You are on page 1of 17


Volume 18, Number 2, 2018 Review Article
ª Mary Ann Liebert, Inc.
DOI: 10.1089/ast.2017.1649

Viruses at Large in the Universe

Aaron J. Berliner,1 Tomohiro Mochizuki,2 and Kenneth M. Stedman3

Downloaded by Gothenburg University Library from at 01/10/18. For personal use only.

Viruses are the most abundant biological entities on modern Earth. They are highly diverse both in structure and
genomic sequence, play critical roles in evolution, strongly influence terran biogeochemistry, and are believed
to have played important roles in the origin and evolution of life. However, there is yet very little focus on
viruses in astrobiology. Viruses arguably have coexisted with cellular life-forms since the earliest stages of life,
may have been directly involved therein, and have profoundly influenced cellular evolution. Viruses are the
only entities on modern Earth to use either RNA or DNA in both single- and double-stranded forms for their
genetic material and thus may provide a model for the putative RNA-protein world. With this review, we hope
to inspire integration of virus research into astrobiology and also point out pressing unanswered questions in
astrovirology, particularly regarding the detection of virus biosignatures and whether viruses could be spread
extraterrestrially. We present basic virology principles, an inclusive definition of viruses, review current vi-
rology research pertinent to astrobiology, and propose ideas for future astrovirology research foci. Key Words:
Astrobiology—Virology—Biosignatures—Origin of life—Roadmap. Astrobiology 18, xxx–xxx.

1.1. Where Are Viruses in Astrobiology? ger communication across disciplinary boundaries. Table 1
describes these goals and subgoals in relationship to how vi-

W e consider viruses to be central to multiple aspects of
astrobiology, but in the current NASA Astrobiology
Strategy (Hays et al., 2015), viruses are mentioned only six
rology can be considered an integral component of astrobiology.

1.3. The Central Role of Viruses in Astrobiology
times in over 250 pages. The European AstRoMap is slightly
The extracellular form of viruses, virions, are the most
more inclusive, with nine mentions of viral elements (two of
abundant biological particles on Earth, with an estimated
them parenthetical) in 42 pages but none of viruses (Horneck
1031 virions in the oceans alone (Suttle, 2005). Whether this
et al., 2016). Perhaps the astrobiology community is not yet
amazing virion abundance is true in extraterrestrial oceans
fully aware of the amazing ubiquity, diversity, and roles of
or was true in primordial Earth oceans are open questions.
viruses in biogeochemistry, evolution, and the origins of life.
Unfortunately, the lack of validated virus biosignatures makes
Therefore, we provide an annotated version of the NASA
detection of extraterrestrial or ancient viruses challenging.
Astrobiology Strategy Goals with a focus on viruses and
Virus infections profoundly influence both global and local
emphasize their critical and underappreciated roles in astro-
biogeochemical cycling (Suttle, 2009) yet have not been in-
biology. By way of background we also provide an overview
cluded in ancient climate models or models for extraterrestrial
of viruses and their replication, while focusing on aspects
climates. Viruses are critical drivers of current evolution
most relevant to astrobiology.
(Enard et al., 2016) and were probably extremely impor-
tant for the early evolution of life on Earth (Koonin et al.,
1.2. An Astrovirology Strategy
2006). These roles of viruses in astrobiology are described
The 2015 NASA Astrobiology Strategy provides a list of in more detail in Section 3. For readers who are less fa-
goals for the astrobiology community which aim to improve miliar with viruses and virus replication cycles, we de-
research products on the origins, evolution, and future of life scribe the history of astrovirology, virus replication, virion
on Earth and beyond, while also aiming to develop stron- structures, and genomes in Section 2.

University of California, Berkeley, California, USA.
Earth Life Sciences Institute, Tokyo Institute of Technology, Japan.
Center for Life in Extreme Environments and Biology Department, Portland State University, Oregon, USA.


was proposed by agree on what a virus actually is. The first use of the term ‘‘astrovirology’’ to our protein shell (also known as a capsid) that packages the viral knowledge was as a session and abstract title at AbSciCon 2004 genomic nucleic acid. Nobel laureate. vivum fluidum’’ (contagious living fluid) (Beijerinck. some viruses can have a lipid-containing subheading in his 2013 essay in Astrobiology: ‘‘The Quest for outer layer.liebertpub. however. and first director of the NASA The standard definition of viruses for many decades there- Astrobiology Institute (NAI). scientists and technologists.’’ Later. Dale W. A more inclu- extraterrestrial life’’ (Griffin.  Coordinate field/mission observations. and life. through a filter that retains all known bacteria ‘‘contagium biology was the late Baruch Blumberg. Science climate. Inspire Future  Enhance the interest in science and  Increase interest in science and technology by Generations technology to the benefit of our society. 2. and reprogram that cell to produce more virus. Downloaded by Gothenburg University Library from online. which can be composed of DNA or ( at 01/10/18. that we prefer. Enhance NASA’s  Research analog environments to  Develop broader proxies for viruses as indirect Missions understand processes underlying evidence of life in analog environments.  Sustain the human imperative to explore  Explore the mostly unknown world (or worlds) the unknown. who made the connection at the after was ‘‘a very small disease-causing agent. called an envelope. Nobel Extraterrestrial Life: What about the Viruses?’’ We completely laureate and pioneering immunologist. ecology. as discussed below. 2013). other than ‘‘obligate Before we start ‘‘looking for viruses in our quest for intracellular’’ this definition is incomplete. (biosignatures) and environments (‘‘envirosignatures’’). of viruses. but. Table 1. is said to have called agree with his statement: ‘‘We should be looking for viruses viruses ‘‘a piece of bad news wrapped up in a protein. Enhance Societal  Act upon the public interest to understand  Increase understanding of our place in the Interest and our place in the Universe and broaden Universe through understanding our Relevance understanding of life. and evolution (Stedman and Blum. 2013).  Enhance effective communication between  Enhance communication with virologists. 1. 2004).  Enhance critical and creative thinking in  Increase benefits to society through application all fields of inquiry. Virions consist of a berg.  Constrain human exploration (minimize adverse impacts on other planetary environments). but the development of the electron microscope in the organized a number of workshops and symposia mostly focusing 1930s revealed that all viruses were found to have an inert on virus origins.  Enhance the ability of society to address  Enhance societal understanding of the roles important challenges that require of viruses on our planet.4. extracellular particle state. What Is a Virus? 2011). laboratory experimentation.  Incorporate virology perspectives to enhance critical and creative thinking. laboratory experimentation. 2005). In addition. discoverer of the hepa.  Support planetary protection efforts. Astrovirology Goals in the Framework of the 2015 NASA Astrobiology Strategy Original goal Subgoals Astrovirology subgoals Foster Interdisciplinary  Understand linkages between geology. The original virus defi. NAIViFoG. Griffin used ‘‘Astrovirology’’ as a RNA. This dis- covery led to the expansion of the standard virus definition to ‘‘a very small obligate intracellular parasite’’ (Acheson. Thereafter. very few astrobiologists have even started looking. the virion. Sir Peter Medawar. interdisciplinary approaches. The History of ‘‘Astrovirology’’ nition was practical: a disease-causing particle that passed The first to publicly connect the study of viruses and astro.1. relationships with viruses and their past and present effects on evolution and life. NAIViFoG has cles. of astrovirology technologies. change at several spatial scales. However. there Astrobiology Science Conference in 2002.  Promote collaborations between  Promote collaborations with virologists. 2 BERLINER ET AL.’’ in our quest for extraterrestrial life’’ (Griffin. and theory. to our All viruses must transfer their genome inside a host cell knowledge. Salvador Luria and coauthors: ‘‘Viruses are entities whose .  Evaluate the roles of viruses in planetary protection.  Understand the linkages between virology. habitability. climate. and life. Promote Planetary  Understand interactions between  Understand virus-environment interactions Stewardship biological activity and environmental at multiple spatial scales. NAI were debates whether they were infectious liquid or parti- formed the Virus Focus Group. we need to sive definition of viruses. including (astro)virologists. government offices and agencies.  Develop more effective proxies for life  Develop and validate virus biosignatures. and theory. For personal use only. 1898). titis B virus.  Coordinate field/mission observations. geology.

2). 2010. cal symmetry not only matches nucleic acid symmetry but sidering an acorn an oak tree or a spermatozoid a human also allows capsid protein subunits to have identical inter- (Claverie. the form visible under the electron easily by using the same proteins repeatedly. The exterior of a virion is able to mission instrumentation than a TEM. which in most cases is made up of re- peating substructures termed capsomeres. However.5 below). except at their ends (Crick and Downloaded by Gothenburg University Library from online. into three viral families. Given that virion structures are unique and distinctive. see the works of the genome size. they are capable of Darwinian evolution. Both of these 2. often found with enveloped viruses (e. There has been delivery of the viral genome into the host cell. Whether largest genomes also have icosahedral virions (Wilson et al. three-dimensional structures with repeating subunits. but if a 2009. for each amino acid) and so is relatively large. influenza connected to a linear cylindrical ‘‘tail’’ which is used to virus) (Fig. but they are not ‘‘self-sustaining’’ per se. Siphoviridae (Fig. it comes close Watson.’’ detected in an extraterrestrial sample. 1A). 2J). (3) repro- progress with scanning electron microscope (SEM) tech- gramming of the cellular machinery to produce more viri- nology for space exploration. Fischer et al. it seems unlikely that a TEM will be put on cycle consists of (1) binding of a virion to a host cell. known to cause the and together form the order Caudovirales (King et al. There has also been progress in cellular organisms generally replicate by binary fission.4. some of the viruses with the Schulz et al. Aherfi et al. They are also more adapt- characteristic of viruses (Fig.liebertpub. either one or both ends of viral genome to other cells’’ (Luria et al. For further ging them symmetrically is an optimal strategy for limiting discussion of the vital nature of viruses. 3). but. to the host cell surface. while (Edmunson et al. Heli- Considering the virion to be a virus is analogous to con. As a result. with enumerating virus-sized particles using dynamic light scat- one mother cell resulting in two progeny cells either by tering.g. While this may not be dif- Following Luria’s description. The geometrical efficiency of virus capsids to NASA’s working definition of life: ‘‘A self-sustaining is thought to be due to the fact that nucleic acid is relatively chemical system capable of Darwinian evolution. Virus refers to the whole virus rep. Viruses Are Not Just Virions: Are Viruses Alive? structures can be formed with a limited number of capsid It is important to make the distinction between a virus and protein subunits and can increase their volume relatively a virion. However. 2). the virus capsid. helical virions. Moreover. Then the process repeats. Podoviridae. The inert virion. These head-tail viruses have an icosahedral ‘‘head’’ virus). and at 01/10/18. primarily for geometrical reasons. (2) a spacecraft in the foreseeable future. one virus replication cycle can result in pore technology (Schmidt and Hawkins.3. Interestingly. symmetry are highly efficient ways of forming large-volume most people. 2016). similar to a soccer ball (e. outside the protein capsid. Viruses thus present a techniques have been applied to natural samples containing different replication mode than cellular life. Virus Replication Cycle visualize most virion morphologies. a basic virus replication ficult on Earth. Particles made of substructures arranged with icosahedral lication cycle (see Luria’s definition above). There are some virion (or a virus-like particle) were to be unequivocally notable exceptions to this geometric conservation ‘‘rule. 2016. and promising nano- division or budding. sample was from. 2016). common cold). viruses are alive or not may be a moot question. (2017) and Koonin and Dolja (2014).... the whole virus replication cycle (Fig. Forterre. a transmission electron microscope (TEM) is required. many virions have additional attach and inject the viral genome into the host bacterium . the envelope.’’ the virion. to 2. 2016). Yang and tens or hundreds of progeny virions. in the case of a form the virion and thus maintains a compact viral genome. When one considers actions with each other. limiting their use for definitive virion identification. virus inside a host cell. or helical symmetry (e. or on the surface of enveloped virions. to our knowledge. tobacco mosaic 2011).5. 1A.g. For personal use only. They are taxonomically classified Virus capsids generally have very simple elegant geome.g.. differentiated by their tail structures. Astonishing Virion Diversity in Extremophiles size from a diameter of approximately 20 nm to over 1 mm for the giant viruses. these techniques provide mini- possible reevaluation of life-detection efforts. Polyhedral and helical structures are widespread in the viral world. very few people would particularly those of the ‘‘extreme’’ viruses of Archaea (see claim that this would not be evidence for life—wherever that Section 2. ASTROVIROLOGY: VIRUSES IN THE UNIVERSE 3 genomes are elements of nucleic acid that replicate inside proteins on their surface that are used to recognize and bind living cells using the cellular synthetic machinery and caus.’’ Viruses inefficient for encoding proteins (three nucleotides required are chemical. These proteins can often be found at ing the synthesis of specialized elements that can transfer the the vertices of polyhedral virions. Therefore. This limits microscope. and (4) release of virions from the host cell to infect not have high-enough resolution to identify virion structures other cells... Another common virion structure is the pleomorphic filled with a double-stranded DNA (dsDNA) genome. In addition. mal shape information. it is tempting to use virions as biosignatures. Virus-Specific Biomarkers? to pre-sort virus-sized particles for downstream processing Luria’s ‘‘specialized element. 2010). nanoparticle tracking analysis. conflate the two. A schematic virus Yamamoto.2. 2006. as they require using one or a few gene products multiple times and arran- infection of a living cell for their replication. but currently this SEM does ons. either with polyhedral symmetry (often icosahedral). Some virions have an additional lipid Viruses of bacteria are dominated by so called head-tail layer or membrane. prompting unknown virions. including many virologists. rhinovirus. Myoviridae. Virions. these techniques could be useful 2. Virions vary in 2. structure. bacteriophages (Fig. Unfortunately. is analogous to a seed or a spore that can only the number of different capsid protein genes required to replicate in an appropriate environment. none of these replication cycle is shown in Fig. is the defining possibly including sequencing.. 1956).. 1978)..

