4
Areas That Could Benefit from Augmentation and Integration

The astrophysical context of life consists of the structures that host life, the substances that compose it, and the astronomical radiant and particle fluxes that affect it. In a somewhat broader framework, one can consider the relevant astrophysical techniques to observe and determine these factors to be part of the intellectual astrophysical context of astrobiology. An example would be the search for biomarkers that require astronomy for remote detection but that could be defined in a manner (chemical disequilibrium) rather disconnected from any specific astrophysical context. The issue in Chapter 3 raised by the duplication of astronomical topics within the NASA Astrobiology Institute (NAI) nodes is not only one of multiple teams exploring similar astronomical projects but is also an issue of whether other astronomical topics of astrobiological interest may have been overlooked. Some of these overlooked topics are merely small gaps in otherwise active areas, but others are largely unexplored.

The one topic of astrophysical research that is being richly explored in an ever more fully realized astronomical context is the search for planets. Planets are being sought around a wide variety of host stars, including white dwarfs, and in a wide variety of environments—for instance, isolated stars, binary stars, and stars in stellar clusters. This research is clearly in the realm of astrobiology but for the time being must be rather disconnected from the biological and geological aspects of astrobiology. The notion of habitable zones has been expanded with our growing understanding of extremophiles, but there is much to be done in terms of placing this work on habitable zones in the broadest astronomical context. Because these topics are already the focus of great and warranted attention, the committee does not stress them in this report.

While there is a great deal of astronomical work on the formation of stars and planets and the chemistry of interstellar clouds, there are gaps in this work, on the delivery of material to planetary surfaces and the processing that occurs. The problem of understanding the delivery of organics should be connected to the topics of star formation and cosmochemistry and the origin of life. It is only in this context that these fields are important to the astrobiology community. Meteoritics provides valuable information, but this discipline does not seem to be well supported in the current NAI framework. Another topic that does not appear to be well covered is the influence of astronomical events on the



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The Astrophysical Context of Life 4 Areas That Could Benefit from Augmentation and Integration The astrophysical context of life consists of the structures that host life, the substances that compose it, and the astronomical radiant and particle fluxes that affect it. In a somewhat broader framework, one can consider the relevant astrophysical techniques to observe and determine these factors to be part of the intellectual astrophysical context of astrobiology. An example would be the search for biomarkers that require astronomy for remote detection but that could be defined in a manner (chemical disequilibrium) rather disconnected from any specific astrophysical context. The issue in Chapter 3 raised by the duplication of astronomical topics within the NASA Astrobiology Institute (NAI) nodes is not only one of multiple teams exploring similar astronomical projects but is also an issue of whether other astronomical topics of astrobiological interest may have been overlooked. Some of these overlooked topics are merely small gaps in otherwise active areas, but others are largely unexplored. The one topic of astrophysical research that is being richly explored in an ever more fully realized astronomical context is the search for planets. Planets are being sought around a wide variety of host stars, including white dwarfs, and in a wide variety of environments—for instance, isolated stars, binary stars, and stars in stellar clusters. This research is clearly in the realm of astrobiology but for the time being must be rather disconnected from the biological and geological aspects of astrobiology. The notion of habitable zones has been expanded with our growing understanding of extremophiles, but there is much to be done in terms of placing this work on habitable zones in the broadest astronomical context. Because these topics are already the focus of great and warranted attention, the committee does not stress them in this report. While there is a great deal of astronomical work on the formation of stars and planets and the chemistry of interstellar clouds, there are gaps in this work, on the delivery of material to planetary surfaces and the processing that occurs. The problem of understanding the delivery of organics should be connected to the topics of star formation and cosmochemistry and the origin of life. It is only in this context that these fields are important to the astrobiology community. Meteoritics provides valuable information, but this discipline does not seem to be well supported in the current NAI framework. Another topic that does not appear to be well covered is the influence of astronomical events on the

