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94 Space Studies Board Annual Report—2007 5.9 The Limits of Organic Life in Planetary Systems A Report of the Ad Hoc Committee on the Limits of Organic Life in Planetary Systems of the Committee on the Origins and Evolution of Life Executive Summary Reflecting the near inevitability of human missions to Mars and other locales in the solar system where life might exist, and given the interest of the public in the question, Are we alone?, the National Aeronautics and Space Administration (NASA) commissioned the National Research Council, which formed the Committee on the Limits of Organic Life in Planetary Systems, to address the following questions: • What can be authoritatively said today about limits of life in the cosmos? • What Earth-based research must be done to explore those limits so that NASA missions would be able to recognize, conserve, and study alien life that is encountered? Theory, data, and experiments suggest that life requires (in decreasing order of certainty): • A thermodynamic disequilibrium; • An environment capable of maintaining covalent bonds, especially between carbon, hydrogen, and other atoms; • A liquid environment; and • A molecular system that can support Darwinian evolution. Earth abundantly displays life that uses solar, geothermal, and chemical energy to maintain thermodynamic disequilibria, covalent bonds between carbon, water as the liquid, and DNA as a molecular system to support Darwinian evolution. Life with those characteristics can be found wherever water and energy are available. The natural tendency toward terracentricity requires that we make a conscious effort to broaden our ideas of where life is possible and what forms it might take. The long history of terran chemistry tempts us to become fixated on carbon because terran life is based on carbon. But basic principles of chemistry warn us against t ­erracentricity. It is easy to conceive of chemical reactions that might support life involving noncarbon compounds, occurring in solvents other than water, or involving oxidation-reduction reactions without dioxygen. The committee found no compelling reason to limit the environment for life to water as a solvent, even if life is constrained to use carbon as the scaffolding element for most of its biomolecules. In water, a wide array of molecular structures are conceivable that could (in principle) support life but be so different from those for life on Earth that they would be overlooked by unsophisticated life-detection tools. Evidence suggests that ­Darwinian processes require water, or a solvent like water, if they are supported by organic biopolymers (such as DNA). Although macromolecules that use silicon are known, few thoughts suggest how they might have emerged spon- taneously to support a biosphere. Many of the definitions of life include the phrase undergoes Darwinian evolution. The implication is that p ­ henotypic changes and adaptation are necessary to exploit unstable environmental conditions, to function opti- mally in the environment, and to provide a mechanism to increase biological complexity. The canonical character- istics of life are inherent capacities to adapt to changing environmental conditions and to increase in complexity by multiple mechanisms, particularly by interactions with other living organisms. One of the apparent generalizations that can be drawn from knowledge of Earth life is that lateral gene transfer is an ancient and efficient mechanism for rapidly creating diversity and complexity. The unity of bio­ chemistry among all Earth’s organisms emphasizes the ability of organisms to interact with other organisms to NOTE: “Executive Summary” reprinted from The Limits of Organic Life in Planetary Systems, The National Academies Press, Washington, D.C., 2007, pp. 1-4. 1 The committee uses the term terran to denote a particular set of biological and chemical characteristics that are displayed by all life on Earth. Thus “Earth life” has the same meaning as “terran life” when the committee is discussing life on Earth, but if life were discovered on Mars or any other nonterrestrial body, it might be found to be terran or nonterran, depending on its characteristics.

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Summaries of Major Reports 95 form ­coevolving communities, to acquire and transmit new genes, to use old genes in new ways, to exploit new habitats, and, most important, to evolve mechanisms to help to control their own evolution. Those characteristics are likely to be present in extraterrestrial life even if it has had a separate origin and a very different unified bio- chemistry from that of Earth life. Because we have only one example of biomolecular structures that solve problems posed by life and because the human mind finds it difficult to create ideas truly different from what it already knows, it is difficult for us to imagine how life might look in environments very different from what we find on Earth. Recognizing the challenges in mitigating that difficulty, the committee chose instead to embrace it. In constructing its outlook, it exploited a strategy that began by characterizing the terran life that humankind has known well, first because of its macroscopic visibility and then through microscopic observation that began in earnest 4 centuries ago. As the next step in its strategic process, the committee assembled a set of observations about life that is considered exotic when compared with human-like life. The committee asked, Can we identify environments on Earth where Darwinian processes exploiting human-like biochemistry cannot exploit available thermodynamic disequilibria? The answer to that question is an only slightly qualified no. It appears that wherever the thermo- dynamic minimum for life is met on Earth and water is present, life is found. Furthermore, the life that is found appears to be descendent from an ancestral life form that also served as the ancestor of humankind (we might not have recognized it if its ancestry were otherwise), and it exploits fundamentally human-like biochemistry. The committee reviewed evidence about abiotic processes that manipulate organic material in a planetary environment. It asked whether the molecules that we see in contemporary terran life might be understood as the inevitable consequences of abiotic reactivity. The committee then surveyed the inventory of environments in the solar system and