(A) Schematic virus replication cycle. (B) The Baltimore classification of viruses by packaged nucleic acid type and route for producing RNA (Baltimore. and single stranded (ss) or double stranded (ds). For personal use only. the virus genome persists in the host cell during cellular replication. forming a provirus or prophage. group II comprises ssDNA viruses. Group I comprises dsDNA viruses. respectively. The provirus (prophage) can be induced to produce new virions. is indicated in upper ovals. Downloaded by Gothenburg University Library from online. 4 BERLINER ET AL. dsRNA viruses. Nucleic acid intermediates used to form mRNA are shown in lower ovals. at 01/10/18. group IV. which includes (+)ssRNA-RT viruses. group V. Upper left: virion inserts the viral genome into a host cell. . often entering the lytic cycle. RNA or DNA. Sometimes the viral genome is integrated into the host genome (circle). negatively stranded (-)ssRNA viruses. 1971). and group VII. In many cases (left arrows). often lysing the host cell in the process. Positive (+) strand refers to the coding sequence of the mRNA. These five groups correspond to non-retroviral viruses. the virus genome is replicated and packaged in newly formed virions. 1. The discovery of retroviruses (RT) that replicate their genomes through both DNA and RNA intermediates led to the estab- lishment of group VI. group III. In other cases (right arrows). The type of nucleic acid genome packaged in virions. Negative (-) refers to the complement of the mRNA. which includes dsDNA-RT viruses which package ssRNA or dsDNA in their virions. The integrated virus genome replicates with the cellular replication cycle.liebertpub. positively stranded (+)ssRNA viruses.

. Due . euryarchaeal halophiles (Atanasova et al. archaeal viruses have surprisingly di.. 2M). also known as ‘‘giruses’’ or Megavirales. Bath and Dyall-Smith. 2C) (Häring et al.. 2N) (Mochizuki et al. 2001. are enveloped with rounded or pleomorphic morphology 1984. infecting hosts such as Thermus grow- Rensen et al. tailed spindle-shaped has been challenged with the discovery of the so-called (Bicaudaviridae) (Häring et al.. Environments where Archaea domi- and Prangishvili. 2016).. In addition. Bize et al. 2005b. 1998). 2. 2I) (Häring et al. 2K. However. virion structures are known. (I) bottle-shaped. more specifically virions.. 2005).or spindle-shaped (Fuselloviridae) (Fig. 2B) (Martin et al. This taviridae) (Fig.. 2004). 2D) morphology. such as hot springs (Rice et al. 2B) (Arnold et al.or infects amoeba in 2003 (La Scola et al. (G) occluded. thermophilic bacteria. et al. Bamford et al.. Prangishvili.. The Mimi- spring-shaped (Spiraviridae) (Fig. virion detection method must encompass this diversity. Sphaerolipoviridae) (Fig. 2003) and neutral hot springs (Mochizuki (Fig. Most markably diverse VLPs. Mochizuki et al.. helical (Rudiviridae. Bacterial viruses are presently classi.. Even Giant Viruses Have Icosahedral Virions observed previously..or spindle-shaped. Direct TEM observation of virus-like par. 2009). 2000a.. many archaeal viruses also display morphologies that were never 2. virus has a virion and genome as large as some bacteria. (K) ovoid. deep sea hydrothermal vents (Geslin et al. 2A) or helical (Fig. 2012) and salt lakes. 1984: Wood et al. 2A) (Fig. giant viruses. Archaeal viruses with found in bacterial or eukaryal viruses. 1989. These include lemon. (C) spherical. from acidic (Martin et al. 2010. Arnold et al. such as polyhedral virions similar to the classical head-tail bacterial viruses or icosahedral (Turriviridae. 2011). Together. Caudovirales have been found in et al. 2E. bottle-shaped started with the startling discovery of the Mimivirus that (Ampullaviridae) (Fig. Clavaviridae. 2012) at 01/10/18.. droplet-shaped (Gut.... Gorlas et al. (L) allantoid. despite the much smaller number of ticles (VLPs) from soil or aquatic environmental samples isolates. such as filamentous or tailless Häring et al.. A few bacterial viruses with other nate. (F) twinned icosahedra.. Any astrovirological (Fig. ICTV-approved families—well exceeding the nine bacterial ameter) particles have the head-tail morphology (Ackermann virus families (Fig. 2004. (E) prolate ellipsoid with or without envelope (dashed line). spindle-shaped viruses (Fig.... 2003). 2011). 2M) (Pietilä et al. 2008.. or salt lakes (Sime-Ngando et al. Mochizuki et al. and isolated from both verse morphology.. 2005b). and many similar Archaea-rich environments.. viruses of the Archaea are currently classified into 15 shows that over 95% of these nano-sized (>500 nm in di. and coil. K L M N a FIG. Generalized representations of virion morphologies: (A) icosahedral. 2005a).or eukaryotic virions contain some variation of the icosahe. upon infection. 3). 2012). Some archaeal viral morphotypes are crenarchaeal and euryarchaeal hosts. 2006). (M) pleomorphic.. (N) spring. (J) head-tail. but no Lipothrixviridae. 2011) are filled with re- fied into nine taxonomic families (King et al.or coil-shaped.. 2000b). viridae) (Fig. 2J) have also been observed and isolated.liebertpub. For personal use only.. The ‘‘small’’ size of viruses.6. Prangishvili. 2010) polyhedral structures. mainly from (Rice et al. 2003. 2012). 2D) ( Janekovic et al. (D) filamentous or helical or rod-shaped. 1983. Zillig mophilic archaea. (B) lemon. The Archaea-specific lemon. (H) budded. ASTROVIROLOGY: VIRUSES IN THE UNIVERSE 5 A B C D E F G H I J Downloaded by Gothenburg University Library from online. 1993. and recently proposed members of the Caudovirales have been isolated from ther- ‘‘Tristromaviridae’’) (Fig. 2B) are frequently isolated from dral (Fig. and pleomorphic (Pleolipo. globular/spherical (Globuloviridae) ing around 60–80C (Yu et al. 2003: On the other hand.

genus. The discovery of giant viruses con. It is not clear how closely ICTV taxonomic classification reflects phylogeny.. (subfamily)... The fundamental ICTV definition of a virus species is ‘‘a polythetic class of viruses that constitute a replicating lineage and occupy a particular ecological niche where the polythetic class is one whose members have several properties in common. This virus was named Mimivirus nome (Legendre et al. family.. 6 BERLINER ET AL. 2011). FIG. Some giant viruses are parasitized by tinues. particularly given rampant recombination between genes in different viruses. 1B. including its size. and only la. yet most of these giant viruses still have icosahed. This figure represents the ICTV taxonomic grouping of viruses with viral families and subfamilies. with the recent findings of Pandoravirus with a 1 mm other viruses. viruses have been classified taxonomically since the 1970s by the International Committee on Taxonomy of Viruses (ICTV) (King et al. Virus taxonomy: In order to provide a uniform virus nomenclature. 2013). and they are grouped by their packaged nucleic acid and replication as shown in Fig. 2011).liebertpub. Downloaded by Gothenburg University Library from online. 2014).’’ for many years.5 million base pair (bp) genome and Pitho- bacterium. Mimivirus was mistakenly identified as a virion and 1. and in some cases order (King et al. Surprisingly. ‘‘mimicked’’ the Pandoravirus and the virion of the Pithovirus are larger bacteria.5 mm and a 600 thousand bp ge- ter determined to be a virus. the genome of because some of its at 01/10/18. (Philippe et al. the virophage. The ICTV classifies viruses in species. 3. For personal use only.’’ Virus species differ from the higher viral taxa. virus with a virion over 1.9–2. to its large size. The first of these to be discovered . which are universal classes defined by strict inclusion requirements. than many prokaryotic cells and even some small eukaryotes rally symmetric virions. ‘‘Bradfordococcus.