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The Astrophysical Context of Life history of life—for instance, the stellar flares and supernovas that would alter the cosmic ray flux into the atmosphere and onto the surface. Specifically, the biological effects of radiation and particle fluxes should be explored. Cosmic rays and high-energy photons may both produce ionization in cells, but their production, propagation, atmospheric penetration, and deposition are different. This report places some emphasis on particle and photon irradiation both because such radiation is a ubiquitous feature of the astronomical environment that is relevant to biology and because it is relatively understudied. Consideration of the astrophysical context of life elucidates the fact that all planets will exist in variable environments. While somewhat abstracted from a specific astronomical context, there are basic issues of how much variability is healthy, or even needed, for the robust evolution of complex life. These issues raise questions about molecular evolution in an astronomical context. With finite personnel and finite time, the committee may not have addressed all the areas that could come within the purview of this report. Some representative areas that it believes are relatively understudied and especially amenable to focused effort in the near future are these: The galactic environment, Cosmic, solar, and terrestrial irradiation, Interstellar and protostellar nebular chemistry, Bombardment, Prebiotic chemistry and photosynthesis, and Molecular evolution in a variable astronomical context. The committee addresses these topics in some detail below. For each topic it attempts to outline relevant astronomical issues that are currently rather divorced from other disciplines of astrobiology but that are deemed to be life-oriented and hence solidly within the rubric “astrobiological research.” The committee also attempts to identify for each topic where interdisciplinary work could be needed. GALACTIC ENVIRONMENT Current Work and Gaps One of the broadest questions one can ask is that about the role of the galactic environment in the origin, development, sustainability, and evolution of life. The galactic environment refers to the astronomical environment in which any life-hosting body resides. The galactic environment consists of the large-scale and highly irregular environment of the Galaxy, with its dense bulge and spiral arms filled with stars and gas of varying composition, analogous to the varied environments in the biosphere of Earth. The galactic environment is also defined by the particular type of star, its location in a dense or rarified portion of the interstellar medium, the star’s location with respect to the spiral arms or the central bulge, and the presence or absence of nearby perturbations caused by catastrophic or milder events that can affect life. As does life on an evolving Earth, the galactic ecological niche will inevitably vary with time as the star wanders through the Galaxy and encounters different conditions and as the star itself evolves. Stars like the Sun could very well have been born in rich clusters where neighboring young stars bathed the solar system with external radiation. In time, the clusters dissolved, leaving the Sun to wander its solitary way, as it does today. Some have referred to this overall galactic environment as a “disturbed galactic ecology.” The question has been raised of whether there is a galactic habitable zone in the same sense as the habitable zones around the Sun and other stars, defined principally by the ability to sustain liquid water.

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The Astrophysical Context of Life The galactic habitable zone has been delineated as an annulus in the Galaxy not too close to the bulge, where excess supernovas may be dangerous, and not too far from the center, where a paucity of heavy elements may prevent terrestrial planet formation.1,2 One point of view is that this annulus may be rather narrow, giving Earth a special, and rare, location with respect to both its host star and the Galaxy. There are many issues to be explored in terms of the space- and time-varying conditions of a given potentially life-hosting stellar system. What is an optimal location or galactic environment for the development and sustainability of life in relation to the spiral arms, the galactic center, and the regions of heavy-element formation? Where, exactly, is the Sun with respect to the galactic center? Where is the co-rotation point, the radius where the Keplerian velocity of the Sun about the Galaxy matches the pattern speed of the spiral arms and therefore drifts but little with respect to patches of newborn stars? The galactic radius of the Sun and its co-rotation point are uncertain by 10 to 20 percent, rendering uncertain the rate at which the Sun encounters a variable galactic environment or moves at rest relative to its immediate surroundings. What are the conditions