ASTROBIOLOGY Volume 13, Number 8, 2013 Mary Ann Liebert, Inc. DOI: 10.1089/ast.2012.

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Essays

The Quest for Extraterrestrial Life: What About the Viruses?

Dale Warren Grifn

Abstract

Recently, viruses have been recognized as the most numerous entities and the primary drivers of evolution on Earth. Historically, viruses have been mostly ignored in the eld of astrobiology due to the view that they are not alive in the classical sense and if encountered would not present risk due to their host-specic nature. What we currently know of viruses is that we are most likely to encounter them on other life-bearing planets; that while some are exquisitely host-specic, many viruses can utilize hundreds of different host species; that viruses are known to exist in our planets most extreme environments; and that while many do not survive long outside their hosts, some can survive for extended periods, especially in the cold. In our quest for extraterrestrial life, we should be looking for viruses; and while any encountered may pose no risk, the possibility of an encounter with a virus capable of accessing multiple cell types exists, and any prospective contact with such an organism should be treated accordingly. Key Words: AstrobiologyMicrobiologyOrigin of lifePathogensVirus. Astrobiology 13, 774783.

The study of viruses has not been applied in Astrobiology to the extent of other disciplines. This is despite viruses outnumbering all other organisms on earth by at least an order of magnitude. (Stedman and Blumberg, 2008)

Viruses: What Are They?

iruses are the most numerous entities on Earth, with an estimated *1030 residing in our oceanic water column and *1031 for the total planetary population (Breitbart and Rohwer, 2005; Suttle, 2005; Youle et al., 2012). Suttle (2005) estimated that if you put the population of viruses that exist in the water column of our oceans next to each other, one after the other in a straight line, and you anchored one end of that line to the surface of Earth, the resulting viral string would extend out into space *10 million light years. The typical number of viruses, most of which are bacteriophages (viruses whose hosts are bacteria), ranges from *106 to 108 per milliliter of seawater, and in near-shore marine sediments and topsoils the number of viruses is approximately 108 per cubic centimeter or gram (Breitbart and Rohwer, 2005; Suttle, 2005; Srinivasiah et al., 2008). Lower concentrations of viruses are known to exist in subsurface environments. In regard to diversity, the number of viral genotypes in a kilogram of marine sediment has been estimated to be as high as 106 (Breitbart and Rohwer, 2005; Edwards and Rohwer, 2005). Viruses are found wherever cellular life exists, to include those that reside in the most

inhospitable environments (i.e., deep sea hydrothermal vents, hot springs, cold water, snow, and ice) (Kaminskyy and Zhivotovsky, 2010). Viruses are composed of a genome surrounded by a protective genome-encoded protein shell known as a capsid. In addition to the capsid, some viruses contain a lipid envelope that contains viral and/or host-derived proteins. There are also naked viruses or viroids and the recently discovered virophage (La Scola et al., 2008). Most viruses range in size from 20 to 300 nm in contrast to bacteria that typically range from 500 to 1500 nm (Fig. 1) (Nayak, 2011). For example, Poliovirus, one of the members of the common human enterovirus group, is typically in the size range of 30 nm, but some viruses are bacterial in size. The Mimivirus has a diameter of *400 nm, and the lamentous Ebola virus ranges from *900 to 14,000 nm in length (Geisbert and Jahrling, 1995; La Scola et al., 2003). Viruses grouped by types of genomic nucleic acid are listed in Table 1 and include genomes composed of RNA or DNA variants. Currently in the eld of viral taxonomy, there are 6 recognized orders comprising 22 families, 109 genera, and 549 species. In addition, there are 65 viral families that are not currently classied into orders that contain 265 genera and 1734 species (ICTV, 2009).

U.S. Geological Survey, St. Petersburg, Florida.