.. The techniques to be used to screen these plumes for genome type is dsDNA. some of the largest virus quences that do not have clear homologs (Edwards and Rohwer. 2003. Given the extremely large To date. A number of researchers except in closely related viruses. their genetic material.. Un. for example aminoacyl tRNA synthetases Yoshida et al. determination. For personal use only. 2013. pendent on cellular translation machinery to produce virus ophage and their relationships to capsidless transposable proteins. 2016). This is Viruses are unique in the current biosphere in that they use particularly surprising given that ACV was isolated from a either DNA or RNA in single. unlike for cellular samples... viruses are critical for structuring Earth’s derived from ancestral RNA parasitic replicators. 2017).. Without exception. 2002. (Aherfi et al. as they are at 01/10/18. known as stranded DNA (ssDNA) in some circoviruses to almost 2. 2013. es. functions can be annotated for a very few genes. based on nucleic acid content or TEM enu. unknown group (i. but the lack of corresponding reference 2013). All viruses are thus absolutely de- elements (Fischer and Hackl.7. cellular genomes are exclusively composed of dsDNA. 2008). 2004). 2017). which 2. 2.. Viruses Are Astronomically Abundant. owing to the extreme physicochemical that will screen for extraterrestrial viral particles in these conditions under which many archaea thrive.. ronmental samples in a culture-independent manner. all isolated viruses of the Archaea have DNA numbers of viral particles in Earth’s oceans. Hatfull.. marine viromes have been among the most intensively . a capsid protein gene and a protein required for omes) in many natural environments generates 60–90% of se- virus genome replication. Based on these numbers..e. 2011. Plants are known to harbor many so-called viroids. Proctor and and often far more than 50% of the putative genes can only Fuhrman. The presence of vir. 1989.8. Viruses have been found be described as ‘‘hypothetical protein’’ (Pedulla et al.. 2009). For a number of (Raoult et al. Virus ing has accelerated studies on genomic diversity of envi- genomes can range in size from less than 2000 bases of single. to our knowledge. important roles in global biogeochemical cycles. For a long time. have shown. Hurwitz and Sullivan. 2012).. alone (Rohwer. However. with a calculated 1031 virions in the oceans biosphere’’ (Filée et al. diverse. in all environments where life has been found on Earth. Brum et al. Pope et al. deep sea hydrothermal vents (Geslin et al. that in 1 mL of seawater.. 2014)... 2003) and sequences in the public database does not allow definitive the submarine mantle (Nigro et al. 2006). Prangishvili. are small structured pathogenic RNA molecules that are made Particularly in Terrestrial Oceans by cellular DNA-dependent RNA polymerase enzymes that Regardless of the debate whether or not viruses are to be do not encode capsids. 2013). 2005). turned with ssDNA archaeal viruses found in halophilic archaea particle imaging or novel microscopy techniques may be (Pleolipoviridae) (Pietilä et al. Suttle.. replicators (Koonin and Dolja. 1990. 2006). it would be very genomes often containing more than 80% of putative genes interesting to determine if there are virions in recently observed lacking homologs in the sequence databases (Snyder et al. Many viral genomes contain genes that have no homologs likely even more (Suttle. 2015). cellular genomes. and play confined to plants and depend on cellular RNA polymerases.9. searchers to make the analogy between these putative viral The latest estimation is that one bacterial cell can be infected sequences and the presence of dark matter or dark energy in by 10 viral species on average. there are from sequenced. no mission is currently planned was speculated that.. 2010).. They are extremely abundant. All cells are ex. no virus genome isolated to reasons. whereas viruses are capsid-encoding or- ganisms (Raoult and Forterre. number cellular life-forms on our planet by at least 10 fold. 2017).. The hy- perthermophilic spiravirus Aeropyrum coil-shaped virus (ACV) has the largest known genome of all ssDNA viruses. 2012).. 2008) Other virophage are date contains a ribosomal subunit protein or ribosomal RNA closely related to and may be derived from transposable gene (Schulz et al. a member of a new viral family) is meration.. but nanopore and nano. These observations have led a number of re- pected to have infectious viruses associated with them. by calling these sequences ‘‘biological dark timated total numbers of virions on planet Earth are truly matter’’ (Pedulla et al.5 metagenomics. and it fortunately. viruses were only found to contain dsDNA genomes.liebertpub. By contrast. Forterre. 2008. Virus Metagenomes for their entire replication cycle. genomes encode genes previously thought to be only present in 2005. 1–10 million viral particles (Bergh et al. Virus Genomes—The Dark Matter with 24 thousand bases. 2003. the Universe. 2016). ASTROVIROLOGY: VIRUSES IN THE UNIVERSE 7 was Sputnik (La Scola et al. 2016) and previously 2015. Simmonds et al. 2016).. example. 2003) or ‘‘the dark matter of the astronomical. where million bp of double-stranded DNA (dsDNA) in Pandoravirus 95% of sequences are similar to previously known sequences. which is more than double the size of Sequence Space of the previously largest known ssDNA genome. Current viroids are unlikely to be considered alive. 2005. However. to be of viral origin. The smallest virus genomes encode only metagenomic analysis targeting virus-sized particles (metavir- two genes. The recent development of high-throughput DNA sequenc- the hypothetical ‘‘RNA world’’ (Koonin et al. However. 2010.or double-stranded forms for host organism that grows at 90C (Mochizuki et al. this view has been over- virions are unclear at this time. leading some researchers to postulate that they are remnants of. Only in the but they could serve as models for archaic parasitic RNA last few decades have scientists realized that viruses out. When a viral genome of an Downloaded by Gothenburg University Library from online. cells are ribosome- capsidless parasitic replicators (Koonin and Dolja. 2015). archaeal observed plumes from Enceladus (Hansen et al. The vast majority of unknown viral sequence is assumed boiling acid hot springs (Rachel et al.. This ribosome dependence led to a recently suggested elements further blurs the distinction between viruses and viro-centric definition of cells and viruses. for Mochizuki et al. or direct descendants from. 2014). and in hyperthermophilic applicable to this endeavor. the Arctic sea ice (Wells and Deming. Rosario and Breitbart. the only possible plumes. encoding organisms. Prangishvili et al.. in general. Some viruses only use RNA 2.. 2005). water plumes from Europa (Sparks et al. archaea (Spiraviridae) (Mochizuki et al.

CRISPR sequences con. 2014. important for nucleotide. et al. There are a 3. Viruses Are Critical for Biogeochemical Cycles et al. and virus biogeography (Held and over. studied.. Roux et al. Roux et al. Up to 25% of fixed carbon is predicted to be recycled sequences between the repeats that are identical to parts of in the upper ocean water column due to the activity of these virus genome sequences or other mobile DNA (Koonin. Viral lysis of abun- (Wilmes et al. 2007).. 2017). the machinery On the other hand. Elena. the CRISPR/Cas9 system. virus-encoded genes are expressed. other so-called auxiliary metabolic genes (AMG). on the role of viruses in ‘‘the great oxygenation event’’ and Sometimes to the Host’s Advantage the amount of oxygen and organic matter in the ancient oceans (Holland. Interac- in their models. 2017). tions between viruses and their hosts can range from para- sitism to mutualism (e. about 5% of the oxygen on Earth is estimated to be Whitaker. for other organisms and maintain the food chain. 2006). Wichman and Brown. It is intriguing to speculate 2. Microbial ecologists are host cell or the organism. 2003. thereby not only removing nutrients from the upper However. Lindell et al.11. which that there may only be up to a million virus species (Brum could lead to the development of virus-specific isotopic bio- et al. called viral shunt (Wommack and Colwell. 2012). 2016). it has beginning to include viruses in terran biogeochemical cycle been realized that some. 2016). This process of carbon recycling is an essential component of has proved extremely useful for determining past infections global climate regulation (Suttle.. resistance to viral infection.. a previously cryptic sequence structure surrounding environment. 1999). CRISPR se. more recently. However.. 2015.. Breitbart.. particularly against a virus that kills ucts change their host’s metabolism. and we suggest that modelers of biotically with their hosts (reviewed in Roossinck. 2017). lowing hosts to adapt to new environments and changing their metabolism. phosphate. of all published viral DNA metagenomes found that nearly 70% of virus-associated genes were novel (Paez-Espino 3. sist of repeated DNA sequences with short so-called spacer 2004). inevitably emerge genomes and metagenomes (Breitbart. similar in gen. the ‘‘Red Queen hypothesis’’ of evolution (Van Valen. carbon. 2011). provides exceptionally strong evolutionary pressure. 2017). Early metavirome studies first indicated an over. that is now known to provide acquired immunity to virus in.. exoplanets and their satellites also consider including viruses Metcalf and Bordenstein. 2015).. Roossinck. However. These genes are found in viruses lication. 2016). and ammonium metabolism. For personal use only. inferring hosts for unknown viruses of cloud-nucleating chemicals (Wilson et al. 2009). 2000. exist—will also coexist with host cells on a spectrum between 2012. More- (Anderson et al. sulfur. In simulations of early life. More recent studies indicate pic fractionation that is different from cellular enzymes... cells would gradually fall to the widely used for genome engineering (Wright et al. viruses also contribute to global nutrient cycling.2. 2016). Each time a viral infection tain so-called CRISPRs (Clustered Regularly Interspersed causes cell lysis. if not most. marine viruses (Wilhelm and Suttle. A recent analysis mutualism and parasitism. 2012. cellular organic matter is released to the Palindromic Repeats). 2012. Roux et al. produced by virus-infected cells using virally encoded pho- tosynthesis genes (Suttle.. 2011. There are two major ways that viruses drive 2016.. there is also strong evolutionary pressure on the virus that infect photosynthetic cyanobacteria and not only allow the to overcome host defenses. ocean but also lowering the carbon content of the oceans. Viruses and their hosts are thus often said (Mann et al.’’ fulfilling Moreover. Sullivan et al. It would be very interesting to whelming diversity of virus sequences with possibly billions determine if these virus-encoded gene products lead to isoto- of virus species (Rohwer. 2008). them to thrive in parts of the ocean that uninfected cells cannot 2010. more importantly for astrovirology. 2. This interplay of host and viral infected cyanobacterium to undergo photosynthesis under evolution has been demonstrated both experimentally and conditions that uninfected bacteria could not but also enable theoretically (Turner and Chao. viruses coexist sym- models (Stec et al. Roossinck. 1999. 2015). Reid. reconstructing extinct viruses (Anders. Viruses Drive Evolution growing number of examples of virus infections that clearly benefit their hosts. have been reported in virus concept to what we now know as viruses. If there were no One of these systems. there are still many new groups markers. This quences also contain a record of past virus infections. in addition to al- virus world. CRISPR—A Virus Defense Mechanism Viruses are assumed to cause 50% of bacterial death in the and Historical Record modern oceans. seafloor.10. with a calculated 1028 virus infections/day Most archaeal and some bacterial cellular genomes at 01/10/18. These burst cells provide nutrients Downloaded by Gothenburg University Library from online. To our knowledge viruses have not In many known cases virus infection is deleterious to the been incorporated in such models..1. tance to viral infection. dant coccolithophore algae may influence climate by release son and Banfield. 2014). .. Viruses Change Host Metabolism. to be in an ‘‘arms race’’ or ‘‘running to stand still. 2016). 2005. evolution: first. 8 BERLINER ET AL. via the so- fection (reviewed in Koonin. 1973). 2009). Evolution of host resis- in many cases.. 2009). 2003). nitro. Weinbauer. 2007. viral genomes also encode genes whose prod. and second. (Suttle. Hamelin et al. Anantharaman (Koonin. by moving exog- Most of these genes are specific for virus replication. Nonetheless. It is probable that extraterrestrial viruses—if they of viruses that are known only by their sequence (Breitbart. 2007). mostly by contributing genes that allow It has been said that evolution and possibly life as we their hosts to survive under conditions under which they would know it would not be possible without viruses (Greene and otherwise perish (reviewed in Roossinck. by providing strong selective pressure for Upon viral infection. Brum et al.liebertpub. 2011.g. 2011). these genes are components of photosystem II. enous genetic materials into cells. 2006). parasitic replicators. has been virus-mediated cell lysis. since viruses require hosts for their rep- for oxygenic photosynthesis. 2016).. The best-characterized of its host. Thus there is still a great deal to discover in our Due to their extremely large numbers.