in the interstellar gas that the Sun or other stars are likely to encounter? The range in density of interstellar gas is large, with potentially significant effects on the ram pressure of the astrosphere and the ability of the astrosphere to screen cosmic rays. When in the development of the Galaxy might it first have hosted life? Must the average concentration of elements be high, or is it sufficient for pockets of enhancement to exist? If so, when would this first occur? What are the effects of rare, but powerful, explosions? An example of the sort of cross-disciplinary work that can bind astronomy with other aspects of astrobiology in a galactic context is the model presented by Shaviv,3 which connects the modulation of cosmic rays as the Sun passes through spiral arms with effect on cloud cover and hence climate and conditions in the biosphere. While the validity of the statistical correlations has been strongly challenged,4 this idea is worth deeper investigation. More work is needed to develop chronometers associated with meteoric data on cosmic ray fluxes. In addition, there may be other means to modulate the cosmic ray flux—for instance, the variable interstellar medium density and associated ram pressure, which determine the extent of the heliosphere and its ability to screen cosmic rays. Finding. The question of whether there is a galactic habitable zone and how it may have evolved raises a large number of interesting issues that have not been adequately explored. Areas of Relevant Independent Astronomical Research While some issues are already clearly in the realm of astrobiology, numerous issues in assessing the galactic environment will remain in the domain of pure astronomy in the near future. Among these are the assessment of the heavy element concentration necessary for planet formation; the correlation of the heavy element abundance of the parent star and the existence of planets and determination of the reason for any such correlation; the location of the Sun with respect to the co-rotation radius; the variability of 1   G. Gonzalez, B. Brownlee, and P. Ward. 2001. “The Galactic Habitable Zone: Galactic Chemical Evolution.” Icarus 152:185. 2   P.D. Ward and D. Brownlee. 2000. Rare Earth: Why Complex Life Is Uncommon in the Universe. Copernicus, New York, N.Y. 3   N.J. Shaviv. 2003. “The Spiral Structure of the Milky Way, Cosmic Rays, and Ice Age Epochs on Earth.” New Astronomy 8:39-77. 4   S. Rahmstorf, D. Archer, D.S. Ebel, O. Eugster, J. Jouzel, D. Maraun, G.A. Schmidt, J. Severinghaus, A.J. Weaver, and J. Zachos. 2004. “Cosmic Rays, Carbon Dioxide, and Climate.” EOS Transactions of the American Geophysical Union 85(4): 38-41.

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The Astrophysical Context of Life the density of the interstellar medium in the vicinity of the Sun; and the statistical properties of the interstellar medium of relevance to arbitrary exoplanets and their host stars. Areas of Potential Interdisciplinary Interaction The issue of a galactic habitable zone raises a raft of interesting questions. Is there an optimal location in the Galaxy? How does one decide? If there is, where is it? How many supernovas are too many, and where in the Galaxy does that zone lie? Can the galactic bulge harbor habitable planets? Can star clusters? Classical habitable zones depend on the presence of liquid water independent of whether there are bugs in that water. In contrast, many of the issues related to a galactic habitable zone cannot be addressed without direct reference to biology. For instance, an attempt to understand where life can comfortably exist and where it will be severely challenged requires knowledge of how life resists and adapts to environmental insults. The question whether modulation of cosmic ray flux can affect climate may sidestep direct issues of biology, but it involves a number of other disciplines. Meteoritics and mineralogy are needed to assess the variation in the cosmic ray flux. Other means of assessment should be explored. Dating of ice ages is an important ingredient, involving climatology, paleoclimatology, and ice-age geology. Because cosmic rays can affect the ionization state of the atmosphere, their modulation as characterized by astronomers should be investigated by atmospheric chemists and photochemists. In general, the topic of galactic habitability requires an interchange among all these disciplines as well as among cell biologists, microbiologists, and molecular biologists who study thermal and radiation damage to cells and genomes. One relevant task is to assess the potential significance of biomolecular damage induced by cosmic rays, which are subject to astronomical influences, relative to damage induced by radiation from environmental sources. Also, what if life elsewhere is not based on DNA? For completeness, the committee mentions the possibility of the transport of life between stars, or interstellar “panspermia.” The possibility of the interchange of microbes between planets, Mars, and Earth has been studied; the conclusions are somewhat optimistic if microbes can be shielded within rocks of centimeter size.5,6 The issue