Introduction

There is considerable evidence that early in its history and episodically throughout time Mars had liquid water on its surface. Carr (1996) provides a good summary of the evidence and implications of water on Mars, and the biological implications have been extensively discussed (McKay 1986, 1997; McKay et al. 1992; Davila and Schulze-Makuch 2016). Figure 1 shows Nanedi Canyon, probably the best evidence for the sustained, stable flow of liquid water on Mars. The indication that Mars had liquid water on its surface is the motivation for considering the possibility of life on it (McKay 1997). Water is the essential ecological requirement for life and presumable for the origin of life as well. Life appears to have evolved quickly on Earth, and although the nature of the origin of life remains uncertain, these theories for the origin of life on Earth would apply to Mars as well (Davis and McKay 1996). Thus it is plausible that if Mars had liquid water habitats for sustained periods in its past, then life arose there as well. The supposition that Mars once had a biosphere has led to suggestions that through human intervention, via terraforming, it could once again be made habitable (e.g., McKay et al. 1991; Fogg 1995; McKay 2009a). The life-forms that would fill such a biosphere could be from Mars or, if necessary, from Earth.

Fig. 1
figure 1

Nanedi Vallis on Mars, the best evidence we have for the sustained, stable flow of liquid water on Mars. The valley is about 2 km across and has the bends and curves familiar from river valleys on Earth. Most importantly on the bottom of the valley is what appears to be the small channel of the river that cut the valley. Image from NASA/Malin Space Sciences

The search for life on Mars poses a logical dilemma: how to search for life without contaminating Mars with life from Earth. Such contamination poses two dangers. First, the search for life on Mars may give positive results because of life carried from Earth. Second, life on Mars may be endangered by competition with transplanted Earth life. As part of the Outer Space Treaty, the space agencies of Earth have agreed to prevent biological contamination in the conduct of scientific exploration of other worlds in order to preserve them for future scientific investigation. The resulting controls on spacecraft are known as planetary protection policies and address the first of the concerns listed above (DeVincenzi 1992; DeVincenzi et al. 1998; Rummel 2001; Rummel et al. 2014). The societal and legal aspects have been considered (Race 1995; Sterns and Tennen 1995), but to date there has been little consideration of the possible negative impact of terrestrial life on native alien organisms.

However, making the distinction between life from Mars and life from Earth may not be straightforward. It is known that meteorites from Mars are present on the Earth (McSween 1994) and that some of these meteorites did not experience temperatures high enough to kill any embedded microorganisms (Weiss et al. 2000). Even if the average transit time from Mars to Earth might be too long to allow for microbial survival against radiation damage (Clark 2001) some meteorites will arrive at Earth quickly enough that survival is probable (Gladman et al. 1996; Mileikowsky et al. 2000). Thus it is possible that Earth and Mars have not been biologically isolated and that during the early history of both planets there was exchange of viable biological material. Even one successful transport among countless meteorites could have been seminal.

Thus, with respect to life on Mars, there exist three possibilities: (1) there is life on Mars that is distinctly different from life on Earth—a second genesis; (2) there is life on Mars that is genetically related to life on Earth; (3) there has never been life on Mars. We must consider the implications of each of these on the search for past life on Mars and on plans for re-creating a biosphere on Mars in the future.

Clearly the last of these is easiest to consider. If there has never been life on Mars then issues of contamination are unimportant with respect to preserving Mars’s biological potential. The search for past life will not yield results—provided that contamination from Earth is not confused for native Martian life. If there were no interest in eventually creating a biosphere on Mars then contamination that would remain dormant even for extended geological periods before dying would not be a concern. Contamination is only a fundamental problem in that it may interfere with, or confound, any deliberate plans for creating a biosphere and purposefully introducing life on Mars as part of future terraforming. Even if there was never life on Mars, if terraforming is to be considered, then the inadvertent introduction of life to Mars should be avoided.

The case in which there is life on Mars and it shares a common ancestor with life on Earth is also straightforward. If life on Mars and life on Earth are related and biological exchange has been an ongoing process throughout their history, then it is still prudent to plan and control any introduction of Earth life on Mars. We know from the ecological history of life on Earth that nonnative species can significantly alter an ecosystem and can drive native species to extinction. This concern may be warranted even if the Martians are all microbial. The concept of extinction is not easy to apply to microbial “species” on Earth where lateral gene exchange blurs the very concept of a species at the microbial level (see, e.g., Cockell 2003). However, lateral gene exchange may not be effective between Mars microbes and those from Earth. Thus the possibility of real extinction of a unique microbial genome is possible on Mars even if Martian life shares a common ancestor with Earth life. Hence, biological contamination that results in the premature mixing of Earth and Martian life is to be avoided until the details of that Martian life are fully understood.