2005). at least partially. A incorporate host genes and transfer them to other cells in a modern infection of a bacteria with a bacterial virus leads to process called transduction. three steps are required: a often acquired by the host genome. One of the first proposed virus- new genes to cells and by transferring genes from one cell to driven evolutionary events is that viruses may have ‘‘in- another. the evolution of DNA as the genetic material. direct ancestor is termed horizontal gene transfer (HGT). is indeed RNA as their genetic material are known to be incorporated. the amount of horizontal gene flow via viral in. puzzling (Rachel et al. This integration viruses. One well-studied example is the syncytin eukaryotic clade. Transitions which led to the predominance of head-tail viruses in the Viruses have been hypothesized to be responsible for the bacterial domain. 1990) and seem to be important for the devel. Horizontally transferred genes are order to convert RNA into DNA.. which also have orthogonal DNA replication systems step generates a copy of the virus genome within the host (Woese. served in archaeal viruses provides another clue regarding leading to massive amounts of HGT. in the form termed a provirus. other primordial cells. particularly if they confer ribonucleotide reductase that transforms ribose to deoxyri- the recipient with an evolutionary advantage. and a reverse-transcriptase that makes a DNA agents of HGT. the ancestors of bacteria. 2015). 2006a). gene transfer agents (GTAs) respectively. 2017). 2000. 2012: Prangishvili et al.. proviruses can be triggered to replicate and produce 2001. human development (Lander et al. to the harsh living conditions of most archaeal virus hosts. and some genes were transmitted to. rich in morphological diversity at the time of the Last Uni- Koonin et al. Viruses as Drivers of Major Evolutionary penetration mechanism to inject their genetic material. and retained by. For example. lution is that viruses drive evolution by the introduction of and even multicellularity. tory). and DeFilippis. cellular domains of life (Forterre. 2013). One recently proposed hy- 2015).. ditions. bacterial viruses evolved a physical 3. 2002. closely resembles the eukaryotic nucleus in both chaeal DNA viruses also integrate their genomes into the host structure and function (Raoult and Forterre. Since genetic bose. the tail. Generalized transducing cellular (and virus) evolution.liebertpub. some of which have been beneficial for cellular genomes. 2002: Ackermann and Prangishvili. 2016).3. the development of the eukaryotic nucleus. 1A). the this diversity is that these genes first arose in viruses. On the other hand. Virus-mediated have been found in virus genomes. 2013). The most parsimonious explanation for and invertebrate animals (Koonin.. the complete opposite. 2008). Some viruses and defective the development of a remarkably nucleus-like structure in the viruses. known as generalized transducing bacteriophage and infected bacterium (Chaikeeratisak et al. This acquisition of genes from a source other than a vented’’ DNA genomes in an ancestral RNA-protein world. acquire cellular genes. The intracellular compartment formed in the Mimi- (cellular genes that cause cancer when misregulated) were virus’ host amoeba. Forterre. The best-studied of these are the retro... that DNA polymerases in the three cellular domains are very viruses that require insertion of their genome into their host different from each other. if not the most im. virus infections led to the formation of the modern three Some viruses insert their genomes into their host’s ge. these prophages can also factory may have led to the development of the nucleus. one group of cellular played a major role in the evolution of early life. 2002). (Villarreal and DeFilippis. a thymidylate kinase that adds a phosphate group to diversity in the viral gene pool is very high and viruses are thymidine. Moreover. But opment of both bacterial pathogenesis and antibiotic resis. organisms. 2006). but each is clearly related to extant genome as part of their replication cycle. into cellular dsDNA genomes (Stedman. incorporate random The remarkable morphological and sequence diversity ob- DNA into their virions and inject these DNAs into host cells.. evolved human genome contains between 8% and 40% virus. Under certain con. due (Bachmann.. retroviruses can Mimiviruses has caused these theories to be revisited (Bell. developed a cell wall to protect themselves from viral infections. of cellular life. indicating that the viral polymerases are gene that is essential for mammalian placental develop. Even viruses that use ssDNA or viruses and limited diversity in bacterial viruses. They suggest that ancient viruses were already been even higher in primordial environments (Woese. Koonin et al. all of these genes into host genomes is likely commonplace. Syncytin is derived from not one but multiple ap. Feschotte and polymerase genes often places viral genes at the base of the Gilbert. In order to overcome this rigid defense system. Upon replication. 2002. ancestral (Filée et al. In portant agent. altered their cell surface proteins by . derived sequences.. therein. A naive assumption would be bacteriophage have been widely used in bacterial genetics that the archaeal virosphere would have limited diversity. It is thus highly likely that viruses versal Common Ancestor (LUCA). and these viral genes HGT is particularly important for evolution in species that have much greater sequence diversity than the correspond- reproduce asexually but is also widespread in both vertebrates ing cellular genes. The argument is nomes (Fig. 2001. been proposed as the origin of the eukaryotic nucleus (Bell. which eventually led to the divergence of the fection is currently considered much higher than once ex. 2016). As their proviruses replicate. For personal use only. in the case of ancestral virus infection that caused the formation of a virus bacterial viruses). and that DNA was adopted later by cellular organisms Viruses are known to be major agents. 2010) and is hypothesized to have gishvili. 2009: Pran- pected (McDaniel et al. driving force. high diversity observed in archaeal tance (Moon et al. the successful transfer of novel viral genes copy from an RNA template. ASTROVIROLOGY: VIRUSES IN THE UNIVERSE 9 Less appreciated but probably no less important for evo. termed the virus factory (or virion fac- discovered (Stehelin et al. 1976). Thus an genome. parently independent ancient retrovirus infections (Lavialle An extended version of this hypothesis is that different et al. 2006. Later. the three domains ancestors of the Archaea. Takemura. generating proviruses (or prophages.. 2012).com at 01/10/18. Bacteria and Archaea (Forterre and Prangishvili. 2002. Many bacterial and ar. 2000).. Interestingly. of HGT. In fact this is how the first oncogenes 2009). 2001). phylogenetic analysis of DNA Downloaded by Gothenburg University Library from online. Due to transduction and promiscuous provirus gene pothesis incorporates ancient viruses as a direct evolutionary acquisition. The recent discovery of the giant new virions. Engulfment of a large DNA virus has also genome. Villarreal ment.

3. 2006b. 1999.. 2013). 2014).5. such phylogeny by a tree-like structure. 2006. Deamer. Koonin et al. Krupovič and Bamford. 2010. especially since all viruses encode capsid rect evidence for ancient viruses in the geological record.. 2008). such that many of millions of years ago from both fossil and genomic data. Their viruses RNA viruses. sequence simi- Stedman. including the origin of DNA. Indirect evidence for ancient viruses comes from genomic However. both in terms of sequence and substrates used. and confounds virus phylogeny (Shi hosts.. Most Garcı́a (2015). 2017). 2015).4. Jalasvuori and Bamford... there is no di- 18S rRNA gene. not unlike enveloped RNA results were obtained with a different capsid protein struc. Recent analyses indicate that there may have been Abrescia et al. 2015. A recent metagenomic larity becomes undetectable for more ancient divergences. However. but see the and Dolja.. 2005. but proteins.. But the polymerases themselves are highly works of Schulz et al. multicellularity.. Similar self-replicating RNAs in vesicles. do not encode a DNA world. the transition between an RNA and most hyperthermophilic archaeal viruses.. further supporting the independent different viral groups based on capsid protein structure origin hypothesis (Koonin et al. and Krupovič. Forterre and Prangishvili. 1991. 2016). to the evolution of multicellularity. active area of origins-of-life research is the encapsidation of Khayat et al. isted in the hypothetical RNA world (Sankaran. 1980. Unfortunately. 2006). bacteria. dimensional structure of major capsid proteins indicates that One piece of evidence is that viruses are the only extant several viruses that infect archaea. indicates that specific An extreme example is the chimeric viruses that appear to viruses and viral defenses are at least tens to hundreds of have undergone recombination between RNA (Baltimore millions of years old (Emerman and Malik. Koonin et al. 2004. and eukarya terran life-forms that use RNA genomes.. 2011.. comparison of the three. 1997.. 2013). the genes in a virus genome do not have the same phylogeny. Iranzo et al. Koonin and Dolja. survey of invertebrate animals discovered hundreds of new The presence of conserved capsid protein structures is . 2008. more recently. Roux et al. viruses (Robertson and Joyce. 2006.. essarily always) encoded in virus genomes. The presence of common viral genes a comprehensive virus phylogeny. 2008. is not straightforward. 10 BERLINER ET AL. For personal use only. in genomes of organisms known to have diverged tens of pant recombination in virus genomes. even though se. it is nearly impossible to place all that the latter is true (Forterre. Villarreal. even if capsid protein structures could provide and structural studies. bacterial viruses. viruses into one phylogeny to represent their evolutionary Witzany. 2010). indicated that recombination between different then glycosylated their capsid proteins in order to attach to the viral genes is rampant. One of the great mysteries of the origin of viruses tionships between distantly related viruses infecting viruses is the origin of the defining characteristic of viruses. 2004. and they have There are also a few researchers who controversially claim been used frequently to reveal the history of some distantly that viruses are remnants of an otherwise extinct fourth related viruses (Koonin. Thus it may be impossible to represent virus cell surface proteins and archaeal virus capsid proteins. the vi- of all three cellular domains (Krupovič and Bamford. together with common antiviral genes. 2017). which is directly coupled Koonin et al. There ture found in a haloarchaeal virus. virus researchers think rRNA genes. Nasir and Caetano-Anollés. rion. What Is the Origin of Viruses? cells on the outside of an aggregate would be more suscep- tible to virus infection than those inside (Ruardij et al. Both of these theories indicate a relatively recent Downloaded by Gothenburg University Library from online. the recognizable polymerase gene in their genomes. Thus classification of in any cellular genomes. 2013). 2012. but some. 2014). 2013). 2016). the origin of the three domains of life..6. Nucleotide polymerases are often (but not nec. the ‘‘invention’’ of apo.. and are also many genes that are found in virus genomes but not herpesviruses (Pietilä et al. Diversity of Viruses and Their Evolutionary origin for viruses. 2012) and 3. viruses may have been involved in the evolution of Dolja. 2005. Moreover.. could be due to virus in. 2016). 2009. or the origin of the However. The third theory is that viruses could Relationships have an independent origin or multiple independent origins Due to the lack of ‘‘universal’’ genes. (2017) and Moreira and López- diverse. separable (Szathmary and Smith. 2017). Unfortunately. 2008. Nevertheless. 2012. particularly when analyzing new viral groups from metagenomic analysis (Mokili et al. HGT (Botstein. in viruses. ptosis or programmed cell death. there appears to be ram. Koonin domain of cellular life (Philippe et al. What Is the Evidence for Ancient Viruses? determining capsid protein structures is highly problematic in astrobiological samples. An quence similarity cannot be detected (Rice et al. and could thus be have a common double beta-barrel capsid protein structure descendants of viruses or similar replicative entities that ex- and are thus extremely distantly related. if viruses were involved in viruses encode a nucleotide polymerase.. as 3. Forterre. as viruses probably have a glycosylation is not frequently observed in bacterial cells and more mosaic or modular genome evolution dominated by viruses. multi- cellularity could provide protection from virus infection. Koonin et al. The evolution of cellular and viral life may not easily be Greene and Reid. There are three predomi- fection pressures (Iranzo et al. such as 16/18S (Koonin et al. 2010. development of the bacterial cell wall. Increasingly. Forterre relationships. Second is that viruses are degenerated cells. Aiewsa- Class IV) and DNA (Baltimore Class II) viruses (Diemer and kun and at 01/10/18. Major capsid protein structures could multiple origins of capsids and thus multiple virus origins potentially become the viral equivalent to the cellular 16S/ (Krupovič and Koonin. eukaryotic nucleus. 2014). identification of the capsid protein gene there is considerable indirect evidence for virus antiquity.liebertpub. 2006. In the presence of excess resources. 2012). 2014. Hendrix et al. nant theories for virus origins: First is that viruses are es- caped cellular genes. glycosylation to escape from viral recognition. This explains the high level of glycosylation on archaeal et al. Krupovič and Bam- seems to be an effective way to discern phylogenetic rela.. they must be very ancient. 2014. ford. Koonin and Finally.

