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5 The Potential for Large-Scale Effects Interpretations of the discoveries made during the past decade of Mars exploration indicate a significantly enhanced potential for habitable surface environments in the past, as well as the potential for habitable condi- tions in the deep subsurface today. At the same time, new discoveries of extreme biological systems on Earth have dramatically expanded the known environmental limits for life, opening the range of potentially habitable conditions. While the existence of habitable conditions provides no guarantee that life ever originated on Mars, the possibility has increased that a martian life form, whether active, dormant, or fossil, could be included in a sample returned from Mars. But these scientific advances have been mirrored by increasing skepticism among the public at large about the risks posed by scientific and technological activities. Controversies concerning, for example, the release of genetically modified organisms into the environment or the intentional or accidental release of exotic pathogens from an increasing number of high-level biocontainment facilities is likely to play some role in any public dis- cussion relating to Mars sample return in general and to a sample-receiving facility (SRF) in particular. Thus, a key question posed to the committee is whether a putative martian organism or organisms, inadvertently released from containment, could produce large-scale negative pathogenic effects in humans or have a destructive impact on Earthâs ecological systems or environments.1 TYPES OF LARGE-SCALE EFFECTS The potential effects that are of concern about biohazards can be divided into three broad categories: â¢ Large-scale negative pathogenic effects in humans; â¢ Destructive impacts on Earthâs ecological systems or environments; and â¢ Toxic and other effects attributable to microbes, their cellular structures, or extracellular products. These concerns are addressed in the following sections. 45
46 ASSESSMENT OF PLANETARY PROTECTION REQUIREMENTS FOR MARS SAMPLE RETURN MISSIONS Pathogenic Effects Understanding of pathogenesis and the nature of biological epidemics has expanded significantly in recent years.2,3 However, the potential for large-scale pathogenic effects arising from the release of small quantities of pristine martian samples is still regarded as being very low. Significant changes have been made in requirements for containing both known pathogens and novel, or unknown, biological materials, and there have been major improvements in containment design, laboratory practices, and operational oversight. 4,5,6 Numerous reports for planning a Mars sample return mission have acknowledged that biocontainment requirements and planetary protec- tion controls will be integrated as essential elements for handling and testing returned samples. 7,8,9,10 As reviewed in Chapter 3, extreme environments on Earth have not yet yielded any examples of life forms that are pathogenic in humans. However, it is worth noting in this context that interesting evolutionary connections between alpha proteobacteria and human pathogens have recently been demonstrated for natural hydrothermal environments on Earth,11 suggesting that evolutionary distances between nonpathogenic and pathogenic organisms may be quite small in some instances. It follows that, since the potential risks of pathogenesis cannot be reduced to zero,12 a conservative approach to planetary protection will be essential, with rigorous requirements for sample containment and testing protocols. Ecological Effects New discoveries in environmental microbiology continue to expand understanding of the taxonomic and metabolic diversity of the microbial world, yet much remains unknown.13 It is worth noting, however, that extreme environments on Earth have not yet yielded any examples of life forms that are disruptive to ecosystem functions. The risks of environmental disruption resulting from the inadvertent contamination of Earth with putative martian microbes are still considered to be low. But since the risk cannot be demonstrated to be zero, due care and caution must be exercised in handling any martian materials returned to Earth. The demand for a conservative approach to both containment and test protocols remains appropriate. Toxicity and Other Potential Effects Although negative effects from nonreplicating biological materials (e.g., toxins and other metabolic by-prod- ucts) are possible, they are unlikely to be responsible for large-scale pathogenic effects. 14 Nonetheless, they are important as potential biohazards that must be considered when designing protection for the workers who will handle returned martian materials. Operationally, the committee anticipates that existing regulatory frameworks (e.g., that of the Occupational Safety and Health Administration and the Centers for Disease Control and Preven- tion), coupled with rigorous laboratory biosafety controls, will be incorporated into future discussions of handling and testing protocols and other operations used in the analysis of returned martian materials. The Question of Panspermia Martian meteorites hold additional importance for planetary protection considerations, beyond the information they convey about environmental conditions on Mars (see Chapter 2). If life originated on Mars and still persists there today, it is possible that over geological time, organisms may have been intermittently delivered to Earth from Mars via impact ejection, a process known as panspermia.15 Thus, it is appropriate to ask if this natural transfer of materials between Mars and Earth (and vice versa) may have caused large-scale effects for Earthâs environments in the past. If large-scale effects have not demonstrably occurred in the past, can the presence of martian meteorites on Earth be used to argue that there are no back-contamination concerns associated with a Mars sample return mission?