Perhaps the most interesting and challenging case is that in which Mars has, or had, life, and this life represents a distinct and second genesis (McKay 2001a). The discovery of a second genesis of life in our solar system has profound scientific as well as philosophical and ethical importance. Philosophically, the discovery would directly address the question of life in the universe, and would suggest that the phenomenon of life is distributed throughout the universe. Scientifically, having another example of life expands the scope of biology from one to two. There may well be significant advances in medicine, agriculture, pest control, and so on, from having a second type of life to study. If that second life is allowed to form a second biosphere, the practical benefits of the study of a second example would extend to the human management of Earth’s global biosphere as well.

The clear separation of the three cases listed above may be misleading, and we may find that scientific inquiry returns ambiguous results. For example, we may find fossil evidence that there was once life on Mars, but we may not encounter any direct evidence that it persists to the present time. Alternatively, we may find evidence for life but cannot clearly determine if it represents a second genesis or a distant relative to life on Earth. The many possible ambiguities are hard to address definitively, but it may be that by framing the questions in terms of the three clear cases—no life, Earth-like life, and second genesis—we may be better prepared for dealing with ambiguous cases as well. Following this approach, the case of a second genesis is the most novel and warrants further consideration, particularly with respect to ethics.

The ethics of a second genesis have been discussed both in terms of assuming it has intrinsic value and alternatively assuming it has only instrumental value (McKay 1990, 2001b). The concept of assigning intrinsic value to life-forms is perhaps most clearly stated in the first two tenets of deep ecology (Naess 1984; Devall and Sessions 1985):

  1. 1.

    The well-being of nonhuman life on Earth has value in itself. This value is independent of any instrumental usefulness for limited human purposes.

  2. 2.

    Richness and diversity in life forms contribute to this value and are of further value in themselves.

When applied to Mars (McKay 1990) these principles argue that a biologically rich Mars is of more value than the fascinating but largely dead world we see today. Furthermore, a Martian biosphere populated by a second type of life would contribute to more diversity than one populated by transplants from Earth.

We know from observations of Mars that it does not have a rich global biosphere. Thus if there is Martian life it is either dormant or surviving within some limited refugia. We do not know what would be the fate of that life if Earth organisms were either to colonize these existing refugia or were to be present as Mars was warmed in the first step of terraforming. It might be that cohabitation of Earth life and an alien type of Martian life is possible. However, the facts of biological competition for resources would seem to indicate that one form would dominate and drive the other to extinction. Thus, it would seem that the notion of the intrinsic worth of life and diversity of life would dictate that we not allow contact between Martian life and Earth life until the implications of such contact are fully understood.

It is important to note that the basis for the ethical issues does not come from assigning intrinsic value to microbes per se, although this has been suggested (Cockell 2005, 2008). On Earth, we freely kill microorganisms. The focus of the ethical concern is for a second type of life capable of independent biological and evolutionary development. Such life enhances the richness and diversity of life in the universe—a worthy goal in itself (McKay 2013; Randolph and McKay 2014). This is true even if the specific organisms involved are only microbes.

One might reject the arguments for the intrinsic worth of life and assume that the value of Martian life must be judged by its instrumental value to humans. However, I argue that the conclusion is the same. There would be considerable benefit to humans from studies of a second type of life and of a Martian biosphere populated by that life. Knowledge in many practical fields, such as medicine, may be advanced from having a second example of life to study. While many of these scientific advances may be realized in small, contained laboratory studies with captive Martian organisms, the full ecological interactions and potential complexity of Martian life could only be studied in the context of a planetary-scale biosphere on Mars.

In summary, control of biological contamination of Mars is desirable if Mars has life, whether it is either alien to, or common with, life on Earth. Furthermore, regardless of Mars’s biological state, if there is consideration of terraforming on Mars, then control of the type and rate of introduction of life from Earth is desirable. While control of contamination is desired even if there is no life or Earth-like life on Mars, the potential implications of contamination are more profound if there is or was a second genesis in the solar system on Mars, besides the one on Earth. In this latter case, in particular, strict control of the introduction of Earth life to Mars is indicated.

