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Viruses Are Ancient Parasites That Have Influenced the Evolution of Contemporary and Archaic Forms of Life

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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 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 © 2010 , 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 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. 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 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 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
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