THE POTENTIAL FOR LARGE-SCALE EFFECTS 47 The Flux of Martian Meteorites The rate of influx of martian meteorites to Earth can be estimated only crudely. Roughly 500 meteorites larger than 0.5 kilogram are thought to fall on Earth every year, but only about four are actually observed because most fall into the ocean, or into sparsely populated areas.16,17,18 Of the 210 meteorites observed to fall between 1815 and 1960, in densely populated areas of Japan, India, Europe, and North America, three were from Mars. Thus, the ratio of martian meteorites to total meteorites is thought to be roughly 1:100. This number is very approximate. So far, about half a dozen martian meteorites have been identified among the 8,000 meteorites recovered from Antarctica. However, considerable analysis is required to identify a martian origin, and most of the antarctic meteorites from Mars have received only cursory examination. If the 1:100 ratio is accepted as being representative, then of the roughly 500 meteorites that fall on Earth every year, perhaps five are from Mars. Because meteorites resemble ter- restrial rocks, they are usually recovered only under special circumstances, such as when they have been observed to fall, or by the accumulation of dark-colored meteorites on natural, light-toned surfaces (e.g., accumulation by ablation of the antarctic ice sheet, or aeolian erosion of desert ergs (âsand seasâ), like the Sahara, or exposure on playa (dry lake) surfaces of evaporite basins, and so on). The Survival of Organisms Ejected from Mars A question of major importance with respect to back contamination of Earth by mechanisms of panspermia is whether putative martian organisms could survive ejection from Mars, transit to Earth, and subsequent passage through Earthâs atmosphere. The Shergottites show evidence for significant shock metamorphism; however, the Nakhlites, Chassigny, and ALH 8400119 show little evidence of shock damage as a result of ejection from Mars. 20 Passage through Earthâs atmosphere heats only the outer few millimeters of a meteorite, and survival of organics in ALH 84001 and of thermally labile minerals in several other martian meteorites indicates that, indeed, only minor heating occurred during ejection from Mars and subsequent passage through Earthâs atmosphere. Transit to Earth may present the greatest hazard to the survival of any microbial hitchhikers. Cosmic-ray- exposure ages of the meteorites in current collections indicate transit times of 350,000 to 16 million years. 21 However, theoretical modeling suggests that about 1 percent of the materials ejected from Mars are captured by Earth within 16,000 years and that 0.01 percent reach Earth within 100 years. 22 Thus, survival of organisms in meteorites, where they are largely protected from radiation, appears plausible. If microorganisms could be shown to survive conditions of ejection and subsequent entry and impact, there would be little reason to doubt that natural interplanetary transfer of organisms is possible and has, in all likelihood, already occurred. Assuming that organisms survive ejection, an important obstacle to long-term viability during transport over interplanetary distances (at low temperatures) is the accumulation of genetic damage from natural background radiation emitted from the radioactive minerals present within the host meteorite. In the absence of active DNA repair, a genome such as that of Deinococcus radiodurans would be degraded and become dysfunctional (i.e., non- repairable) within 200 million years,23 rendering the meteorite sterile with respect to living organisms. A relatively radiation-sensitive bacterium like Escherichia coli present within a meteorite could easily survive for 6 million years.24 Of course, any fossilized remains, or remnant biomaterials, would persist intact, providing a potential record of life. It should be noted that martian materials transported to Earth via a sample return mission will spend a relatively short time (less than a year) in spaceï£§all the while protected in containers. (Note that researchers have yet to discover compelling evidence of life in any meteorite, martian or otherwise.) Thus, the potential hazards posed for Earth by viable organisms surviving in samples is significantly greater with a Mars sample return than if the same organisms were brought to Earth via impact-mediated ejection from Mars. Martian Meteorites, Large-Scale Effects, and Planetary Protection Impact-mediated transfers of terrestrial materials from Earth to Mars, although considerably less probable than such transfers from Mars to Earth, should also have occurred numerous times over the history of the two planets. Thus, it is possible that viable terrestrial organisms were delivered to Mars at some time during the early history