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FIG. 1. Comparative sizes of select microorganisms and genomic DNA. [Figure courtesy of Reynolds, K.A. and Pepper, I.L. (2000) Microorganisms in the environment. Chapter 2, Figure 2.2, p 11, published in Environmental Microbiology, edited by R.M. Maier, I.L. Pepper, and C.P. Gerba, ISBN 0-12497570-4, copyright Elsevier B.V.] Color graphics available online at www.liebertonline.com/ast

The question of whether viruses can be classied as alive is one that has been debated since their discovery (Beijerinck, 1899; Villarreal, 2004; Moreira and Lopez-Garcia, 2009). In Villarreals article titled Are Viruses Alive? he points out how they have been viewed as inert chemicals or, due their dependence on host cells for replication, living a kind of borrowed life (Villarreal, 2004). Viruses dock with a host cell membrane and use membrane fusion to trick the host cell to internalize it or inject their genomes through their hosts cell wall/membrane. Once the virus has gained entry into its host, it can enter a state of coexistence or pirate host systems for the purposes of replication (parasitic or lethal infections). The production of more copies of oneself or prodigy is a hallmark of life, but the requirement of an obligate host confounds the debate of whether viruses are alive (Moreira and Lopez-Garcia, 2009). While most regard viruses as pathogenic in nature, many virus-host relationships are asymptomatic in nature. In fact, viruses can shuttle benecial genes (i.e., antibiotic resistance, virulence, photosynthetic, etc.) to a host that provide the host with enhanced ability to compete in its environment (Mann et al., 2003; Roossinck, 2011). Regardless of ones view as to whether a virus is alive or not, their ability to move genes between hosts has driven the evolution of life on this planet (Villarreal, 2004; Forterre, 2010).

Viral Host Relationships Speculation on the origin of viruses has included the hypothesis that viruses occurred before the more complex prokaryotes based on the existence of widespread genes that are only found within viral genomes (virus hallmark genes, i.e., reverse transcriptase, RNA-dependent RNA polymerase, jelly-roll capsid protein, and rolling-circle replication endonuclease) (Koonin et al., 2006; Forterre, 2013). Other hypotheses have included that viruses are escaped genes or degenerative unicellular organisms that lost genetic capability to replicate on their own (Bubanovic et al., 2005; Villarreal, 2005). While the origin of viruses is still an unresolved issue [to date there is no viral fossil record in comparison to that observed with cellular life (Laidler and Stedman, 2010; Orange et al., 2011)], the most commonly agreed point of view is that viruses are ancient and polyphyletic, and evolved independently of host replication systems (Villarreal, 2005; Moreira and Lopez-Garcia, 2009; Forterre, 2010). In nature, viral-host relationships can be detrimental or benecial to the host. An example of a benecial transfer of genetic material to a host by viruses is the bacteriophage genes that encode Shiga-like exotoxin (Imamovic et al., 2009). This bacteriophage-mediated genetic transfer is believed to benet the bacterial host by enabling compromised host cells

776 Table 1. Viral Groups Based on Genome Nucleic Acid Type Nucleic acid RNA viruses Single negative stranded Single positive stranded Host Plants Invertebrates Vertebrates Bacteria Fungi Plants Invertebrates Vertebrates Bacteria Fungi Plants Invertebrates Vertebrates Fungi Invertebrates Vertebrates Bacteria Plants Invertebrates Vertebrates Bacteria Amoeba, Algae, Fungi Invertebrates Vertebrates Plants Vertebrates Examples, Familycommon name

GRIFFIN

Double stranded

Single positive stranded reverse transcriptase DNA viruses Single stranded

BunyaviridaeTomato spotted wilt virus RhabdoviridaeY-organ virus (crab virus) FiloviridaeEbola virus LeviviridaeEnterobacteriophage MS2 BarnaviridaeMushroom virus X BromoviridaeTobacco streak virus TetraviridaeNudaurelia beta virus (moths and butteries) PicornaviridaePoliovirus CystoviridaePseudomonas phage F6 ChrysoviridaePenicillium brevicompactum virus PartitiviridaeWhite clover crytic virus 1 BirnaviridaeDrosophila X virus ReoviridaeRotavirus PseudoviridaeSaccharomyces cerevisiae Ty1 virus MetaviridaeAscaris lumbricoides Tas virus RetroviridaeHIV InoviridaeVibrio phage CTX GeminiviridaeBeet curly top virus ParvoviridaeAedes aegypti densovirus MyoviridaeEnterobactriophage T4 MimiviridaeAcanthamoeba polyphaga mimivirus IridoviridaeTiger frog virus AdenoviridaeHuman Adenovirus species AG CaulimoviridaeCauliower mosaic virus HepadnaviridaeHepatitis B virus

