mikä ei ole totta,
mutta ei pidä myöskään olla tunteita vailla oleva
yksinkertainen kone, jonka elämän täyttämiseen riittää
pelkkä tosiasioiden, havaintojen ja mittausten loputon
jono. Välillä on hyvä ottaa kosketusta johonkin, mikä ei
oikein tahdo mahtua ihmisen tajuntaan.
Hiekka, aallot, tähdet. Kaikkeus.

Esko Valtaoja, Ihmeitä
(cid:2)

ABSTRACT

Jalasvuori, Matti
Viruses are ancient parasites that have influenced the evolution of
contemporary and archaic forms of life
Jyväskylä: University of Jyväskylä, 2010, 94 p.
(Jyväskylä Studies in Biological and Environmental Science
ISSN 1456-9701; 213)
ISBN 978-951-39-3996-0
Yhteenveto: Virukset ovat muinaisia loisia, jotka ovat vaikuttaneet nykyisten ja
varhaisten elämänmuotojen kehitykseen
Diss.

Even the simplest bacterial cell is a very complex organism that could not have
emerged spontaneously within the lifetime of the Universe. Therefore the first
cells were already products of evolution. However, very little is known of this
primordial evolutionary process that produced the cellular organisms.
Interestingly, viruses appear to have emerged before the first bacterial and
archaeal cells and thus the process seem to have generated also viruses along
with the cells. In this thesis a new lineage of ancient viruses (infecting solely
thermophilic bacteria and halophilic archaea) was discovered. This lineage is
evolutionarily related to a previously studied lineage of double-beta barrel
viruses and therefore these icosahedral, inner membrane containing viruses
probably separated into two lineages already before the emergence of the last
universal common ancestor of cells. In order to study the possible processes
that could have generated first viral genes within a primordial community of
simple (RNA-based) replicators, a rule-based computing system was developed.
Computational simulations suggested that the first viral-genes may have served
as an information sharing mechanism between proto-cells. Possibly the modern
viruses emerged from these proto-viruses while the cells evolved into more
complex entities. Viruses could also have been the driving force in the isolation
of the proto-cells from the primordial community since the isolation would
have made the emerging cells less likely to be infected with viruses. In order to
test this hypothesis, the effect of genetic isolation was studied with modern
bacteria under bacteriophage selection. Bacteriophages, which exploit the gene-
transfer apparatus of bacteria for recognizing the host cell, rapidly decreased
the percentage of bacteria that are able to exchange genetic material with other
cells. This suggests that similar isolation might indeed have occurred also on
primordial conditions due to viral selection.

Keywords: viruses; plasmids; origin of cells; bacteriophages; astrobiology;
Bacteria; Archaea.

Matti Jalasvuori, University of Jyväskylä, Department of Biological and Environmental
Science, P.O. Box 35, FI-40014 University of Jyväskylä, Finland.
(cid:2)

Author’s address Matti Jalasvuori
Department of Biological and Environmental Science
P.O. Box 35
40014 University of Jyväskylä, Finland
[email protected]

Supervisor Professor Jaana Bamford
Department of Biological and Environmental Science
P.O. Box 35
40014 University of Jyväskylä, Finland

Reviewers Docent Janne Ravantti
Department of Biosciences
Division of Genetics
P.O. Box 56, 00014 University of Helsinki, Finland

Docent Kirsi Lehto
Unit of Plant Physiology and Molecular Biology
20014 University of Turku, Finland

Opponent Professor Rob Lavigne
Laboratory of Gene Technology
Katholieke Universiteit Leuven
Leuven B-3001, Belgium
(cid:2)

CONTENTS

ABSTRACT
CONTENTS
LIST OF ORIGINAL PUBLICATIONS
ABBREVIATIONS

1 INTRODUCTION ............................................................................................... 11
1.1 An overview to prokaryotes: Bacteria and Archaea ............................. 12
1.2 Horizontal gene transfer ........................................................................... 14
1.3 Conjugative plasmids ................................................................................ 15
1.4 Prokaryotic viruses and viral life strategies ........................................... 16
1.4.1 Virus classification ........................................................................... 18
1.4.2 Bacteriophages - Caudovirales ......................................................... 20
1.4.3 Bacteriophages - Tectivirales ............................................................ 21
1.4.4 Other icosahedral bacteriophages with membranes ................... 26
1.4.5 Archaeal viruses and their unique morphotypes ........................ 27
1.4.6 Prokaryal viruses and host evolution ........................................... 29
1.5 Origin of cells and viruses ........................................................................ 30
1.6 Early evolution of life ................................................................................ 34

2 AIMS OF THE STUDY ....................................................................................... 37

3 MATERIALS AND METHODS ........................................................................ 38

4 REVIEW OF THE RESULTS .............................................................................. 40
4.1 Genome sequence and characteristics of the Thermus phage
P23-77 (I) ..................................................................................................... 40
4.2 Genomic sequences of phage IN93 and the integrated
virus-like elements in Thermaceae and Halobactericeae (I, II) ................. 41
4.3 P23-77-like viruses and virus-like elements form a globally
distributed viral lineage spanning the domains of Bacteria and
Archaea (II) ................................................................................................. 43
4.4 Genome sequence of Bacillus anthracis phage AP50 (III) ...................... 44
4.5 Plasmid-dependent bacteriophage selects plasmid-free cells in
bacterial populations (IV) ......................................................................... 46
4.6 Bacteriophage indirectly selects less pathogenic Serratia marcescens
phenotypes (V) ........................................................................................... 47
4.7 Computational system for studying the evolution of a primordial
compartment matrix inhabited by ribozyme-like agents (VI) ............ 47

5 DISCUSSION ....................................................................................................... 48
5.1 Early emergence of inner-membrane containing icosahedral
viruses .......................................................................................................... 48
(cid:2)

5.2 A possible (recent) evolution in the capsid architecture among
Thermus infecting viruses P23-77 and IN93 ........................................... 50
5.3 Evolution of Serratia marcescens under selection of a T7-like
phage ........................................................................................................... 56
5.4 Plasmid-dependent viruses reduce horizontal gene transfer and
provide a potential tool for fighting antibiotic resistances .................. 57
5.5 Are the Diverse Crenarchaeal Viruses Survivors of the Early
Virosphere? ................................................................................................. 59
5.6 Viruses and the Early Evolution of Life ................................................. 60
5.6.1 Viruses and the evolution of proto-cells ....................................... 60
5.6.2 Decrease of virus diversity after extinction events and its
possible effect on host evolution .................................................... 61
5.6.3 Endomembrane compartments in emerging eukaryotic cells ... 63
5.7 Viruses and the Life in the Universe ....................................................... 65

6 CONCLUSIONS .................................................................................................. 69

YHTEENVETO (RÉSUMÉ IN FINNISH) .................................................................. 72
REFERENCES ................................................................................................................ 74
ORIGINAL PUBLICATIONS