48 ASSESSMENT OF PLANETARY PROTECTION REQUIREMENTS FOR MARS SAMPLE RETURN MISSIONS of the two planets. As noted above, it is also possible that if life had an independent origin on Mars, living martian organisms may have been delivered to Earth. Although such exchanges are less common today, they would have been particularly common during the early history of the solar system when impact rates were much higher. Despite suggestions to the contrary,25 it is simply not possible, on the basis of current knowledge, to deter- mine whether viable martian life forms have already been delivered to Earth. Certainly in the modern era, there is no evidence for large-scale or other negative effects that are attributable to the frequent deliveries to Earth of essentially unaltered martian rocks. However, the possibility that such effects occurred in the distant past cannot be discounted. Thus, it is not appropriate to argue that the existence of martian meteorites on Earth negates the need to treat as potentially hazardous any samples returned from Mars via robotic spacecraft. A prudent planetary protection policy must assume that a potential biological hazard exists from Mars sample return and that every precaution should be taken to ensure the complete isolation of any deliberately returned samples, until it can be determined that no hazard exists. CONCLUSIONS The committee concurred with the basic conclusion of the NRCâs 1997 report Mars Sample Return: Issues and Recommendations 26 that the potential risks of large-scale effects arising from the intentional return of martian mate- rials to Earth are primarily those associated with replicating biological entities, rather than toxic effects attributed to microbes, their cellular structures, or extracellular products. Therefore, the focus of attention should be placed on the potential for pathogenic-infectious diseases, or harmful ecological effects on Earthâs environments. The committee found that the potential for large-scale negative effects on Earthâs inhabitants or environments by a returned martian life form appears to be low, but is not demonstrably zero. Changes in regulations, oversight, and planetary protection controls over the past decade support the need to remain vigilant in applying requirements to protect against potential biohazards, whether as pathogenic or ecological agents. Thus, a conservative approach to both containment and test protocols remains the most appropriate response. A related issue concerns the natural introduction of martian materials to Earthâs environment in the form of martian meteorites. Although exchanges of essentially unaltered crustal materials have occurred routinely through- out the history of Earth and Mars, it is not known whether a putative martian microorganism could survive ejec- tion, transit, and impact delivery to Earth or would be sterilized by shock pressure heating during ejection, or by radiation damage accumulated during transit. Likewise, it is not possible to assess past or future negative impacts caused by the delivery of putative extraterrestrial life, based on present evidence. Assessing the potential for impact-mediated interchanges of viable organisms between Earth and Mars remains an active area of research that may eventually lead to a more refined understanding of the potential hazards associ- ated with Mars sample return. Thus, the committee encourages continued support for research to assess the potential for impact-mediated interchanges of viable organisms between Earth and Mars. NOTES â 1â National Research Council, Mars Sample Return: Issues and Recommendations, National Academy Press, Washing- . ton, D.C., 1997, pp. 19-22. â 2â N.E. Morton, âFifty Years of Genetic Epidemiology, with Special Reference to Japan,â Journal of Human Genetics . 51:269-277, 2006. â 3â R.M. Anderson, âEvolutionary Pressures in the Spread and Persistence of Infectious Agents in Vertebrate Popula- . tions,â Parasitology 111:S15-S31, 1995. â 4â M.S. Race and E. Hammond, âAn Evaluation of the Role and Effectiveness of Institutional Biosafety Committees in . Providing Oversight and Security at Biocontainment Laboratories,â Biosecurity and Bioterrorism-Biodefense Strategy Practice and Science 6:19-44, 2008. â 5â J.W. Le Duc, K. Anderson, M.E. Bloom, J.E. Estep, H. Feldmann, J.B. Geisbert, T.W. Geisbert, L. Hensley, M. . Holbrook, P.B. Jahrling, T.G. Ksiazek, G. Korch, J. Patterson, J.P. Skvorak, and H. Weingartl, âFramework for Leadership and Training of Biosafety Level 4 Laboratory Workers,â Emerging Infectious Diseases 14:1685-1688, 2008.