of transport of life between stars, while enticing, does not appear to the committee to be an especially fruitful topic at this time. The transport times are expected to be long, the radiation doses high, and the probability of planet-fall small.7 In any case, this notion just puts off the ultimate question, how the transition from chemistry to biochemistry occurred (see the section “Prebiotic Chemistry and Photosynthesis”). There is, as yet, no indication of an environment more hospitable for the origin of life than Earth. A bright idea might render the transport of life between the stars fruitful, but the committee does not consider it further in this report. Missions, Role of Other Agencies Missions to characterize the local interstellar medium (ISM) through which the Sun has passed and will pass in the future are relevant. The keys to characterizing the three-dimensional morphology, 5   National Research Council. 1998. Evaluating the Biological Potential in Samples Returned From Planetary Satellites and Small Solar System Bodies. Space Studies Board. National Academy Press, Washington, D.C. 6   C. Mileikowsky, F.A. Cucinotta, J.W. Wilson, B. Gladman, G. Horneck, L. Lindegren, J. Melosh, H. Rickman, M. Valtonen, and J.Q. Zheng. 2000. “Risks Threatening Viable Transfer of Microbes Between Bodies in Our Solar System.” Planetary and Space Science 48:1107. 7   H.J. Melosh. 2003. “Exchange of Meteorites (and Life?) Between Stellar Systems.” Astrobiology 3:207.

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The Astrophysical Context of Life densities, and temperatures of the local ISM are (1) high-resolution spectroscopy and (2) access to strong resonance lines. The ultraviolet (UV) has many strong resonance lines, but it requires going above Earth’s atmosphere, and unfortunately, the only two high-resolution spectrographs in space are in questionable condition. The de-orbiting in a few years of the Hubble Space Telescope (HST) is under active consideration, and the Far Ultraviolet Space Explorer (FUSE) is near the end of its active life. The Cosmic Origins Spectrograph designed for HST may yet be installed in a servicing mission, or it might be launched as a free flyer. The European Space Agency might fly a UV mission with suitable resolution sometime after 2008. Missions that could better characterize the cosmic ray spectrum—especially at low energies, where solar modulation is strong but variable—would be useful. A study of lunar rocks to determine the record of cosmic ray variation in relatively pristine material would be of great interest. Recommendation. NASA should promote the study of topics related to galactic habitability, including (1) correlating stellar heavy element abundance with the existence of planets, (2) characterizing the interaction among stellar winds, the interstellar medium ram pressure, and the resulting cosmic ray flux, and (3) determining which regions of the Galaxy could give rise to and sustain life. COSMIC, SOLAR, AND TERRESTRIAL IRRADIATION Current Work and Gaps The effects of irradiation manifest themselves in many ways. Optical light is a source of energy by way of photosynthesis. UV photochemistry may have played an important role in the prebiotic synthesis of organic compounds on early Earth (see the section “Prebiotic Chemistry and Photosynthesis”). UV radiation, primarily from the Sun, affects molecular structure by, for instance, forming cyclobutane pyrimidine dimers, misconnections in the strands of DNA that interfere with the ability of the molecule to reproduce. UV radiation can also activate transposable genetic elements that are active in gene transfer. High-energy photons (x rays and gamma rays) are a source of ionization damage in cells. The energetic particles generated by the Sun and those arriving from outside our solar system as cosmic rays produce cascades of secondary particles that also induce ionizations in cells, with similar effects. Although incident ionizing radiation must pass through the thick atmosphere of Earth, about 1 percent of its energy will reach the ground as biologically active UV auroral radiation.8 Irradiation is both a mutagen and a selective agent, thus affecting both steps in natural selection. Irradiation can also affect life indirectly by influencing climate. The idea that the evolution of terrestrial and extraterrestrial life is influenced by irradiation sources was presented by Sagan and Shklovskii.9 Contemporary literature often treats UV and ionizing radiation from a parent star as primarily destructive and that from galactic sources only as a potential cause of mass extinctions. The case can be made, however, that the role of irradiation extends beyond these destruction scenarios and that irradiation has been significantly involved in the origin and evolution of life. The significance of the irradiation environment depends on, among other things, the proportion of 8   D.S. Smith, J. Scalo, and J.C. Wheeler. 2004. “Transport of Ionizing Radiation in Terrestrial-like Exoplanet Atmospheres.” Icarus 171:229-253. 9   C. Sagan and I.S. Shklovskii. 1966. Intelligent Life in the Universe. Holden-Day, San Francisco, Calif.