Double stranded

Double strandedreverse transcriptase

to release a toxin that is inhibitory to predators (protest grazers) or the bacterias host (triggered by immune response) (Imamovic et al., 2009; Lainhart et al., 2009). Other examples of bacteriophage-mediated virulence conversion are bacteriophages that impart the capability of certain prokaryote species to produce toxins (i.e., cholera, diphtheria, and staphylococcal) and antibiotics (Freeman, 1951; Betley and Mekalanos, 1985; Waldor and Mekalanos, 1996). In aquatic environments, bacteriophages have been shown to move photosynthetic genes and thus sustain photosynthetic capability in phototrophs (Mann et al., 2003). An infected eukaryotic cell committing apoptosis (a prime example of cellular altruism) is an example of a detrimental relationship. Some detrimental infections may be asymptomatic and not produce symptoms. Asymptomatic infections may result in the assimilation of the viral genome within its host (termed lysogeny for bacteriophage infections of this type) followed by a latent or dormant phase. After a period of dormancy, latent or asymptomatic infections can enter a lytic stage that is typically triggered by some form of host cell stress ( Jiang and Paul, 1996; Williamson et al., 2002). The lytic stage results in rapid reproduction of the virus ending with the release of the replicated viruses and often the destruction of the host cell. The number of released viruses (known as burst size) can range from a few to thousands (Ellis and Delbruck, 1939; Bailey et al., 2004; Choi et al., 2010; Minor, 2011). In regard to host specicity, viruses can be grouped into two classes: those that only infect a given host or host tissue

type (specic viruses) and those that can infect more than one host (generalized viruses). Polio, mumps, and the dengue viruses are examples that only cause disease in primates. Bacteriophages like the F-specic bacteriophage f1 only infect hosts that produce pili, which are bacterial cell surface protein appendages used for conjugation ( Jacobson, 1972). Bacteriophages with broad host ranges have been shown to infect many species within a given genus and in some instances to be able to infect multiple genera ( Jensen et al., 1998; Evans et al., 2010). Multi-host eukaryote viruses include members of the caliciviruses that are known to infect both marine and terrestrial mammals. Researchers have estimated that an infected 35-ton gray whale could shed *1013 caliciviruses daily (which could survive > 2 weeks at 15C) and hypothesized that these types of oceanic reservoirs could serve as inoculum for terrestrial hosts (Smith et al., 1998). The Avian inuenza virus is capable of infecting a number of vertebrate hosts, which to date have included humans, pigs, horses, and birds (Naffakh et al., 2008). The cucumber mosaic viruses (vector-borne by aphids) have a host range of over 800 species of plants (Palukaitis et al., 1992). The benet of host specicity is nding a niche where adaptation to evolving host defense systems is limited to a few or one coevolving genome (Elena et al., 2009). The disadvantage of host specicity is the probability that a newly replicated virus can nd a host upon cellular release. The benet of host generalization is the availability of many hosts, which thus increases the likelihood that a newly replicated virus can nd a receptive cell to infect. The

