The Quest for Extraterrestrial Life: What About the Viruses?

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 field 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-specific 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-specific, many viruses can utilize hundreds of different host species; that viruses are known to exist in our planet's 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: Astrobiology—Microbiology—Origin of life—Pathogens—Virus. Astrobiology 13, 774–783.

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?

V 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 filamentous 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 field 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 classified into orders that contain 265 genera and 1734 species (ICTV, 2009).

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 0-12-497570-4, copyright Elsevier B.V.] Color graphics available online at www.liebertonline.com/ast

Table 1.

Viral Groups Based on Genome Nucleic Acid Type

Nucleic acid	Host	Examples, Family—common name
RNA viruses
Single negative stranded	Plants	Bunyaviridae—Tomato spotted wilt virus
	Invertebrates	Rhabdoviridae—Y-organ virus (crab virus)
	Vertebrates	Filoviridae—Ebola virus
Single positive stranded	Bacteria	Leviviridae—Enterobacteriophage MS2
	Fungi	Barnaviridae—Mushroom virus X
	Plants	Bromoviridae—Tobacco streak virus
	Invertebrates	Tetraviridae—Nudaurelia beta virus (moths and butterflies)
	Vertebrates	Picornaviridae—Poliovirus
Double stranded	Bacteria	Cystoviridae—Pseudomonas phage Φ6
	Fungi	Chrysoviridae—Penicillium brevicompactum virus
	Plants	Partitiviridae—White clover crytic virus 1
	Invertebrates	Birnaviridae—Drosophila X virus
	Vertebrates	Reoviridae—Rotavirus
Single positive stranded—reverse transcriptase	Fungi	Pseudoviridae—Saccharomyces cerevisiae Ty1 virus
	Invertebrates	Metaviridae—Ascaris lumbricoides Tas virus
	Vertebrates	Retroviridae—HIV
DNA viruses
Single stranded	Bacteria	Inoviridae—Vibrio phage CTX
	Plants	Geminiviridae—Beet curly top virus
	Invertebrates	Parvoviridae—Aedes aegypti densovirus
	Vertebrates
Double stranded	Bacteria	Myoviridae—Enterobactriophage T4
	Amoeba, Algae, Fungi	Mimiviridae—Acanthamoeba polyphaga mimivirus
	Invertebrates	Iridoviridae—Tiger frog virus
	Vertebrates	Adenoviridae—Human Adenovirus species A–G
Double stranded—reverse transcriptase	Plants	Caulimoviridae—Cauliflower mosaic virus
	Vertebrates	Hepadnaviridae—Hepatitis B virus

The question of whether viruses can be classified as alive is one that has been debated since their discovery (Beijerinck, 1899; Villarreal, 2004; Moreira and Lopez-Garcia, 2009). In Villarreal's 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 host's 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 beneficial 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 one's 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 beneficial to the host. An example of a beneficial 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 benefit the bacterial host by enabling compromised host cells to release a toxin that is inhibitory to predators (protest grazers) or the bacteria's 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 specificity, viruses can be grouped into two classes: those that only infect a given host or host tissue type (specific 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-specific 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 15°C) and hypothesized that these types of oceanic reservoirs could serve as inoculum for terrestrial hosts (Smith et al., 1998). The Avian influenza 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 benefit of host specificity is “finding 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 specificity is the probability that a newly replicated virus can find a host upon cellular release. The benefit of host generalization is the availability of many hosts, which thus increases the likelihood that a newly replicated virus can find a receptive cell to infect. The 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 fitness (a lowered ability to efficiently 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 fitness (Elena et al., 2009).

Earth's viruses, whether they have lytic or lysogenic host relationships, must survive the extracellular environment to find 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 identified 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 phenotype’—the capacity to rise from their own ashes.”

Table 2.