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The Astrophysical Context of Life cellular mutation caused by (1) cosmic and geological background radiation (see below), (2) nonirradiative, exogenous factors, and (3) other factors that contribute to diversity, such as lateral transfer of genes, gene duplication, and the evolution of developmental systems involving DNA, cellular and organismic structure, and social and ecological interactions. The relative significance of these various factors will undoubtedly change as life evolves from a primitive state to more sophisticated biochemistries. There are hints that irradiation has interacted with life for a very long time. Mechanisms specific to the repair of irradiation-induced damage are found in organisms from prokaryotes to humans. The mechanisms involved in the ancient process of lateral gene transfer and the more recent process of meiosis are often the same as those involved in repair of DNA damage due to UV and ionizing radiation. That early organisms were already subjected to UV radiation is suggested by the fact that both obligately and facultatively anaerobic bacteria show intrinsic resistance to UV damage and use photoreactivation to repair UV-induced pyrimidine dimers. Photosynthesis is an important interaction between light and life (see the section “Prebiotic Chemistry and Photosynthesis”). The detection of cyanobacterial biomarkers in Archean rocks10 and the genetic sequencing of major bacterial families11 suggest that the five major photosynthetic lineages and oxygenic photosynthesis arose by the mid-Archean, 2.8 to 3.0 billion years ago, and perhaps much earlier (although one of the phyla, the green no-sulfur bacteria, may have acquired parts of the photosynthetic machinery from the other phyla only 2.3 billion years ago12). There are extremely radiation-resistant microbes, such as Deinococcus radiodurans, that contain a large (but not exhaustive) suite of radiation repair mechanisms.13,14 All of these facts point to an important, early, and ongoing role for radiation in the evolution of life on Earth, including a role in issues of habitability. It is natural to suspect that analogous processes will occur for life on planets with other host stars. Finding. Optical, UV, and ionizing radiation have had a significant influence on life from the early stages in its evolution on Earth, and this will probably be so for exoplanets that harbor life. ARC proposes to study the effects of various forms of radiation on the survival of life in extreme environments and to examine specific biota for radiation resistance by doing exposure experiments. The Search for Extraterrestrial Intelligence Institute (SETI) will consider iron as a UV blocker and study the survival of organisms in the high-UV environment of Chile but not in the broader astronomical context of a young Sun or a host star of another stellar type. The Virtual Planetary Laboratory (VPL) is beginning to study the effects of illumination of planetary atmospheres by stars of various types. Otherwise, the topic of astronomical irradiation is underrepresented in the efforts of the current NAI teams and of the Exobiology program. 10   J.J. Brocks, G.A. Logan, R. Buick, and R.E. Summons. 1999. “Archaean Molecular Fossils and the Early Rise of Eukaryotes.” Science 285:1033-1036. 11   J. Xiong, W.M. Fischer, K. Inoue, M. Nakahara, and C.E. Bauer. 2001. “Molecular Evidence for the Early Evolution of Photosynthesis.” Science 289:1724-1730. 12   J. Raymond, O. Zhaxybayeva, J.P. Gogarten, S.Y. Gerdes, and R.E. Blankenship. 2002. “Whole-Genome Analysis of Photosynthetic Prokaryotes.” Science 298:1616-1620. 13   J.R. Battista. 1997. “Against All Odds: The Survival Strategies of Deinococcus Radiodurans.” Annual Review of Microbiology 51:203-224. 14   “Deinococcus Radiodurans—A Radiation-Resistant Bacterium.” Available at <http://www.usuhs.mil/pat/deinococcus/index_20.htm>. Accessed on April 26, 2005.