ASTROVIROLOGY disadvantage is intracellular competition with co-infecting viruses and adapting to the evolution of multiple host defense systems (Elena et al., 2009). While experiments utilizing bacteria, plant, and mammalian viruses that typically infect a single host demonstrated lost tness (a lowered ability to efciently infect) when forced to adapt to an alternate host, viruses such as the Foot and Mouth Disease Virus have demonstrated the ability to acquire new hosts without losing original host tness (Elena et al., 2009). Earths viruses, whether they have lytic or lysogenic host relationships, must survive the extracellular environment to nd new host cells. Based on our understanding of cellular life on Earth and the driving role that viruses have played in evolution, it should be expected that, if viable extraterrestrial cellular life were discovered, viruses or virus-like entities would also be present. If we discover a planet that has suffered cellular extinction, it is possible that the last viable entity on the planet was viral or viral-like. If this is the case and viruses are shed by the last remaining cellular hosts into various extracellular environments, what is the likelihood that these viral entities would remain viable for any extended period of time? What do we know about extracellular viral survival on Earth? Virus Survival and Life in Extreme Environments Table 2 lists the results of virus survival experiments that were obtained for various extracellular environments that include water, soil, and space. Unlike their metabolically active hosts, viruses are not metabolically active outside the host cell, do not require osmotic maintenance to remain viable, and thus are ideally suited for long-term survival. In marine surface water, UV-induced nucleic acid damage was identied as a primary contributor to viral inactivation in addition to losses driven by particulates and heat-labile substances in the water column (Noble and Fuhrman, 1997). Gerba and Schaiberger (1975) had previously reported a reduction in viral infectivity due to the association of viruses with marine particulate matter but noted that this association resulted in an increase in virus survival. While UV radiation can kill viruses and host cells, viruses carrying matched or compatible genes to those damaged in their prospective host can infect and thus restore host function (Villarreal, 2004; Mann et al., 2005). UV-damaged viruses are capable of injecting their genomes into host cells, and replication of the virus can be restored if infection by multiple viruses results in an equivalent undamaged viral genome. Villarreal (2004) stated that Viruses are the only known biological entity with this kind of phoenix phenotypethe capacity to rise from their own ashes. While elevated temperature can be lethal to many viruses, there are linages that evolved to tolerate extreme heat environments such as those found in hot springs and around marine geothermal vents (Anderson et al., 2011; YoshidaTakashima et al., 2012). In two Yellowstone National Park hot springs, where temperatures and pH ranged from 75C to 93C and 1.5 to 6.5, respectively, 12 different morphotypes of viable archaeal viruses were reported (Rachel et al., 2002). In a study conducted in Italian volcanic acidic (pH 1.5) hot springs where temperatures ranged from 87C to 93C, ve different morphotypes of viable archaeal viruses (determined via enrichment assays and transmission electron microscopy)

777 were reported (Haring et al., 2005). In addition to those viruses that have evolved to thrive in extreme heat environments, likewise there are those known to have evolved to tolerate extreme cold environments. At an internal depth of 0.51.5 cm in Artic sea ice, where host activity was greatest, virus concentrations in melt ranged from 9.0 106 to 1.3 108 mL - 1,which was up to 100-fold higher than that observed in the underlying water column (Maranger et al., 1994). Viable viruses were also observed at a temperature of - 12C in sea-ice brine (Wells and Deming, 2006). In Antarctica, viruses were observed associated with moss that typically infect dicotyledonous plants, which raises questions of host specicity and range in this coldweather environment (Polischuk et al., 2007). Extreme cold or cryogenic storage is widely used to preserve microorganisms. Stocks of Inuenza viruses as old as 40 years that were cryogenically stored ( - 70C) demonstrated little loss of viability (Merrill et al., 2008). With regard to long-term virus survival, Hollings and Stone (1970) demonstrated that at room-temperature storage 57 lyophilized stocks of plant viruses out of 74 remained viable after 1 year, and 19 of 74 remained viable after 10 years. Priscu et al. (2006) argued for an improved understanding of life in ice on Earth to enhance our search for life on other icy worlds. There are other instances (prophage in dormant or preserved prokaryotes) yet unexplored where viruses might survive considerable periods of time. Recently, viable bacteria and fungi were cultured from desert dust samples (Saharan desert dust that fell onto ships sailing in the Atlantic) collected in 1838 and given to Charles Darwin (Gorbushina et al., 2007). Could these bacteria and fungi that were dormant for over 160 years harbor inducible viruses (Gorbushina et al., 2007)? Likewise, what of the potential presence of prophage in a bacterium reported to have been revived from a 25- to 40-million-year-old amber sample (Cano and Borucki, 1995)? It should be emphasized that our current level of understanding of bacterial survival is limited by our inability to culture the majority of these organisms, and the eld of virology is immature in comparison. Issues such as long-term virus survival are hampered by our current lack of culturable hosts. Does our understanding of virus survival and viral host specicity translate well to what we may encounter on other planets? Cave Exiguus Creatura (Beware of the Tiny Creature) As viruses are the most numerous entities on Earth, it is likely that we will encounter them in extraterrestrial habitats that harbor cellular life. Whether cellular life is sparse or not, the use of viruses or viral constituents as biomarkers may aid our efforts to identify life or understand how life originated on extraterrestrial bodies ( Jalasvuori et al., 2009). From our current state of knowledge of viruses and cellular specicity, the potential threat of extraterrestrial viruses to life on our planet via sample return missions or to astronauts is viewed with questionable risk. In regard to planned sample return missions, the current debate on an acceptable particle escape threshold that is based on the estimated lower size limits of living cells (*50 nm) should be oriented to the potential threat that may come from the lower size range of our known viruses, many of which exist in the range of < 50 nm (ESF/ESSC, 2012). One of the arguments in support