2011). but this work should be of et al.liebertpub. macroscopic effects of virus infection could predated the divergence of the three domains of cellular be detectable. 2004. chemical signatures and isotopic fractionation. oids.8. present in low Earth orbit on the ISS in aerogel for over a Standard detection strategies for existing life. there may have been multiple. Virus Biosignature Detection host. 100-million-year. isoprenoids. The Tanpopo mission collected particles high priority. if host metabolism is changed by virus genes. These deposits appear to for UV irradiation on the International Space Station (ISS). such as terrestrial samples. Could Viruses Be Spread Extraterrestrially? riophage T4. level. a plant virus mental composition (inductively coupled argon plasma mass that is highly resistant to desiccation and can be crystallized. for example. chemical from Earth. Moreover. Similarly. Such an significant loss of activity (Parvenov and Lukin. (viral capsids).. serve as detection strategies space environment for up to 2 years. fully as- meteoritic samples collected in the Tanpopo aerogel contain sembled virions are composed of three of the four standard virions would be very interesting but unlikely to be unam- cellular macromolecules including nucleotides (DNA or biguous due to the lack of validated virus biosignatures. 1992). or FTIR spectroscopy). however. some viruses also months (Laidler and Stedman. extraction of rocks with organic solvents followed by liquid However. It is not known thereafter (Laidler et al. amino acids. Direct detection of viruses is more However. 2011). The most parsimonious expla. Moreover..1). this that endolithic viruses or viruses encased in salt crystals could be detectable remotely. Unlike most of current techniques is insufficient to determine whether host-derived viral components. independent ac. also serve as There is almost no evidence for viruses in the rock record.. Orange et al. Whether any micro- for existing viruses. and caroten- old amber (Poinar and Poinar. mainly due to lack of biomarkers. chemical. there are a viruses have been shown to impact life at an ecosystem limited number of clades. but none of these studies addresses possible survival such as methane or N2O should be detectable remotely. It is theoretically possible however. 2010. Stedman. While the standard Structures resembling virus inclusions formed by current array of chemical signatures for detecting extinct life includes insect viruses have been detected in ca. cyclic alkanes.. and ele- the space environment... but infectivity was completely lost could be useful as indirect measurements. be due to massive lysis of coccolithophore algae. Virions are smaller than their 3. A few studies have examined virus stability in species (GC-MS. specific virus chemical signatures are still under inves- tion of the well-studied bacteriophage T4 and extremophile tigation. Laboratory silicifica.. given changes to Earth’s biogeochemical cy- life (Rice et al. 1973). have what was thought to be virus-specific nucleotide mod- ifications. In both analyses. detection strategies for extinct viruses. this modified nucleotide has recently been found in human DNA (Bachman et al. Laboratory methods to identify the isotopic possibly volcanic activity would have ejected viral particles abundances (high-resolution mass spectrometry). 5-hydroxy-methyl cytosine in bacte- 3. Samples have just been to our knowledge if virus-specific AMG fractionate isotopes returned from the Tanpopo mission on the ISS (Kawaguchi differently than cellular enzymes.7. cles (see Section 3. can be adapted for biosphere and due to the small particle size and mass of use in virus detection by simple manipulations of equipment most virions. some viral lipids exhibit a Downloaded by Gothenburg University Library from online. 2012). proteins. realistic given the average size of a virion. Poliovirus and bacte- from potential cellular material in bulk samples is problem- riophage T1 were exposed to the space environment on atic. organic inclusions in rock are viral in origin (Laidler and distinct chemical signature from the lipids of host organisms. sterols. including year and also exposed terrestrial bacteria and yeast to the biomolecules and chiral excess. of viruses to interplanetary transit. However. However. Because virions do not metabolize directly. At present there is no evidence for virions in any extra- Common techniques for biosignature at 01/10/18. thus the proportional relationship between components What might virus biosignatures be? The 2015 NASA in detectable biomolecules of viruses could provide a vi- Astrobiology Strategy describes the breakdown of current rus biosignature if high-enough (<10 nm) spatial resolution . hopanoids. to virus infection (Wilson et al. A survey of virion stability studies was published (Griffin. More promising is detection of a virus-mediated event. disequilibria such as could survive space exposure. NMR. possibly due but infectivity was not tested thereafter (Bérces et al.. 2011). 2005). Enveloped viruses containing lipids may provide a viruses led to the determination that the spatial resolution detectable chemical signature (Kyle et al. 2014). For personal use only. As opposed to cellular life. 2015). 2010. remote detection of individual virions is implausi- nation for these data is that these virion protein structures ble.4 above). 2016). ASTROVIROLOGY: VIRUSES IN THE UNIVERSE 11 indirect evidence for ancient viruses’ lineages (see Section techniques and strategies for life detection into remote 3. differentiating viruses infectivity loss (Koike et al.. including and cellular evolution (Krupovič and Koonin. spectrometry) all can be used with little to no modification was exposed to simulated interstellar radiation and low to identify and characterize extant virus samples along with temperature (77 K) high vacuum (10-8 torr) with minimal samples of potential life. event has been proposed to have led to the famous chalk Dried bacteriophage T7 was used as a biological dosimeter deposits of the white cliffs of Dover. redox. high-altitude balloons and rockets for short times without such as massive lysis or death of host organisms.. Although based on structures of their capsid proteins. it is likely that meteoritic bombardment or and technique. considering the high abundance in the modern chromatography and demineralization. Tobacco mosaic virus. Krupovič and Bamford. 2017). such a distinction may prove critical in the chemical detection tectable virion morphology was lost over periods of days to of viruses in the rock record. 2009). de. 2013). RNA). and in some cases lipids (viral envelopes). Orange et al. quisitions of virus capsid proteins throughout both viral The standard detection strategies for extinct life. and mineralogical chemical signatures should We found that silica-coated bacteriophage T4 could survive not be used as direct detection mechanisms for viruses but a month of drying. but for how long is not clear. when virus capsids are classified and direct detection of extinct and existing life. no by-products 2013).

Bamford. Se. Grants MCB 1243963 and MCB 0702020..J. B. and the ubiquity and role of viruses in Earth’s ecosystems. Rönnholm. such Abrescia. and quence identification of the amino acids or nucleotides of a NASA.G. (ViroChip). Annu Rev Biochem Downloaded by Gothenburg University Library from online. Microbiol Rev 54:130–197. interactions in hypersaline environments..A.S. Virology viruses in the origin and evolution of early life. contributed to this Kukkaro. (2005) Constituents of SH1.H. A. outreach to astrobiologists and the general public regarding Atanasova. 2016. 2016). W. (1990) Linkage map of Escherichia coli K-12. H. Science 344:757–760. Bamford. and owns StoneStable. Inc.. and Banfield.S. . M.M. is founder and Chief Scientific Officer various chemical techniques can be applied for the detection of StoneStable. Nat Chem 6: look elsewhere. Roine. techniques such as melting and filtration of ice followed by ultrasensitive analysis using Author K. K. Anderson.A. (2012) Prokaryote extraterrestrial viruses. doi: trial material. M. E.P. J.A. P.. Entering the second century of virology. Arnold. U..M. P.. and some bioinformatics techniques can identify un. their cellular counterparts. J. More than a century has passed since the discovery of the Anantharaman. and Stuart. some cases.H.. and characterization of known existing viruses. as high throughput sequencing or high density microarrays (2012) Structure unifies the viral universe.J.P. interests exist.B.. X. S. Many viruses produce complex capsid Foundation. Colson. J. and Baross. Nonetheless. For personal use only. (2) consideration CRISPRs as a metagenomic tool to identify microbial hosts of virus-detection experiments to be used for missions that of a diffuse flow hydrothermal vent viral assemblage.I. However.. H. D. could be obtained.J. J Virol 79:9097–9107. Zillig.. M.B.. Virology 272:409–416. Author T.. J. a novel supported by Kurita Water and Environment Foundation lipid-containing virus infecting the halophilic euryarchaeon research grant program. PCR and phylogenetic analy. Acknowledgments edition 8.. Wiley.. and Zillig. Award number NNA11AC01G.. lab-on-a-chip methods using capillary electrophoresis and laser-induced fluorescence. D. Baltimore. Holz. N. N.. and Prangishvili. 81:795–822. T. J. a single protein is sufficient for assembly of a grant numbers 17H05811 and 17H05229. D. and Nelson. K. P. The authors acknowledge Autodesk. (2017) Marine origin of 4...W. particularly endolithic Arnold. Arch Virol 157: we find that the development of virus-specific biomarkers 1843–1849.F. stock.. Ut- viruses. of the Urayama et al. 2nd known but prevalent viruses (Roux et al. G.. 2016). Oren. and KAKENHI grant from Ministry of Educa- geometries from the arrangement of repeated proteins. Duhaime. Laurinavičius. 2011).H. highly abundant cosmopolitan viruses (Roux et al. Science and Technology of Japan. Somerharju. References sensitive mass spectrometry. New York. Sports. SIFV.. and (4) more 267:252–266. and Raoult. Author K. I.1038/ncomms13954. Science 320:1047–1050. J. a novel virus of the extremely thermophilic and acidophilic archaeon In the longer term. W.M. Ziese.g.. viruses studied by electron microscopy. H. (2011) Using clude (1) validation of virus biosignatures... (2) characterization of terback. 12 BERLINER ET AL. Ziese.. R. Culture. article while employed by Autodesk. (2000a) SNDV. Microbiol Ecol 77:120–133. Uribe-Lewis. the identification of truly novel viruses.H. been intimately involved in the origin of life. and ultra. A.liebertpub. Inc. doi: 10. and Dick. (1) more exposure studies of viruses. first viruses.M. to the space environment. (3) greater research into the roles of extremely thermophilic crenarchaeon Sulfolobus. future astrovirology research in the short term should in. S. highly abundant yet underappre.. (4) determination whether virus-encoded dynamics and acquired virus resistance in natural microbial and transferred AMG fractionate isotopes differently than communities. (2012) Global network of specific virus-host Viruses are an integral. and Katzourakis.E.. S. but are not limited to. B. declare no competing financial clude. Ravantti.1.E.. of Fig. Front Microbiol 7. D. ses. Foundation. we can Toner.. H.. and T. at 01/10/18. should be an active area of astrovirology research and is Aherfi.. Dyall-Smith. Weidmann.. ed.. Inc.K. (1971) Expression of animal virus genomes. immunoassays. award number 16B094.. Kalkkinen. (2016) Giant highly relevant to the detection of viruses in extraterres. N. H. J.. Inc. (2011) Fundamentals of Molecular Virology. Acheson.00349. U.F. These modern techniques. These in... but let’s start looking. viruses of amoebas: an update. Crosby. Bachmann. They play a critical role in 14:426–440..3389/fmicb. the National Science proteins could provide insight into the sample identity. We do need to A. S.. Nat Commun 8. Oksanen.M. Williams. can identify known viruses (e. (3) in.. biogeochemical cycles and evolution today and may have Bachman. In addition to the common techniques applied to extinct Author Disclosure Statement viruses described above.. remains problematic.. N. Kristjanson. M. 2012). Brazelton. 1049–1055.. Detection of repeated supported by Portland State University.. J... Yang.. (2014) Sulfur oxidation genes in finally start focusing beyond our own planet. Yozwiak et al. Wendt. Murrell. Aiewsakun.J. D. FEMS sample water plumes from Enceladus and Europa. astrovirology objectives should include Sulfolobus. Authors A.2016. K. was and Bamford.. (2008) Virus population terrestrial systems. 3 and cover art..A. employee Joe Bacteriol Rev 35:235–241.F.K. Future Outlook retroviruses in the early Palaeozoic Era. B. Andersson. (2000b) A novel lipothrixvirus. Klenk. Grimes. clusion of viruses in models for ancient oceans and extra.S. A. and Balasubramanian. (2014) 5-Hydroxymethylcytosine learn much more about viruses on modern Earth before we is a predominantly stable DNA modification. M. P. D. G. such as potential Ackermann. in tion. Environ Microbiol ciated part of life on Earth. was complete capsid (Acheson.P. 10. Author A.. La Scola. D. Japan Prize Haloarcula hispanica. Lachoff for his assistance in generating an initial version Bamford.H. Priorities for diverse deep-sea viruses. Breier.B. virion provide immediate insight into identity of the virus.