The complete and effective sterilization of every spacecraft going to Mars is probably not an achievable option and would be pointless anyway since several spacecraft have already been sent to Mars with known bioloads. Instead, an adequate and achievable approach to controlling biological contamination on Mars is to require it to be reversible (McKay 2007, 2009b). This would imply, for example, that if at some time in the future a second genesis of life were discovered on Mars, then all Earth contamination could be removed.

Practicality of Biological Reversibility on Mars

On Earth there are many environments in which some type of reversible exploration is a goal. For example, Antarctic exploration is conducted in such a way that all structures can be removed at the end of their service life. In addition, in some of the valleys (e.g., Barwick Valley) that comprise the Dry Valleys of Antarctica, all trace of human exploration was removed and the valleys have been set aside for preservation. Expeditions into these valleys are conducted only in biocontainment suits.

On Earth, reversible exploration has generally not involved reversibility at the microbial level. This is reasonable on the surface of the Earth, because it is clear that microbes are carried worldwide by winds. However, for the exploration of subsurface environments, such as Lake Vostok in Antarctica, microbial isolation is an important issue.

Biologically reversible exploration of Mars—even at the microbial level—is possible because of the sterilizing nature of the Martian ultraviolet (UV) light. Bacterial endospores of Bacillus subtilis exposed to Mars-like levels of UV light were reduced by 99.9% in 30 s and after 15 min there were no survivors from an initial population of about 2 million (Schuerger et al. 2003). Further experiments showed that the low pressure on the surface of Mars exacerbated the deleterious effects of the UV (Schuerger et al. 2003). Due to the low temperatures and dry conditions on Mars, growth is not possible, and microorganisms are therefore not able to repair the DNA damage caused by UV light. In the Martian atmosphere, scattering by carbon dioxide and dust results in a diffuse UV radiation field, which while weaker than the direct solar beam is still capable of sterilization over a few hours at most. Thus surfaces exposed to direct sunlight on Mars are sterilized in minutes and those exposed to indirect sunlight (shade) on Mars are sterilized in hours.

Reversing the Contamination Already Present on Mars

One aspect of the discussion about contamination on Mars that is often overlooked is that Mars is already contaminated. The Viking landers were treated by heating to 117 °C with nitrogen gas circulation for 43 h for Viking 2 and for 50 h for Viking 1 (Ezell and Ezell 1984, p. 274). There is no indication from the mission results that the landers were not sterile, but subsequent research has shown that many microorganisms can survive this heat treatment and in fact can form resistant stages as a result. Less uncertain is the contamination on the Pathfinder lander in 1997 and all subsequent missions (Barengoltz 2005), as there was no requirement for sterilization for these missions. Instead, the requirement was only that the bioload be reduced to less than 300 bacterial spores per square meter and no more than 300,000 total, consistent with the National Academy of Science recommendations (1992). (The numerical values for this bioload requirement are set in Appendix 16 of NASA management directive NHB 8020.12.) At the time of launch, planetary protection personnel estimated that there were less than 24,000 spores on the craft (Goodwin 2000, p. 223). The current Mars Curiosity rover which arrived at Mars in August 2012 followed similar guidelines and landed with an estimated 278,000 viable spores (Benardini et al. 2014).

Microorganisms on the outside surface of any Martian lander or rover would be quickly killed by the UV light. However, microorganisms inside the vehicles would be protected from the UV (Fig. 2). Without a source of energy and at the low Martian temperatures, such microorganisms would be viable but dormant. Eventually, they would perish due to accumulated cosmic radiation that could penetrate the metal of the vehicle. A typical lethal dose for radiation-resistant microorganisms is 20 Mrad, and the cosmic radiation dose on Mars is about 10–20 rad/year. Thus microorganisms shielded from UV light within the Pathfinder vehicles could survive for about a million years and would be revived if conditions suitable for their growth were generated on Mars during that time.

Fig. 2
figure 2

Life from Earth arrives on Mars on the Sojourner rover in 1997. This rover was not sterilized before launch. At the time of launch planetary protection personnel estimated that there were fewer than 24,000 bacterial spores on the craft. Any metal surface provides protection from solar UV and would have to be removed, or sterilized in place, as part of the decontamination of the landing site. NASA/JPL

Decontaminating the sites of successful missions would be possible. All vehicles would have to be removed as well as any metal containers that could provide UV shielding for microorganisms (Fig. 3). In addition, the soil in the vicinity of the landing might require treatment. A device similar to a snow blower would blow the surface dust into the atmosphere where any microorganisms protected by the dust would be exposed to UV light. To achieve effective sterilization, the dust particles need to be suspended in the Martian light for a few hours (Schuerger et al. 2003). More testing and simulation, possibly on Mars, is needed before the practical design of this dust decontamination method is final.