Table 2. Virus Survival Host Birds/mammals Birds/mammals Birds/mammals Birds/mammals Birds/mammals Birds/mammals Birds/mammals Mesh bags of chicken manure, litter, feed, and the allantoic spike sealed in vials Banknotes Methanogenic landll leachate/ water Fresh and marine surface waters Mihai et al., 2011 Domanska-Blicharz et al., 2010 Davidson et al., 2010 Davidson et al., 2010 Graiver et al., 2009 Thomas et al., 2008 Guan et al., 2009 Survival environment Survival time or inuences on infectivity Reference

Virus

Avian inuenza H5N1

Avian inuenza H5N1 Avian inuenza H9N2

12 days at 2235C 20 days at 4C > 60 days at 4C 1 week at pH 5.0, 3 weeks at pH 7.0, 20C

Avian inuenza H9N2

Distilled water Allantoic uid diluted in pH buffer/phosphate-buffered saline Allantoic uid

Avian inuenza H6N2

Inuenza A

Avian inuenza H6N2 and Newcastle disease virus Birds/mammals Mammals Mammals Mammals

Venezuelan equine encephalomyelitis (VEE) and Sindbis viruses (SV) Hepatitis C virus

Distilled deionized water (DD) at 4C, 21C, and 30C and tap water (TW) at 21C Dried samples on stainless steel discs Syringe blood Farm slurry

Relative to 37.0C, 18 times longer at 20C, and 70 times longer at 4C Elevated temperature and non-neutral pH = decreased survival. Landll survival rates of 30600 days 3 days without respiratory mucus 17 days with respiratory mucus 5065C bag specimens < 7 days, vial control > 21 days 1328C bag specimens < 21 days, vial control > 21 days DD at 4C = 21 days. At 21C and 30C survival *.13 log10 day - 1 less over the same time period 7 days at room temperature 63 days at 37C = 1 h at 55C, many weeks at 5C

Fitzgibbon and Sagripanti, 2008 Doerrbecker et al., 2011 Paintsil et al., 2010 Botner and Belsham, 2012

778 Mammals Mammals Mammals Swine feces and urine Carcasses and excretions onto nearby soil Distilled water (DI), articial marine (AM), ltered marine (FM), and unltered seawater (UM) Mammals Arid riverbed soil amended with DI and diluted sewage efuent

Hepatitis C virus Foot and mouth disease virus, swine fever virus, bovine viral diarrhea virus, swine inuenza virus Swine fever virus

Weesendorp et al., 2008 Henning et al., 2005 Wetz et al., 2004

Rabbit hemorrhagic disease virus Poliovirus

Poliovirus

-life (survival of the starting population) of 24 days at 5C and 13 h at 30C 3 months in carcasses and 1 month for excreted viruses Days to survival of only 1% of the starting titer at 22C = 16.0 for DI, 18.2 for AM, 18.2 for FM, and 4.4 for UM Days to survival of only 1% of the starting titer at 30C = 13.0 for DI, 7.4 for AM, 6.8 for FM, and 4.0 for UM At 1C > 70 days under aerobic and anaerobic conditions. At 23C and 37C decreases in survival time or surviving % of spikes