.2015... Speich. Khanna. Newton. and Laurent... (2010) Paleovirology—modern Bell. P. Orig Life logical drivers of ocean viral communities.B. Gorsky.J. and Suttle. (1989) Filée. R. Gasol. Nguyen. J. In 47th Lunar and Planetary Science Conference nica. PLoS Biol 8. H... Forterre. Dimier. and Neidholdt. L. Washington.O. and Hackl. Beijerinck..Y. Alberti. Not. Wilson. A. F. Rev Genet 13:283–296..G.... Bonch-Osmolovskaya. Egyeki. S. (1980) A theory of modular evolution for bacte.S.V. Springer. and Dyall-Smith. S.0441. American Society for variable pressure scanning electron microscope (MVP. M. Horneck. J. D. E. lution of DNA polymerase families: evidences for multiple Nature 340:467–468. MacLellan. J. (2012) The origin of virions and Chaikeeratisak. Dor- R. EXPOSE-R facility: biological dosimetry of solar extrater. A.H. Coker. experimental evolution.. P. Wincker. M.. J.T.. Biol genus Thermococcus. G. (2009) The viral eukaryogenesis hypothesis: a key consequences of ancient viruses. (2006) Viruses take center stage in cellular and viruses) as the major source of evolutionary novelties. Hin... P.L. Genome Biol 7:110. virus. J. Gregory. D. 1261498. Rev Microbiol 3:504–510. Curr Opin Microbiol 5:525–532. Chaffron.. Searson.. three DNA viruses to replicate their genomes: a hypothesis gamp. Sunagawa. Harvey. Evol 54:763–773... Crick. C. G.1098/rstb. ASTROVIROLOGY: VIRUSES IN THE UNIVERSE 13 Bath.P. M. Time: Friends. C.M. Environ Microbiol 14:503–516. R. S. Botstein.C. and Krupovič. (2016) Host genome integration Astrobiology Science Conference 2004: Special Supplement. T. discovered in an extreme environment suggests recombina. (2008) Viruses in acidic geothermal envi. In Abstracts from the Fischer. doi:10. Schenck. R.M. D.R.. Le Romancer.G. D.... C. war between ribosome. Forterre. C.L.. Science 355: Forterre. Prieur. F.L.. Ann Rev Mar infects marine zooplankton. (2012) TPV1.. Diemer.. doi:10. Acinas.pbio. Karsenti. Forterre. Blumberg. J.1000301. (2016) Evolutionary transitions during RNA virus Amsterdam 65:1–22. gene exchange between cellular and viral proteins.R. de Vargas.C.E.3390/life7010005. handelingen der Koninklijke akademie van Wetenschappen te Elena. E.J.J. D. S.. The Netherlands. In Viruses: Essen- M. and Prangishvili. structure during viral replication in bacteria. and Gilbert. J. Ver. J.L. Kandels-Lewis. ‘‘Pyr- Life 7. edited by G. P. A... A. F. tial Agents of Life. the first virus-like particle Deamer. H. and Prieur. (2010) Giant virus with a remarkable complement of genes Breitbart. Enard.... G. for the origin of cellular domain. Marine T4-type bacteriophages. (2006a) Three RNA cells for ribosomal lineages and C. Jerman. Poulos. K. Ann NY Acad Sci. S. Abstracts. Change Agents. M.liebertpub. Ogata. Patterns and eco.. Gwennap. J. K.. Ann NY Acad Sci 354:484–490. and Filée. Cruaud. Direct 7. M. 1178:91–105. C. G.A. Res Microbiol 159: the dark matter of the biosphere..A. Microbiology. (2003) PAV1.M.. and Krisch. 19508–19513. M. (2005) Viral metagenomics. and Rohwer.. C. Lunar and Planetary Institute.. DC. A...12469. (2010) Defining life: the virus viewpoint. (2017) Assembly of a nucleus-like drecht. and Heldal. 103:3669–3674.. For personal use only.. Greene. C.1371/ role for viruses in the emergence of eukaryotes from a pro. K. M. journal. Nat als Ursache der Fleckenkrankheit der Tabaksblätter. Nat 14:47–53.1186/1745-6150-7-13. (2002) Evo- Downloaded by Gothenburg University Library from online.. Guidi. Schwenck.A.. D. Tara Oceans Coordinators.. P. (2012) Endogenous viruses: in- restrial UV radiation. eLife Panitz. J. J.M..K. S. doi:10. G. Proc Natl Acad Sci USA 358–366. M. (2004) Astrovirology. and Malik. transition to the DNA world: a story of viruses and cells..B. C. Forterre. an archaeal virus SEM) for in-situ Mars surface sample analysis [abstract of the Fuselloviridae family that infects Haloarcula hispa. Buschauer. G. Perrot. Forterre. (1998) His1. and Stedman.. ISME Forterre. D. regional variation and dominance of non-tailed viruses... J..W. and Pogliano.. Erb. Gaskin. M. H. Nature 177:473– at 01/10/18.D. A.’’ J Bacteriol 185:3888–3894. (2001) Viral eukaryogenesis: was the ancestor of the 371. Feschotte. International Journal of Astrobiology sights into viral evolution and impact on host biology. Cai. D. (2015) The PUR experiment on the 5.A.-M. W. G. Allen. (2006b) The origins of viruses and their possible P. Foes. (1898) Über ein Contagium vivum fluidum Edwards. 102:12471–12476. J Mol Bize.. and giant virus-induced reactivation of the virophage Ma- International Journal of Astrobiology 3:26–27.A... ococcus abyssi. (1956) Structure of small Geslin. Børsheim. Lucas.S. A.F. K. Proc Natl Acad Sci USA 107: Sci 4:425–438. P. Picheral. P. karyotic world environment. Bork. and roles in major evolutionary transitions. C. T..G. (2002) The origin of DNA genomes and DNA morphological analysis of marine viruses shows minimal replication proteins.. High abundance of viruses found in aquatic environments. V. a ubiquitous component of ronments of the Kamchatka Peninsula. C. G. Erauso. and Sullivan. Roux. Fekete. M. E.7554/eLife. Witzany. Prokofeva. (2015) Ocean plankton. doi:10. D. Forterre. Pesant. Science 348: Evol Biosph 40:151–160. Kovács. (2012) Marine viruses: truth or dare. M. I. isolated from a hyperthermophilic euryarchaeote. Koonin.. G. B. Peng. pp 43–60. Bienvenu.. Tétart.. Sullivan. O. S. (2016) Viruses Bérces. virocells: the escape hypothesis revisited.. doi:10. and Watson. Bowler.A. K.. P. Philos Trans R Soc Lond B Biol Sci Bell. Biochimie 87:793–803... Houston. and Geslin. Gaillard. P.A. Nature 540:288–291. Ignacio-Espinoza. F. a report from the Doloboff. Bratbak. M.. K.C.and capsid-encoding organisms (cells Claverie. (2005) The two ages of the RNA world.. C. Vavilina. evolution.S.L.A. (2005) Prangishvili.. M. nucleus a complex DNA virus? J Mol Evol 53:251–256.. M... J Virol 72:9392–9395. S.. Brilot. S. P. (2017) The role of lipid membranes in life’s origin. A. R. P. riophages. Brum. G. Proc Natl Acad Sci USA B. N. C. (2014) Viruses Throughout Life & Edmunson...J. E. L. (2012) A novel virus genome Gorlas. X. Iudicone.. and Rontó. Emerman.H.. are a dominant driver of protein adaptation in mammals. S. M. 2301]. and Petrov. P.. S. A. Ann NY Acad Sci 1178:65–77. and Reid.L. G. P. Doulcier. Garrett..F. Virus Res 117:5–16. and the J 7:1738–1751.. the first virus isolated from the hyperthermophilic tion between unrelated groups of RNA and DNA viruses. . M. Brum. S. Fischer.. viruses. (2016) A miniaturized American Academy of Microbiology. Sen-Lin. Suttle. (2013) Global Forterre. (2009) The great billion-year 194–197.C. Bergh...

and Miyaji.V. K.J. ditions.R.. Jahnke.L.. and Johnson. F1000Res 5.. (1999) Evolutionary relationships among di. F. M.1073/pnas. D. (2015) 2015 Astrobiology Strategy. E. A. Kyle. Koonin. Larson. (2009) Viral biogeography re..... L. Y. G. (2017) The evo. J. Leuko. and Sullivan. doi:10.A..I. (2005b) Virology: independent virus Koonin. Origin of Biological Evolution. C. Zillig.J. Smith. through transmission-virulence trade-offs. H. viruses.1621061114.J.. M. B. D. M.A.M. R. Yokobori. Hurwitz.... (1991) The phylogeny of RNA-dependent RNA Downloaded by Gothenburg University Library from online. Jungang.. S.. (2016) AstRoMap European Astrobiology and evolution of viruses of eukaryotes: the ultimate modu- Roadmap. the Ampulla.liebertpub. a family of Houston..F.V. V. and Bamford.. K.Q.. M. Krupovič.pone.... Claverie. Walter. (1992) Survival rates of some moproteus: a novel virus family. Koonin.M.T. B... E.B. Astrobiology 16:201–243. and Koonin. G. Nature 436:1101–1102.0057355.J. C. A. Kawai. Biol Direct 1:29..1016/j. and Whitaker. . Rull.H.. Nat Rev Microbiol 6: dino. Hajimorad. vili. P.. (2006) The Holland. R.E. Koonin. Proc Natl Acad Sci of gene sharing.. K. L. Nagasaki. universe..I... Krupovič. D. Genet 192:39–45. Rachel. J. Pilat-Lohinger.I.W.E. N.H... En.V. Brucato.E. Lawrence. D. J. (2017) Evolution of RNA-and DNA-guided an- Hays. Astrobiology 16:363–376.. Wolf.J. F.... V. doi:10.. Pryor. Cell Cycle 13:3083– viruses: 20 families and only five different architectural 3088.. (2008) Structural co. and Koonin. R.. R. R... anaerobic. (2005a) Viral diversity in hot springs of Pozzuoli.V. J. E. perthermophilic archaeal genera Pyrobaculum and Ther. Acid. Peng.. M.L.. sulfur re.. Chen. Esposito.V. H.. J.H.. (2011) Virus Taxonomy: Ninth Report of the International Häring. Jeger. C. V. F. Peng. E. V. T. DC.C. D. E. and Dolja. X.A. J Gen Virol 72: Italy. A. Robert. Stetter. Garrett. New K. R. [abstract 2228]. verse bacteriophages and prophages: all the world’s a phage. Hendrix. (2013) A virocentric perspective viron Microbiol 11:457–466. S. Garrett. J. (2008) Virus evolution: how Virome (POV): a marine viral metagenomic dataset and as.. and Tian. L.. Hendrix.. viruses of the extremely thermophilic. Virology 323:233–242..1186/ Held.. Young.. M. and ence Conference Abstracts. R.V. and Koonin. doi:10. Adams. Ta- about the viruses? Astrobiology 13:774–783. and at 01/10/18. Wunderl. (2013) The Pacific Ocean Krupovič. M. and Dolja. J Virol 79:9904–9911. Hilker.. vealed by signatures in Sulfolobus islandicus genomes. Allen. (2016) The double. Saddle River. Philos Trans R Soc Lond B Biol Sci 361:903–915. principles for virion assembly.8737.R. 10.V..M..T. E. M. Oshima.. (2005) Structure of an archaeal virus capsid Hansen.. E. Hashimoto. Virus Res 241. larity.04.. E.V.. 925–939... Wolf. Muller. L. E. D. C.1128/mBio. Taguchi..W. Grenfell. Burns. The Big Bang of picorna-like virus evolution antedates the Gomez. H. B.. M. J.. Nishimura.V. Koonin. K. and Dolja. doi:10. G.V. Lunar and Planetary Institute. Proc Natl Acad Sci USA 96:2192–2197. B.. H. far does the double b-barrel viral lineage extend? Nat Rev sociated protein clusters for quantitative viral ecology. (2016) Investigation Hamelin.S. 2197–2206. Rachel. Washington..L. and Raoult. T.W. Ford. A.. M.. Lee. and Prangish.N. Lefkowitz.. TTV2 and TTV3. Koonin. E. USA 114. R. and Koonin.. Yano. R. and Bamford. Biol Direct 12. Drancourt... Krupovič. of the interplanetary transfer of microbes in the Tanpopo M.. (2014) Virus-host arms race at the joint origin of multicel. V.G.V. and Dolja.. A. R. Proc Natl Acad Sci USA 102:18944–18949. (2016) Horizontal gene transfer: essentiality and development outside a host. H... NJ.. lutionary network of viruses and capsidless selfish elements. M.V.M.. and Krupovič. K. N..1.A. polymerases of positive-strand RNA viruses. Harrison. world of bacteriophage diversity. Virology 479:2–25. from a new family.. and Prangishvili.. G. E. Rachel. Brügger. Häring. E.. Science 299:2033. on the evolution of life. F.. M.. M.-I... Onofri. D. (2003) A giant virus in amoebae. L. M. (2004) Morphology York. I. Dolja. A.V.2017. and characterization of a unique archaeal virus. G.. s13062-017-0177-2. Garrett.R. (2008) Horneck.. and genome organization of the virus PSV of the hy. Koonin. Stewart. gas leaving Enceladus. and roles in evolutionary transi- Hatfull. 14 BERLINER ET AL. (2008) Water vapour jets inside the plume of King. Holz.O.V. radiation of eukaryotic supergroups. Audic. doi:10. R.F. and Prangishvili. (2006) The oxygenation of the atmosphere and ancient Virus World and evolution of cells. Rettberg. Microbiol Mol Biol Rev 78:278–303. (2012) Preservation evolution of viruses and cells in the primordial world. One 8. J. and Stedman..B. Strazzulla.. mBio 7. W. protein reveals a common ancestry to eukaryotic and bacterial Wallis. K. and Yamagishi. X. E. Nature 456:477–479.M. (2010) Order to the viral Iranzo. L. H. and Carstens. (2017) Multiple origins of viral stranded DNA virosphere as a modular hierarchical network capsid proteins from cellular ancestors. Y. (2015) Dark matter of the biosphere: the amazing tions. editor in chief. E. Orig potential of lipid-containing viruses under silicifying con- Life Evol Biosph 38:165–181. PLoS Microbiol 6:941–948. Iranzo. Curr Opin Virol 1:118–124. (2015) Origins Capria. F. ducing archaebacterium Thermoproteus tenax. K. D.virusres. M. and Prendeville. Adv Space Res 12:271–274. bata.D. Committee on Taxonomy of Viruses. Gierl. tivirus defense systems in prokaryotes and eukaryotes: com- NASA. mon ancestry vs convergence. ianus bottle-shaped virus. Mol Gen X. mission at the Exposed Facility of the International Space lution of parasitic and mutualistic plant-virus symbioses Station. Krupovič..E. (2013) The quest for extraterrestrial life: what Kawaguchi. Upper Häring. (2014) Virus world as an evo- Hatfull.-M.. Tang...1371/journal. (1983) TTV1. F. oceans..011. M. Meinke.R. (2011) The Logic of Chance: The Nature and viridae. Neumann.. Griffin. S. Curr Opin Virol 3:546–557.A. In 43rd Lunar and Planetary Sci- Janekovic. M. FT Press Science. J Virol 89:8107–8110.00978-16. Koike.. the Globuloviridae.V. evolvability in prokaryotes. M. J. L..F.. Birtles. R.V. Koike. Tsiganis. Jalasvuori. and Bamford. and Bamford. doi: Khayat. E. Lobkovsky.12688/f1000research. Senkevich. Vestergaard. Sala. D.V. J..F..H. terrestrial microorganisms under simulated space conditions. Academic Press. Larsen. T. W. Westall. N.M. J. Martin. Tanaka. S.. S. Colwell. E. (2011) Double-stranded DNA lularity and programmed cell death. Y. R. La Scola. H. M. de Lamballerie. Palomba.M. Sun. For personal use only. E.K. M. J Virol 84:12476–12479. W.