Fig. 3
figure 3

First advanced life on Mars. Plant growth experiments on near-term missions to Mars can be conducted in a way consistent with biologically reversible exploration. Image by Shrox

At the (many) sites on Mars where spacecraft have crashed, the procedures for decontamination would be similar—if more extensive. Here all the pieces of metal would need to be located and collected. The soil surrounding each piece would have to be aerated. Metal-detection technology could be easily applied to this problem. The depth of penetration of metal fragments depends on the nature of the crash but is not likely to be more than a few meters. For example, the depth of craters created by the crash of the heaviest intact pieces of the space shuttle Columbia were a few meters deep or less (e.g., Gehman et al. 2003).

Biologically Reversible Human Exploration

Contamination associated with human bases poses new problems in planetary protection. McKay and Davis (1989) argued that the focus of planetary protection should shift from preventing contamination to defining and minimizing the contamination. The notion of biological reversibility provides a guide for how to minimize contamination from human bases.

Reversing the biological contamination produced by a human base would follow the same pattern as that for robotic spacecraft. First, all materials at the site, particularly metals, would be removed. Then, the surface soil and any soil that has been in contact with materials from the base would be aerated to allow for UV sterilization. The scope of the effort would be larger for a human base, but the increase in difficulty is proportional to the increased effort of a human base. The added overhead of decontamination would likely be a constant fraction of the cost of the mission itself—either robotic or human.

Implications of Biologically Reversible Exploration

Because of the strong sterilizing UV radiation present on Mars, it is conceptually straightforward to decontaminate missions to Mars even though these missions were not designed with such decontamination in mind. Nonetheless, there are ways in which mission design could make decontamination of future missions easier, in particular for missions that crash on Mars. Failed spacecraft would be easier to locate and decontaminate if they landed intact. Mission scenarios that result in crashes at atmospheric terminal velocity (hundreds of m/s) on Mars rather than at interplanetary approach velocities (tens of km/s) provide another way to reduce the difficulty of cleanup after a crash.

As a specific case consider the crash of the Mars Polar Lander in 1999. The most probable failure scenario for this mission was the premature cutoff of the retrorockets. The vehicle would therefore have hit the surface at atmospheric terminal velocity or less. Considering the craters formed by the largest pieces of the Columbia shuttle, the crater produced by the impact of the Polar Lander would be expected to be of the order of a few meters wide and a meter deep. At this depth there is no danger that any pieces of the spacecraft containing microorganisms would reach depths with liquid water and habitable conditions. Missions that fail to communicate with Earth after either having landed intact or having crashed on the surface—the likely fate of the 2003 Beagle II lander and the 2016 Schiaparelli lander—are no more difficult to decontaminate than successful missions.

Future robotic missions to Mars should be designed with biological reversibility as an explicit consideration. It is probable that this will have negligible effect on the existing planetary protection procedures. Even plant growth modules on near-term missions, as illustrated in Fig. 3, could be compliant with biologically reversible exploration.

Deep Drilling, Deep Water, Deep Trouble

The area in which biologically reversible exploration does significantly impact mission design and operation is related to missions that drill deeply below the surface of Mars. Once below the surface, the sterilizing effect of the UV light is no longer operative. Furthermore, the possibility of liquid water below the surface implies the possibility of lateral spread of contamination and even growth. There would be no practical way to decontaminate a subsurface aquifer on Mars once contamination had entered it. If the subsurface water is global in extent then such contamination would completely alter the biological state of Mars beyond reversal in any practical way. Thus complete and thorough sterilization with adequate levels of control and check are needed for deep drilling into deep subsurface water.

When Should We Stop Caring

Biologically reversible exploration on Mars is primarily a way to preserve options for Mars’s biological future while there is incomplete information on the present biological state of that planet. In addition, biologically reversible exploration allows for control on the nature and timing of microorganisms that are introduced to Mars from Earth. The search for life on Mars is one of the key goals of the Mars exploration program, and it may be that future discoveries will obviate the need for biological reversibility. The most clear-cut case would be the discovery that Mars had life, and that life was related to Earth life and had already virtually all the microbial diversity present in Earth microorganisms. In this case the need for biological reversibility is clearly diminished or altogether eliminated. On the other extreme, exploration might show that Mars never had life. In this case the need for biological reversibility is restricted to the minor consideration of timing and sequence for introducing Earth life forms in terraforming.