Hurst et al., 1980

(continued)

Table 2. (Continued) Host Mammals Mammals Clothing Mineral water Biziagos et al., 1988 Gerba and Kennedy, 2007 Survival environment Survival time or inuences on infectivity Reference

Virus

Poliovirus and hepatitis A virus (HAV)

Adenovirus, rotavirus, and hepatitis A virus

Viral hemorrhagic septicemia virus Tobacco mosaic virus Plant Bacteria Simulated interstellar w/ *250 equivalent years of irradiation Spaceightsduration 1.5528 h, radiation dosage 0.6 mrad to 36 rad Groundwater

Fish

Challenged Pacic sardines

At 4C > 1 year, at room temperature (2026C) Poliovirus < 300 days, HAV < 360 days Washing with detergent and standard household dryer conditions = survival of 18% of the starting titer, with the addition of bleach = survival of 0.01% of the starting titer 66.7% sh mortality at 13C and 6.7% sh mortality at 20C 82% survival rate Koike et al., 1992

Arkush et al., 2006

Bacteriophage (Escherichia coli prophage)

Parfenov and Lukin, 1973

Bacteriophage MS2 and PRD1

Bacteria

Yahya et al., 1993

779 Bacteria Distilled deionized water (DD) at 4C, 21C, and 30C and tap water (TW) at 21C Bacteria Bacteria Bacteria Seawater Articial seawater Leaf surfaces in northern Italy

Bacteriophage MS2

Fitzgibbon and Sagripanti, 2008

Bacteriophage T2

Gerba and Schaiberger, 1975 Zaccardelli et al., 1992 Noble and Fuhrman, 1997

Bacteriophage (Xanthomonas campestris phage) Marine bacteriophage (4 isolated host/phage systems)

Prophage production rates relative to control experiments ranged from 0 (1 of 12 ights) to 4.6 times greater (11 of 12 ights averaged 2.0 times greater) At 7C phage were stable for 80 days. At 10C and 23C decreased survival rates with PRD1 inactivation rates lower than MS2 for most water samples MS2 *3 slower inactivation rates at these temperatures in comparison to VEE and SV (see Fitzgibbon and Sagripanti, 2008, reference above in birds/mammals host). TW at 21C, inactivation rates twice that observed at 21C with DD H2O 5 days incubation at 24C, 60 times greater survival in the presence of clay than without 5 days on peach leaves in an orchard during the summer Relative to local sunlight and water column exposure = native (coastal California) phage decay rates of 4.17.2% h - 1 Non-native (North Sea) phage decay rates of 6.6 to 11.1% h - 1