Virus Survival

Virus	Host	Survival environment	Survival time or influences on infectivity	Reference
Avian influenza H5N1	Birds/mammals	Fresh and marine surface waters	12 days at 22–35°C20 days at 4°C	Mihai et al., 2011
Avian influenza H5N1	Birds/mammals	Distilled water	>60 days at 4°C	Domanska-Blicharz et al., 2010
Avian influenza H9N2	Birds/mammals	Allantoic fluid diluted in pH buffer/phosphate-buffered saline	1 week at pH 5.0, 3 weeks at pH 7.0, 20°C	Davidson et al., 2010
Avian influenza H9N2	Birds/mammals	Allantoic fluid	Relative to 37.0°C, 18 times longer at 20°C, and 70 times longer at 4°C	Davidson et al., 2010
Avian influenza H6N2	Birds/mammals	Methanogenic landfill leachate/water	Elevated temperature and non-neutral pH=decreased survival. Landfill survival rates of 30–600 days	Graiver et al., 2009
Influenza A	Birds/mammals	Banknotes	3 days without respiratory mucus17 days with respiratory mucus	Thomas et al., 2008
Avian influenza H6N2 and Newcastle disease virus	Birds/mammals	Mesh bags of chicken manure, litter, feed, and the allantoic spike sealed in vials	50–65°C bag specimens <7 days, vial control >21 days13–28°C bag specimens <21 days, vial control >21 days	Guan et al., 2009
Venezuelan equine encephalomyelitis (VEE) and Sindbis viruses (SV)	Birds/mammals	Distilled deionized water (DD) at 4°C, 21°C, and 30°C and tap water (TW) at 21°C	DD at 4°C=21 days. At 21°C and 30°C survival ∼.13 log₁₀ day⁻¹ less over the same time period	Fitzgibbon and Sagripanti, 2008
Hepatitis C virus	Mammals	Dried samples on stainless steel discs	7 days at room temperature	Doerrbecker et al., 2011
Hepatitis C virus	Mammals	Syringe blood	63 days at 37°C	Paintsil et al., 2010
Foot and mouth disease virus, swine fever virus, bovine viral diarrhea virus, swine influenza virus	Mammals	Farm slurry	≤=1 h at 55°C, many weeks at 5°C	Botner and Belsham, 2012
Swine fever virus	Mammals	Swine feces and urine	½-life (survival of ½ the starting population) of 2–4 days at 5°C and 1–3 h at 30°C	Weesendorp et al., 2008
Rabbit hemorrhagic disease virus	Mammals	Carcasses and excretions onto nearby soil	3 months in carcasses and 1 month for excreted viruses	Henning et al., 2005
Poliovirus	Mammals	Distilled water (DI), artificial marine (AM), filtered marine (FM), and unfiltered seawater (UM)	Days to survival of only 1% of the starting titer at 22°C=16.0 for DI, 18.2 for AM, 18.2 for FM, and 4.4 for UMDays to survival of only 1% of the starting titer at 30°C=13.0 for DI, 7.4 for AM, 6.8 for FM, and 4.0 for UM	Wetz et al., 2004
Poliovirus	Mammals	Arid riverbed soil amended with DI and diluted sewage effluent	At 1°C >70 days under aerobic and anaerobic conditions. At 23°C and 37°C decreases in survival time or surviving % of spikes	Hurst et al., 1980
Poliovirus and hepatitis A virus (HAV)	Mammals	Mineral water	At 4°C >1 year, at room temperature (20–26°C) Poliovirus <300 days, HAV <360 days	Biziagos et al., 1988
Adenovirus, rotavirus, and hepatitis A virus	Mammals	Clothing	Washing with detergent and standard household dryer conditions=survival of 1–8% of the starting titer, with the addition of bleach=survival of 0.01% of the starting titer	Gerba and Kennedy, 2007
Viral hemorrhagic septicemia virus	Fish	Challenged Pacific sardines	66.7% fish mortality at 13°C and 6.7% fish mortality at 20°C	Arkush et al., 2006
Tobacco mosaic virus	Plant	Simulated interstellar w/∼250 equivalent years of irradiation	82% survival rate	Koike et al., 1992
Bacteriophage (Escherichia coli prophage)	Bacteria	Spaceflights—duration 1.5–528 h, radiation dosage 0.6 mrad to 36 rad	Prophage production rates relative to control experiments ranged from 0 (1 of 12 flights) to 4.6 times greater (11 of 12 flights averaged 2.0 times greater)	Parfenov and Lukin, 1973
Bacteriophage MS2 and PRD1	Bacteria	Groundwater	At 7°C phage were stable for 80 days. At 10°C and 23°C decreased survival rates with PRD1 inactivation rates lower than MS2 for most water samples	Yahya et al., 1993
Bacteriophage MS2	Bacteria	Distilled deionized water (DD) at 4°C, 21°C, and 30°C and tap water (TW) at 21°C	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 21°C, inactivation rates twice that observed at 21°C with DD H₂O	Fitzgibbon and Sagripanti, 2008
Bacteriophage T2	Bacteria	Artificial seawater	5 days incubation at 24°C, 60 times greater survival in the presence of clay than without	Gerba and Schaiberger, 1975
Bacteriophage (Xanthomonas campestris phage)	Bacteria	Leaf surfaces in northern Italy	5 days on peach leaves in an orchard during the summer	Zaccardelli et al., 1992
Marine bacteriophage (4 isolated host/phage systems)	Bacteria	Seawater	Relative to local sunlight and water column exposure=native (coastal California) phage decay rates of 4.1–7.2% h⁻¹ Non-native (North Sea) phage decay rates of 6.6 to 11.1% h⁻¹	Noble and Fuhrman, 1997

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; Yoshida-Takashima et al., 2012). In two Yellowstone National Park hot springs, where temperatures and pH ranged from 75°C to 93°C 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 87°C to 93°C, five different morphotypes of viable archaeal viruses (determined via enrichment assays and transmission electron microscopy) 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 0.5–1.5 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 −12°C 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 specificity and range in this cold-weather environment (Polischuk et al., 2007). Extreme cold or cryogenic storage is widely used to preserve microorganisms. Stocks of Influenza viruses as old as 40 years that were cryogenically stored (−70°C) 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 field 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 specificity 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 specificity, 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 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 specificity to their hosts and thus will not be able to infect organisms of Earth origin. Although host specificity is a trademark of Earth's 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 self-replicating 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 specificity 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 specificity outside pathogenic relationships (and even here one can argue host benefits) 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 specificity is a valuable asset. While host specificity 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 significantly 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 first identified and described viruses were host-specific pathogens. What we know of viruses at this point is that we are most likely to encounter them on other life-bearing planets and that, yes, they tend to be host-specific, 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.

Footnotes

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.

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