Proving that Mars never had life may seem impossible but that determination may be easier to make on Mars than it would be on a planet like Earth. The key difference is the presence of persistent permafrost regions. Studies on Earth have shown that permafrost is arguably the best natural environment for preserving biological material over geological time (e.g., Gilichinsky et al. 1992). On Earth permafrost that is 3–5 million years old is found in the Siberian Arctic (Gilichinsky et al. 1992), and there may be massive ground ice in Beacon Valley, Antarctica, which is over 8 million years old (Sugden et al. 1995; Gilichinsky et al. 2007).

Earth has experienced epochs of warmer conditions that would have melted even the polar ice sheets and hence no ice older than about 25 million years is likely to be found on Earth. However on Mars the situation is quite different, and there is likely to be permafrost that has been continuously frozen for over 3 billion years. If there was life on Mars during this period, some record of it would be preserved in this permafrost (Smith and McKay 2005). If a deep core is obtained from Mars and the geological evidence confirms that it preserves a record of deposition that stretches back to 3 or 4 billion years, and if this core contains no evidence of life then I, for one, would conclude that Mars never had life and that we could plan future missions and terraforming accordingly.

As discussed above, there are good reasons for supposing that impacts and meteorites could result in the natural exchange of biological material between Earth and Mars. Therefore, it may be argued that even if Mars has indigenous life, if that planet is made habitable and life flourishes there then cross contamination between the planets is inevitable, as Mars life is carried to Earth and vice versa. This would be true if human activities with respect to large impacts are not considered. It is almost a certainty that humans will develop the technology to shield planets from impacts: Spaceguard, the idea that NASA and other space agencies will set up systems for tracking and intercepting objects on a collision course with Earth. This technology will not be deployed specifically to prevent biological cross contamination of the planets, but to protect human life on Earth and in settlements on Mars. Thus future biological isolation between the two planets can be maintained.

Terraforming

The question of a second genesis of life directly affects terraforming. If life is detected in a living or revivable state on Mars, and if biochemical investigation determines that Martian life is a second genesis of life, then the motivation for altering Mars (terraforming) is not focused on Earth life but instead is focused on enhancing the richness and diversity of the indigenous Martian life.

If a second genesis of life were discovered on Mars all previous robotic landers and rovers would be removed from the surface or sterilized in place.

The Martian life would be studied in detail to determine the environmental conditions that support its growth. The assumption would be that Martian life would thrive best in warm and wet conditions because the early history of Mars was warm and wet, and thus any life that originated on early Mars is likely to be similar to Earth life in requiring liquid water conditions. Once all Earth life were removed, “terraforming” would proceed to allow that life to spread globally.

Any indigenous life on Mars is likely to be microbial, and while it may spread globally on a Mars that has been altered to be warm and wet, it will not create the diverse and powerful biosphere that could be created with Earth life (especially trees). This is as it should be because the goal of terraforming in the case of indigenous life should not be focused on creating an environment suitable for humans but on enhancing the richness and diversity of life in the universe (McKay 2013; Randolph and McKay 2014).

Conclusions

We are faced with the challenge of preserving the future biological potential of Mars as we explore to understand its biological past. Preventing all contamination of Mars is an unrealistic goal. Instead I have suggested here a guiding principle of biologically reversible exploration. The main points and conclusions of the argument are:

  1. 1.

    Most importantly, biologically reversible exploration protects the possibility that life on Mars may be a second genesis. Also, we desire to promote that life separately from Earth life.

  2. 2.

    Secondarily, biologically reversible exploration allows for control over the nature and sequence of life-forms brought from Earth to Mars.

  3. 3.

    The strong solar ultraviolet radiation on Mars makes biological reversibility feasible. To achieve decontamination of missions previously sent to Mars, all metal objects would be removed and the soil in contact with these surfaces would be ejected into the atmosphere where the individual soil grains would be bathed in sterilizing UV.

  4. 4.

    Biological reversibility is not a significant departure in cost or complexity from current practice in planetary protection.

  5. 5.

    For deep drilling, especially to subsurface aquifers, biological reversibility has strong implications.

  6. 6.

    Plant growth modules on near-term robotic missions and human bases can be designed and operated in a way consistent with biologically reversible exploration.

  7. 7.

    The exploration of Mars should continue to be biologically reversible until the nature of life on Mars, if any, is understood, and plans for introducing life from Earth to Mars have been clarified.

  8. 8.

    Future natural biological exchange between Earth and Mars due to meteorites will be stopped as a consequence of human technology to guard planets against the devastation of large impacts.