A. T... Rubin. P.. Rappé. C. R.1128/mBio. virology of ‘syncytins’.. and Campbell. Sci Adv Stedman. Kandasamy. K. Karthikeyan. lineage of viruses with a membrane envelope. Biogeosciences 8:1465–1475. Mann. (2013) Reversible inactivation and desicca. N. Pavlopoulos. Esnault. and Clokie.C.J.S.. J..-D. Nature 424.. Desnues. Ritchie.E. Laurinmäki. (2003) Origins of (1978) General Virology. Metcalf. M.. W. S. J Virol 87:13927–13929. A. Orange..M. J. S. Prangishvili.. Y.. Sako. Park...H. (1973) Results and prospects icosahedral DNA viruses with a pandoravirus morphology.. Curr Opin Virol 2: 15902. D.. Jacobs- . Y. Y. B.. and Steward. A.E... J Bacteriol 193:5412–5419.. M. D. F.M. K. and Raoult. Cook. Sci Rep 5...2014. Consortium. J.. and Dutilh. K. Cell 113:171–182.Y.1098/ tremophilic archaea. T. O. A. N.. G. (2013) Pan- Martin. M.. S. M. O. S.. (2015) A phylogenomic Laidler... D.. doi:10.1098/rstb. Millard. and Lukin. Lescot. (2012) Archaeal virus with Prangishvili. Lewis. and Stedman. mas. Gross... Jacobs-Sera. W. Jacobs-Sera.S. M. A. J.R. Mochizuki. Tanaka. J. (2013) Paleo. Forterre. S. Luria.. K.. M. (2010) Diversity of viruses of the hy. Jungbluth. viruses of hyperthermophilic archaea.. and Prangishvili. and Bordenstein.. W. R..02129-16. Virology 402: Lawrence..... D.N.. Legendre.. Huntemann. J. M.. J.S..1126/sciadv. (2010) Virus silicification origin of eukaryotes? Philos Trans R Soc Lond B Biol Sci under simulated hot spring conditions. Iva- Adrait.. Geslin. G.A. D..R. Bertaux. doi: human genome.L. C. D. 10.. L. Hedlund. O. (2014) Thirty-thousand-year-old distant relative of giant Parfenov. M. doi:10.. Le Romancer. Delaney.A. Bruley. Abergel.A. Lucas-Staat. B.. 10604–10609...H. (2005) Fossil evidence of insect and Prangishvili.A. V.. and Caetano-Anollés.. T. EMBO J 3:2165–2168. Houtz. (2002) Remark- . Proc Natl Acad Sci USA 109:13386–13391. ASTROVIROLOGY: VIRUSES IN THE UNIVERSE 15 La Scola. (1990) Viral mortality of Moon. (2013) The wonderful world of archaeal viru- exceptional virion architecture and the largest single-stranded ses.R.. Falbo. and Krupovič. Sera. E. virome. Yoshida. Häring.1126/science Pietilä. D. Bardarov..... doi:10..H. Young... J. D. Seltzer.F. E. J. T. Jacobs... S.Y. Shmakova. P. C.. Ruhnau.W. L.G. G. Annu Rev Microbiol 67:565–585. Proc R Soc Lond B Biol Sci 368. Poirot. P. Mi- Lander. F.. and Pedulla. G... Proc Natl Acad Sci USA 110: crobiol 15:546–552.H. D. marine bacteria and cyanobacteria.S. C. Rachel.R. Krupovič. E. M.. and the International Human Genome Sequencing randa. J.. doi:10. L.. D. C. and Hatfull. 289–294.R. and Seo.. J.G.-C.1002/97804700 and future perspectives in virus discovery. Arslan. and Abergel. and Heidmann. New York. S.. Pehau-Arnaudet.. Darnell. E. 63–77. L.M. Claverie. D. C.. srep09784. representative of the family Clavaviridae. S. A..A. Astrobiology 10:569– 370. (2011) Provirus veals a continuum of phage genetic diversity. B. J. R. Nature 536:425–430.A. 1. Koonin. Philippe.K.A. Kess- mediated horizontal transfer of a Staphylococcus aureus ler. Lin. G. Chabin. C.1038/424741a. Vernochet. Paulin. D.. Aeropyrum pernix spindle-shaped virus 1 and Aeropyrum Prangishvili. D. Tho- Downloaded by Gothenburg University Library from online.7554/eLife.J.. G. S.a0000774. M.. Hendrix. J. P.I. comparison of a large collection of mycobacteriophages re- Mochizuki. Bailey. Jr. Ford.. Bowman. Lawrence. mBio 8. 160–179.. Jacobs. Park. Pagnier. G. Kalkkinen. completes the HK97 fold story. J.. J Invertebr Pathol 89:243–250. D. Science 341:281–286. Nature 438: Pannunzio. doi: induction in hyperthermophilic archaea: characterization of 10.R.. Sako. N. a virus... T.. the first Asai. tion tolerance of silicified at 01/10/18.. D. Heid.0507. rstb. 86–89.E..1038/ Fournous. Kirakov.M.. Bartoli. Jr. C. M. Suzan-Monti. (2009) An ssDNA virus infecting archaea: a new McDaniel. virulence-associated genomic island. S... L. K.H. Jeudy...06416..B. Cresawn. N. D. L. and Westall. Forterre. D. perthermophilic archaeal genus Aeropyrum.R.F. T.P. (2010) High frequency of horizontal gene 72:307–319.H. A. Roine. C. A.. Aicher. Russell. Proctor. W... doi:10. a temperate UV-inducible DNA reaching that of parasitic eukaryotes. Forterre..D. (2011) Experimental fossilisation of viruses from ex- in placentation. P. APBV1. Science 330. Nature 343:60–62. John Wiley and Sons. doraviruses: amoeba viruses with genomes up to 2. E..Y. C. R. N. and Kyrpides. viruses yield proteins during host infection. Merchat. Lavialle. Reiter. Robert. J.. E. C. 576. W. doi:10.. Rivkina.. Mokili. C. Janekovic. D..... and isolation of Pope..D. Pietilä. Curr Opin Mi. I. Nasir. Rohwer. retroviral env genes exapted for a role F. D.. M.. and Fuhrman. Garin.P. J. Res Microbiol 154: Mochizuki.A. Barrassi.-T. G. Dupressoir. Kumar.. Stetter.W. M.D. A. eLS doi:10.. S.. R.. Y. F. Prangishvili..A.pub3. and data-driven exploration of viral origins and evolution. Yeats. Poirot.. and Bam- ocaldarius isolate B12. S.W. Ko. Shugart. P. Mol Microbiol K... Basta. (2005) Photosynthesis genes in marine worth.. C. Y. Garrett.. and Paul. M. W. J. K. Nigro. J. Nature 409:860–921. Y. J.. O. and López-Garcı́a. (1984) SAV 1. Doutre. (2016) Uncovering Earth’s Couté. E. G. J. of microbiological studies in outer space. pathogens.. (2008) The virophage as a unique Moreira.F. Labadie. D. Hendrix. Fitzgerald.L.M. J..A.P.. Brucker..E. J. eLife 4. Bahjat.K.0327.1192243. R.. Wads- Chisholm. nova.. A. highly mosaic mycobacteriophage genomes. J..W..A.liebertpub.. Legendre.A. R.. DNA genome. T. D.. Baltimore.. Keenan. Bertaux. Eloe-Fadrosh.. and Butcher... and Prangishvili.A. N. V. virus-like particle from the archaebacterium Sulfolobus acid.5 Mb and Zillig. Johnson. and Claverie. For personal use only. H.. Bruley. Sako. N. and Prangishvili. Space Life Sci 4: Proc Natl Acad Sci USA 111:4274–4279... D.M. Coute..C. Hwang. Hendrix.2012...-M.1500527. (2003) Marine ecosystems: bacterial photosynthesis genes in Lescot.. D. L. Gorlas. Paez-Espino.O. J. and cells: do we need a fourth domain of life to explain the Laidler.D.. Robinson.. mann. (2012) Metagenomics (2016) Viruses of the archaea. B. Mikhailova... Thomas. M. M.. Lindell. C. (2001) Initial sequencing and analysis of the (2017) Viruses in the oceanic basement.. S. (2015) Phage. W. J.. G. Poinar.. (2015) Evolution of viruses parasite of the giant mimivirus. (2003) Evolutionary insights from studies on pernix ovoid virus 1. transfer in the oceans. G....... J. Forterre. Bettstetter. L.R. the Aeropyrum pernix bacilliform virus 1. A.G. D. Hsieh. and Hatfull.. C.. Cady. Nature 455:100–104. Jaffe.L. ford. M. G. (2015) Whole genome 347–354..-C. A. Russell.. and Poinar. Bamford. (2012) The complexity of (2013) Structure of the archaeal head-tailed virus HSTV-1 virus systems: the case of endosymbionts. Schvarcz. M. Church. Z.. Cornelis..