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The Astrophysical Context of Life Areas of Relevant Independent Astronomical Research The characteristics of host stars, including the Sun, when they are young and life might first form need to be better understood. There are indications from the study of solar analogues—that is, stars like the Sun at different stages in their evolution—that high-energy chromospheric activity and stellar winds were much more intense in the past. In addition, young stars are more susceptible to flares and variability. This irregular behavior might have contributed to temporal variability of the environment and hence to genetic diversity (see the section “Molecular Evolution in a Variable Astronomical Context”). The fluctuating radiation environment needs to be better characterized for a range of stellar types. Consideration should be given to the spectral distribution at the source and after transmission through various types of planetary atmospheres in order to evaluate the effect on atmospheric structure and chemistry, climate, and potential surface biota. Sporadic external events like supernovas15 and gamma-ray bursts16 can affect biological processes by brute extinction if they are sufficiently close and intense, but such events will be rare. Exposures to the light from supernovas last only weeks to months, and the most intense stage of gamma-ray bursts lasts only tens of seconds. Only half the planet would be exposed, and even then life in sheltered environments might survive. To quantify other, more subtle possible biological issues, it is necessary to determine by direct or statistical methods the rate of occurrence and the spectral output of various astronomical sources of potential biological significance. As an example, a supernova explodes in our Galaxy about every 100 years. The number of explosions near a given planet increases as approximately the distance squared in the flat plane of the galactic disk. A typical supernova would have to be very close, perhaps a parsec, to beat the solar UV background at Earth, and such events are very unlikely.17 More distant supernovas could still affect outer moons in our solar system, where the solar flux is smaller, or planets around a dimmer, less UV-powerful star. Even more distant supernovas might affect life on a planet by producing cosmic rays directly or by impacting the astrosphere of a star and allowing more ambient cosmic rays to reach the planet. Exposure to the short-term irradiation of a nearby supernova is likely to have a very different effect than immersing a solar system in the subsequent supernova remnant, which would be characterized by efficient particle acceleration. If a supernova remnant envelops a planetary system, the ambient cosmic ray flux could be enhanced for 10,000 years or more. There are issues surrounding the formation and propagation of associated cosmic rays that would determine the exposure of a life-bearing planet to ionizing particle radiation that are still not well understood. Finding. Life on a young planet could be exposed to an intense, intrinsically variable irradiation field, and a variety of galactic sources might affect the UV, ionizing radiation, and particle flux incident on a planet. Recommendation. NASA, other funding agencies, and the research community should devote funding and effort to characterizing the UV, ionizing radiation, and particle flux incident on evolving, potentially life-hosting planets and moons. 15   N. Gehrels, C.M. Laird, C.H. Jackman, J.K. Cannizzo, B.J. Mattson, and W. Chen. 2003. “Ozone Depletion from Nearby Supernovae.” Astrophysical Journal 585:1169-1176. 16   J. Scalo and J.C. Wheeler. 2002. “Astrophysical and Astrobiological Implications of Gamma-Ray Burst Properties.” Astrophysical Journal 566:723-737. 17   Gehrels et al. Op. cit.