THE POTENTIAL FOR LARGE-SCALE EFFECTS 49 â 6â D. Frasier and J. Talka, âFacility Design Considerations for Select Agent Animal Research,â Ilar Journal 46:23-33, . 2005. â 7â J.D. Rummel, M.S. Race, D.L. DeVincenzi, P.J. Schad, P.D. Stabekis, M. Viso, and S.E. Acevedo, eds., A Draft Test . Protocol for Detecting Possible Biohazards in Martian Samples Returned to Earth, NASA/CP-20-02-211842, NASA Ames Research Center, Moffett Field, Calif., 2002. â 8â National Research Council, The Quarantine and Certification of Martian Samples, National Academy Press, Wash- . ington, D.C. 2002. â 9â M.S. Race, âEvaluation of the Public Review Process and Risk Communication at High-Level Biocontainment . Laboratories,â Applied Biosafety 13:45-56, 2008. 10â The iMARS Working Group, Preliminary Planning for an International Mars Sample Return Mission: Report of the . International Mars Architecture for the Return of Samples (iMARS) Working Group, National Aeronautics and Space Admin- istration, Washington, D.C., and European Space Agency, Paris, France, 2008. 11â S. Nakagawa, Y. Takaki, S. Shimamura, A.L. Reysenbach, K. Takai, and K. Horikoshi, âDeep-sea Vent Epsilon-pro- . teobacterial Genomes Provide Insights into Emergence of Pathogens,â Proceedings of the National Academy of Sciences of the United States of America 104:12146-12150, 2007. 12â D. Warmflash, M. Larios-Sanz, J. Jones, G.E. Fox, and D.S. McKay, âBiohazard Potential of Putative Martian Organ- . isms During Missions to Mars,â Aviation Space and Environmental Medicine 78:A79-A88, 2007. 13â See, for example, National Research Council, The New Science of Metagenomics: Revealing the Secrets of Our . Microbial Planet, The National Academies Press, Washington, D.C., 2007. 14â R.A. Moore, I. Vorberg, and S.A. Priola, âSpecies Barriers in Prion DiseasesâBrief Review,â Archives of Virology . Supplement 19:187-202, 2005. 15â See, for example, H.J. Melosh, âThe Rocky Road to Panspermia,â Nature 332:687-688, 1988. . 16â B. Mason, Meteorites, Wiley, New York, 1962. . 17â H. Brown, âThe Density and Mass Distribution of Meteoritic Bodies in the Neighborhood of the Earthâs Orbit,â . Journal of Geophysical Research 65:1679-1683, 1960. 18â H. Brown, âAddendum: The Density and Mass Distribution of Meteoritic Bodies in the Neighborhood of the Earthâs . Orbit,â Journal of Geophysical Research 66:1316-1317, 1961. 19â These meteorites are named after the location in which the first representative of each class was discovered. ALH . 84001 is the name of a particular martian meteorite that does not fit into the Shergotty, Nakhla, or Chassigny families of meteorites. 20â H.Y. McSween, Jr., âWhat Have We Learned About Mars from SCN Meteorites,â Meteoritics 29:757-779, 1994. . 21â H.Y. McSween, Jr., âWhat Have We Learned About Mars from SCN Meteorites,â Meteoritics 29:757-779, 1994. . 22â B.J. Gladman, J.A. Burns, M. Duncan, P. Lee, and H.F. Levison, âThe Exchange of Impact Ejecta Between Terrestrial . Planets,â Science 271:1387-1392, 1996. 23â R.C. Richmond, R. Sridhar, Y. Zhou, and M.J. Daly, âPhysico-Chemical Survival Pattern for the Radiophile D. . radiodurans: A Polyextremeophile Model for Life on Mars,â SPIE Conference on Instruments, Methods, and Missions for Astrobiology II, Denver, Colo., SPIE 3755:210-222, 1999. 24â Michael J. Daly, personal communication, November 7, 2008. . 25â See, for example, A.P. Pavlov, V.L. Kalinin, A.N. Konstantinov, V.N. Shelegedin, and A.A. Pavlov, âWas Earth Ever . Infected by Martian Biota? Clues from Radioresistant Bacteria,â Astrobiology 6:911-918, 2006. 26â National Research Council, Mars Sample Return: Issues and Recommendations, National Academy Press, Washing- . ton, D.C., 1997.