Orton. M.. J. NJ. H. Eden. Picheral.. Princeton University Press. Takaki.. PLoS Biol 4:1344–1357.. ecosystem.J. King. Tang. J. Tesh. Kyrpides. 2:203–217. C. C.P. A.P. Buchmann. Bronner. Alberti. and Brussaard. RNA virus surveillance. X. J. La Scola..Z.. N. F.. (2015) 40 years of Brumfield.R.. J. K. A. (2003) Global phage diversity.. Yutin. doi: (2004) The structure of a thermophilic archaeal virus shows 10... their mark as mutualistic microbial symbionts. Bork. Cra- Rice...J. and Sullivan. Schouten.. Arch Virol 147:2419– lombet..V. Szathmary.. Ogata.. M.. Nat Commun 4. Microbiol Rev 28:127–181.. S. F.. T. H...J. Koonin.. Rice. Stedman. Xu... T.. and Hawkins. FEMS the invertebrate RNA virosphere. A. povic. Gillitzer. Wincker.liebertpub. B. C. Duarte.. Curr Opin Virol 1:289–297. B. Suttle. M.. Biol 187:555–571.R. DC. G. a double-stranded DNA viral capsid type that spans all Stec.P. M.. G. M... R. Rohwer. Y. L. K. C.. Nibert..R.J. Sunagawa. W.. Nat Rev Microbiol 5:801–812. Virology 479: Viruses from extreme thermal environments. Bie- tween the major groups of eukaryotic single-stranded DNA lawski.. P.B. L. Quemin.. (2016) The RNA world at thirty: a look back with Turner.. Poulos. Jensen. M. G. T. A. Bioanalysis 8:867– comprehensive dsRNA sequencing method for intracellular 870.. and Blumberg. Y. evolution of core photosystem II genes in marine cyano- Roux.. C. Robert. Vaqué. E. 16 BERLINER ET AL. bacterial viruses and their hosts. Nat Rev Microbiol 9:99–108. (1973) A new evolutionary law. M. B. S. L.. Nature 398:441–443. Qin. (2005) The NASA Astro- Roossinck. (2006) Prevalence and viruses. and at 01/10/18.E.. Lee.J.A. Holmes.A.. Horn. Roberto. M. Takemura..B. Lin.. D.. Nature 540:539–543. L. C. T. S... Bettarel. Snyder. Spuhler. B.... J. K.. Adams. N... Schmidt. R. (2011) Exploring the viral world (1976) DNA related to the transforming gene(s) of avian through metagenomics. credible Microbes. M.M. Sime-Ngando....M... (2001) archaeal virology: expanding viral diversity. M. Davison. (2009) Viruses: a vast reservoir of genetic diversity S.W. S.. doi:10..I. K. (2005) producers: the first major transitions leading to life. S. McDermott. Daims. (2016) Redefining Weinbauer. Nature 437:356–361.. Johnson. (2017) Consensus statement: virus taxonomy in Natl Acad Sci USA 113:2478–2483. M. F. Proc Natl Acad Sci USA 101:7716–7720...J. June 22–24. M. R. (2004) Viruses and the Evolution of Life.E.-H. Willits. J Virol 89: Stedman. R.. and Vogt.R. and Chisholm. D. M. Environ Microbiol 13: from Mimivirus. Villarreal.B. X. Retrovirology 6.M. E.A. Wiedenheft. Chen. 2429.. Forterre. J. J. C. D. and archaea with a unique architecture among DNA viruses. E. (2014) Highly efficient self. Robertson. P.... (2007) Marine viruses—major players in the global Searson. 2004.3847/0004-637X/829/2/121. M. Chen. P...B. Li. meta-omics era. (2016) FLDS: a through chip-based optical detection. Lee.. D. D. D.. T. (2017) Giant Villarreal. Gorbalenya. G. and Claverie.. Hull. Simmonds.M. Vaulot...C. J.. Caputi. E....F. CA.-P. the age of metagenomics. B. For personal use only.-i.L. Annu Rev Virol Roossinck. Snyder. P.. Wang. Sullivan..M. P. S... (2008) Redefining viruses: lessons in hypersaline Lake Retba. Thompson. and DeFilippis. J. J. (2005) Viruses in the sea. Gasol.K. Chem Biol 21:238–245. Abergel. L. M. E. E. Krupovič. J.-S. and Forterre...J. M. Tian. and Nunoura. virus genes in DNA virus and host genomes. Microbes Environ 31:33–40. and Smith.E.V. K. Raoult. Sullivan. (2011) The good viruses: viral mutualistic biology Institute Virus Focus Group workshop and field trip symbioses.B. (1997) From replicators to re- Ruardij. Roossinck.X. X. J. J.. Nature 537:689–693.2-megabase genome sequence of Mimivirus. J Virol 74:7079–7084. and Chao. (2016) Ecogenomics and driver of global processes. Stehelin.. Sparks. D. doi:10. S. E. Science A. to Mono and Mammoth Lakes. able morphological diversity of viruses and virus-like par. Hand.-J.. The 1. and Breitbart. (2000) A hypothesis for Shi. M. Delwart.1038/ncomms3700. Suttle. V. M. E. Desmond. Carstens..P... (2016) A virus of hyperthermophilic C.A. Poulain... Veldhuis. Varmus. Ortega. Lara. L. Brister. craft.-C. Forterre. M. Cell 113:141. DNA viruses as the origin of eukaryotic replication proteins. Stedman. J.J.. Princeton.J. Tara Oceans Coordinators. T. P.. H. K. Lucas. P....-D. L. and 260:170–173. Duhaime. F.G. Li. Loy.. A. J. J Mol Evol 83:169–175. Varsani.. and Zhang. Dutilh. J. Chaffron. J Theor Modeling the bloom dynamics of the polymorphic phyto. M. karyotic nucleus.. (2004) Ecology of prokaryotic viruses. Bowler. Breitbart. (2016) Probing for evidence of Downloaded by Gothenburg University Library from online.. (2017) Modelling plankton ecosystems in the replicating RNA enzymes. N. Van Valen. (2011) Diversity of virus–host systems Raoult. Bergeron... N. (2016) Single-virus analysis Urayama. G. Bishop. Koonin. Ibarbalz.C. Bolduc. Rosario..C. (2001) Poxviruses and the origin of the eu- Harmful Algae 4:941–963.M.. Kru- 306:1344–1350... and Joyce. Sabanadzovic.. Theory 1:1–30.F. Renesto... and Young. P. Kuhn. Enault. sarcoma viruses is present in normal avian DNA. Robin. Harrach... M. Dimier. .N. K. K.W. N. Krupovič. Senegal. Sci USA 98:13341–13345.J. (2016) Virus: An Illustrated Guide to 101 In. F. P.E. (2004) J.. Lindell. Evolutionary Vierheilig.. ASM viruses with an expanded complement of translation system Press.. Wagner. S.H. M.. Science 356:82–85.B.. B... B.. Pesant. M.A. Nat Rev Microbiol 6:315–319. P. D’Alelio. D. and Deustua. M. Kandels-Lewis. M. Audic. 1956–1972.R. Washington.. Benk} o. Ivanova. Douglas. C. Tucker. bacteria! Viruses make trobiology 5:441–443. Are we ready? Mar Genomics 32:1–17.. E. Cruaud. E. Nature Roux. and Young. Acinas... J. d’Alcalà. Stedman. Y. Rensen..M. M.. S. As- Roossinck. M. S.E. J.. Buttigieg. Solonenko. components. D.. C. P. S. M. Sankaran. E. RNA virus. L. van der Vlugt.R. Sullivan. Schulz.A. Suttle. Nat Rev Microbiol 15:161–168. D.G. S. E. A. and Prangishvili..A. (2015) Move over.. C.R. Co- ticles in hot terrestrial environments..P.P. H.. S.D. J. S. and Breitbart.. domains of life.M.P. (2015) Deep recombination: RNA and ssDNA 6532–6535. Mochizuki. Suttle.J.K... M. J. ocean viruses. (1999) Prisoner’s dilemma in an its author.. M. Suzan.B. McGrath. Brum.L.. T.S.E. A.. M. W... E. S. C..1186/ and potential biogeochemical impacts of globally abundant 1742-4690-6-S2-I7. Lefkowitz. Cao. D. S.M.B.. (2013) Chimeric viruses blur the borders be. M. Proc Natl Acad 369–378. M. F. plumes on Europa with HST/STIS. plankter Phaeocystis globosa: impact of grazers and viruses. Proc Zerbini.T. J.. Astrophys J 829. and Woyke.. Gribaldo. and Iudicone. J Mol Evol 52:419–425.

J. ssDNA ¼ single-stranded DNA Yozwiak. (2006) Modelled and measured encing.J. A. and DeRisi.K. Stedman munities. TEM ¼ transmission electron microscope A.G. J Bacteriol 171: CRISPRs ¼ Clustered Regularly Interspersed 93–98. and Allen. M.V. and Banfield. M. L. Skewes-Cox. (2016) Biology dsDNA ¼ double-stranded DNA and applications of CRISPR systems: harnessing nature’s HGT ¼ horizontal gene transfer toolbox for genome engineering.. Syst Appl Microbiol 16:609–628. Stenglein. nome maintenance. (2016) Quantification of virus of Viruses particles using nanopore-based resistive-pulse sensing tech. Accepted 20 July 2017 Wommack.2016.R.1371/journal. PLoS One 8. C. D..3389/fmicb. and Brown. Yu. Cell 164:29–44... Palindromic Repeats Wright. T. For personal use only.B. Wilmes. J. S. P.pntd dynamics of viruses in Arctic winter sea-ice brines. L..W.. Box 751 Curr Top Microbiol Immunol 328:1–42. Slater. doi:10. (1989) Isola. C.. their plasmids and their viruses in structure and function of aquatic food webs.L.E. G. Woese.O. W. (1993) ent cycles in the sea viruses play critical roles in the Screening for Sulfolobales. Simmons. Microbiol 8:1115–1121.1371/journal SEM ¼ scanning electron microscope .F. Portland. and Colwell. Hain. Abbreviations Used Wood. Takaki. doi:10. (2002) On the evolution of cells. and Takai. J. R. and Kristjansson. I. C..J. OR 97207-0751 Witzany. J. (2000) Virioplankton: viruses in aquatic ecosystems. NAIViFoG ¼ NASA Astrobiology Institute Virus K.L. Microbiol Mol Biol Rev 64: 69–114.R. Kletzin. P.L. Biology Department Wilson. Lanzendörfer. and Yamamoto. M. J.. Front Microbiol 7.. ICTV ¼ International Committee on Taxonomy Yang.A. K.A. H. and Doudna. 781–788. (2013) Metagenomic analysis of viral communities in Focus Group (hado)pelagic sediments. A. M. E-mail: kstedman@pdx. Van. Nuñez. Holz. Janekovic. C. (2010) Experimental evolution and characterization of Thermus bacteriophages. Y..H.0001485.D.J.W.01500. Harris.W. (2012) Virus identification VLPs ¼ virus-like particles in unknown tropical febrile illness cases using deep sequ- . (2006) Isolation Wichman. Kenneth M. M. and Konisky. ASTROVIROLOGY: VIRUSES IN THE UNIVERSE 17 Wells. J.0057271. Biosemiotics 1:191–206... M.pone.liebertpub.. E.L.X..E.... A. Proc Natl Acad Submitted 10 January 2017 Sci USA 99:8742–8747. V.. Balmaseda. T. J. P.. Wilhelm. Arch Virol of viruses: Microviridae as a model system. FEMS Microbiol Rev 33:109– at 01/10/18...R. M. Philos Trans R 151:663–679. Environ . PLoS Negl Trop Dis 6.. Eitoku. Nunoura. and Ackermann. Denef.A. ISS ¼ International Space Station niques. (1999) Viruses and nutri. and Deming. W. W. Bioscience 49: Icelandic solfataras. N. J. (2009) The Portland State University Phycodnaviridae: the story of how tiny giants rule the world. doi:10. and Suttle. (2008) The viral origins of telomeres and telo- merases and their important role in eukaryogenesis and ge.. Address correspondence to: (2009) The dynamic genetic repertoire of microbial com.. Whitman.. ACV ¼ Aeropyrum coil-shaped virus tion and characterization of an archaebacterial virus-like AMG ¼ auxiliary metabolic genes particle from Methanococcus voltae A3. Etten. Schleper. S. NAI ¼ NASA Astrobiology Institute Yoshida.K. H. Soc Lond B Biol Sci 365:2495–2501.. J. Downloaded by Gothenburg University Library from online.