asked which ones might be suitable for life of the terran type. The survey made clear that most locales in the solar system are at thermo­ dynamic disequilibrium, an absolute requirement for chemical life, and that many locales at thermodynamic disequilibrium also have solvents in liquid form and environments where the covalent bonds between carbon and other lighter elements are stable. Those are weaker requirements for life, but the three together appear, perhaps simplistically, to be sufficient for life. The committee asked whether it could conceive of a biochemistry adapted to those exotic environments, much as human-like biochemistry is adapted to terran environments. Because few detailed hypotheses are available, the committee reviewed what is known, or might be speculated, and considered research directions that might expand or constrain understanding about the possibility of life in such exotic envi- ronments. Finally, the committee considered more exotic solutions to problems that must be solved to create the emergent properties that we agree characterize life. The committee found that using thermal and chemical energy to maintain thermodynamic disequilibria, covalent bonds between carbon atoms, water as the liquid, and DNA as a molecular system to support Darwinian evolution is not the only way to create phenomena that would be recognized as life. Indeed, the emerging field of synthetic b ­ iology has already provided laboratory examples of alternative chemical structures that support genetics, ­catalysis, and ­Darwinian evolution. Organic chemistry offers many examples of useful chemical reactivity in nonwater ­liquids. Macro­molecular structures reminiscent of those found in terran biology can be formed with silicon and other elements. Accordingly, the committee identified high-priority Earth-based laboratory and field studies aimed at doing the following: • Explore the limits of life on Earth, with an emphasis on detection of life in extreme environments that might have chemical structures and metabolisms different from those of terran life that has already been characterized. • Pursue the origin of life, especially on the basis of information from NASA missions, the inventory of organic materials in the cosmos, and interactions between organic materials and minerals set in a planetary context. • Contribute basic research to understand interactions of organic and inorganic species in exotic solvents, including water under extreme conditions (as found on Venus, Mars, Europa, Enceladus, and elsewhere), water- ammonia eutectics at low temperatures (as might be possible on Titan), and liquid cryosolvents (as found on Triton and elsewhere). • Contribute to laboratory synthetic-biology research into molecular systems that are capable of Darwinian evolution but are different from standard DNA and RNA, especially those designed to improve understanding of the chemical possibilities of supporting Darwinian evolution.

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96 Space Studies Board Annual Report—2007 The committee offers the following recommendations: Recommendation 1. The National Aeronautics and Space Administration and the National Science Foundation should support these kinds of laboratory research: • Origin-of-life studies, including prebiotic-chemistry and directed-evolution studies that address ­physiologies different from those of known organisms; • Further studies of chirality, particularly studies focused on the hypothesis that specific environmental con- ditions can favor chiral selection, or on an alternative model that life with L-amino acids and D-sugars is better “fit,” from an evolutionary perspective, to evolve into complex organisms; and • Work to understand the environmental characteristics that can affect the ability of organisms to fractionate key elements, including not only carbon but also sulfur, nitrogen, iron, molybdenum, nickel, and tungsten. Recommendation 2. The National Aeronautics and Space Administration and the National Science Foundation should support these kinds of field research: • A search for remnants of an RNA world in extant extremophiles that are deeply rooted in the phylogenetic tree of life; • A search for organisms with novel metabolic and bioenergetic pathways, particularly pathways involved in carbon dioxide and carbon monoxide reduction and methane oxidation coupled with electron acceptors other than oxygen; • A search for organisms that derive some of their catalytic activity from minerals rather than protein enzymes; • A search for organisms from environments that are limited in key nutrients, including phosphorus and iron, and determination of whether they can substitute other elements, such as arsenic, for phosphorus; • A search for life that can extract essential nutrients—such as phosphorus, iron, and other metals—from rocks, such as pyrites and apatite; • A search for anomalous gene sequences in conserved genes, particularly DNA- and RNA-modifying genes; • Study of the resistance of microorganisms that form biofilms on minerals to the harsh conditions of inter- planetary transport; and • A search for life that stores its heredity in chemicals other than nucleic acids. Recommendation 3. The National Aeronautics and Space Administration should support these kinds of space research: • Programs that combine the exploration of potential metabolic cycles with the synthetic biology of unnatural nucleic acid analogues and their building blocks and that use the results to guide the design of instruments; • Astrobiology measurements that can potentially distinguish between life on Mars (and possibly other b ­ odies) that arrived via material ejected from Earth (or vice versa) and life that emerged on another body inde- pendently of life on Earth; • Inclusion in missions planned for Mars of instruments that detect lighter atoms, simple organic functional groups, and organic carbon to help distinguish between “replicator-first” and “metabolism-first” theories of the origin of life; similar considerations should guide inclusion of small-organic-molecule detectors that could func- tion on the surfaces of Europa, Enceladus, and Titan; and • Consideration, in view of the discovery of evidence of liquid water-ammonia eutectics on Titan and active water geysers on Saturn’s moon Enceladus, of whether the planned missions to the solar system should be r ­ eordered to permit returning to Titan or Enceladus earlier than is now scheduled.