780 of an astronaut low-risk scenario (or return via astronaut contamination) is that life may have been transported and seeded onto habitable planets and moons from a biologically rich planet (like Earth) via impact event ejecta (lithopanspermia) (Nicholson et al., 2005) and thus when encountered will not truly be extraterrestrial or foreign in nature. Although this type of extraterrestrial encounter may indeed pose minimal risk, it could be argued that there is risk through long-term separation of populations and/or lack of immunity (even if restricted to prokaryote populations) much like what is seen on the human scale with travelers diarrhea, the spread of smallpox by Europeans into Native American populations, and the introduction of the Myxoma virus into rabbit populations in Australia (Fenner, 1959; Jones, 2006). Another possibility is that life we may encounter on other planets or moons evolved independently of life on Earth. The low-risk argument here is that any viruses that infect organisms we encounter have specicity to their hosts and thus will not be able to infect organisms of Earth origin. Although host specicity is a trademark of Earths viruses, the existence of generalized viruses like the cucumber mosaic virus, which can infect many different hosts within the kingdom Plantae, is well documented. Further, there is genetic evidence that some vertebrate viruses may have evolved from an ancient incidental infection of a vertebrate by a plant virus (Gibbs and Weiller, 1999). It may be that life on other planets evolved so differently from the manner in which it evolved on Earth that an extraterrestrial virus could not gain access to a terran cell, but it is also as likely that life evolved in a very similar manner as it evolved on Earth and that viral penetration into a terran cell is not insurmountable. There are several hypothetical scenarios where an extraterrestrial virus capable of infecting various cell types may evolve. One hypothesis in regard to the evolution of life on Earth is the clay hypothesis, which asserts that selfreplicating clays and associated organic molecules provided templates for primitive organic synthesis (Cairns-Smith, 1966). In this hypothesis, biochemistry evolved from geochemistry due to natural selective environmental pressures on inorganics (Cairns-Smith, 2005). Clay structural environments can provide a shielded cellular-like environment for nucleic acid (i.e., UV shielding) and cellular evolution, and this potential mode of life evolution may have occurred on other planets or extraterrestrial bodies (Cairns-Smith and Hartman, 1986; Holm et al., 1992; Scappini et al., 2004). It has been hypothesized, based on the existence of widespread genes only found within viral genomes, that a virus world may have evolved from inorganic precellular compartments and coevolved with emerging cellular life (Koonin et al., 2006). In this scenario, it is possible that extraterrestrial viruses at an early evolutionary stage of cellular coevolution may not have yet acquired host specicity and, if encountered, are capable of infecting cellular life of Earth origin. Another scenario that could result in an encounter with generalized viruses is a situation where viruses may evolve in an end-life phase of a dying world. Imagine if Earth, a biologically rich planet harboring diverse viral communities, was to slowly undergo a loss of cellular life to a point of extinction. It is not unimaginable that viral evolution in this setting would favor generalized viruses as available host numbers decreased. Currently on Earth, viral specicity

GRIFFIN outside pathogenic relationships (and even here one can argue host benets) is a means by which advantageous genes can be quickly shuttled to related cells giving the community advantages in competitive environments. From the perspective of a competing cellular linage, sharing advantageous genes with potential adversaries could be detrimental; thus viral host specicity is a valuable asset. While host specicity is advantageous in a biologically prime environment, it would not be on a dying world. Due to a dwindling of available resources, the ability of previously adversarial or competitive hosts to enter a state of altruism and share genetic information (i.e., ability to metabolize different nutrients or adapt to potentially harmful physical stressors such as temperature change) would become paramount. Altruism in the microbial world under low-nutrient conditions has been demonstrated as an advantageous strategy (Blower et al., 2012). Viruses and their ability to facilitate rapid genetic exchange can be viewed as the architects of altruism on our planet. An altruistic state on a dying planet may result in the last viable entity on the planet being an extremely versatile virus. In this scenario, which may be similar to what occurred on Mars if cellular life was at one time abundant and subsequently signicantly reduced in number or lost, it is possible that a generalized virus evolved and is currently extant or preserved in ice. What may present an obstacle to identifying extraterrestrial microbial life and an understanding of its potential risks to Earth is our perceptions of life and its origins. It has been only recently that the profuse nature of viruses or the role that they have played in driving the evolution of all organisms on our planet has been recognized. Historically, viruses have been dismissed as important entities in regard to evolution and planetary exploration due in part to the fact that most of the rst identied and described viruses were hostspecic pathogens. What we know of viruses at this point is that we are most likely to encounter them on other lifebearing planets and that, yes, they tend to be host-specic, but the existence of multi-host viruses is well known. Additionally, viruses are known to have adapted to extreme environments, and while most do not survive long outside the host cell, prolonged survival in cold-temperature settings has been documented. We should be looking for viruses in our quest for extraterrestrial life, and it may be that viruses pose no risk to human planetary exploration. However, the possibility of risk exists, and our potential contact with them should be treated accordingly. Acknowledgments I would like to thank Dr. Hon Ip of the USGS National Wildlife Health Center located in Madison, Wisconsin, for reviewing the manuscript and offering some creative insight. References
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Address correspondence to: Dale Warren Grifn Environmental/Public Health Microbiologist U.S. Geological Survey 600 4th Street South St. Petersburg, FL 33701 E-mail: dgrifn@usgs.gov Submitted 21 December 2012 Accepted 20 April 2013