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The Astrophysical Context of Life Areas of Potential Interdisciplinary Interaction If photon and particle irradiation plays a role in the chemistry and structure of the atmosphere and the climate of a host planet and in the origin, evolution, and sustainability of life on that planet, then characterizing the significance of that radiation means that the biological, atmospheric, and geological influences need to be understood. For instance, one must know the state of the Archaean atmosphere—that is, whether it contained sulfur or aerosol screens—in order to evaluate the intensity of surficial UV. The effect of irradiation on climate requires careful modeling of the time-dependent atmospheric chemistry and structure. One needs to know the biological dose rates for a spectrum of mutagenic responses to evaluate whether a particular fluctuating chromospheric emission or a nearby supernova can have a significant effect on biological processes. The study of astronomical irradiation sources must be closely coupled to the other areas of astrobiology in order to properly assess the rate of significant events and their impact. Ultraviolet and Ionizing Radiation Damage and Repair One area where photon and particle irradiation intersect with biology is the processes associated with radiation damage and repair. Photon and particle irradiation are two of many sources of exogenous damage to genomes. Irradiation can cause direct damage in the form of pyrimidine dimers, single- and double-strand breaks, cross-strand exchange, and multiple lesions. Irradiation can also produce indirect damage by forming oxygen radicals,18 as can other processes, both exogenous and endogenous. Irrespective of their source, reactive oxygen species cause damage to proteins, lipids, and DNA. Survival of a cell exposed to radiation depends on the extent of genomic damage during irradiation, the efficiency of repair, and the extent of cellular damage inflicted during recovery by metabolism-induced oxidative stress. While irradiation can cause some damage similar to endogenous effects, it also produces damage such as cross-strand attachments and multiple lesions, for which there is no endogenous analogue. The repair processes for this unique damage must have evolved relatively independently of repair processes for endogenous damage. Understanding the genetic history of these repair processes unique to radiation may give new clues to the evolution of life on Earth. Irradiation damage can be so severe as to lead to apoptosis, but it can also be one contributor to unrepaired damage and hence to mutation and evolution. An important source of mutation is replication error. This must have been especially true early in the evolution of life, when proofreading was less efficient. In modern life, endogenous damage and replication errors are repaired with remarkable efficiency. The rate of damage due to toxic reactive oxygen species (hydroxyl radicals, hydrogen peroxide) produced as a consequence of cellular metabolism is estimated to be higher by orders of magnitude than that due to current background levels of ionizing radiation.19 On the other hand, the net rate of mutation after repair mechanisms have done their work is roughly equivalent for radiation and endogenous effects. This is why one avoids too many chest x rays. The difference is presumably due to the very high efficiency of repair processes for replication error and endogenous damage compared with the less efficient repair of damage by ionizing radiation. Selection for the ability to repair errors in replication, chemical damage, irradiation damage, and other lesions in the genetic material would have been intense from the very beginnings of life. Studies of 18   G. Hanel, B. Gstir, S. Denifl, P. Scheier, M. Probst, B. Farizon, M. Farizon, E. Illenberger, and T.D. Märk. 2003. “Electron Attachment to Uracil: Effective Destruction at Subexcitation Energies.” Physical Review Letters 90(18): 188104. 19   J.A. Imlay. 2003. “Pathways of Oxidative Language.” Annual Review of Microbiology 57:395.

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The Astrophysical Context of Life the regulation of repair processes are ongoing in many laboratories, using the latest techniques in high-throughput analysis of transcription and protein expression. A great deal of additional biochemical experimentation, coupled with molecular phylogenetic studies, will be required to learn more about the origins of DNA repair pathways, including those that are unique to the repair of irradiation damage. In principle it should be possible to gain a reasonable understanding of DNA repair pathways in the last common ancestor, but learning about DNA repair at earlier stages, characterized by rampant gene swapping, will be much more difficult. A better understanding of the origins, nature, and control of DNA damage repair is clearly important for understanding the response of organisms to geological background radiation (see the section “Interstellar and Protostellar Nebular Chemistry”), solar UV, and cosmic ionizing radiation. However, these studies of radiation damage repair are also important for understanding biomedical problems, including the genesis and treatment of cancer, genetic diseases, and certain aspects of aging. Solar UV irradiation is the most powerful carcinogen to which humans are routinely exposed.20 The primary danger of exposure of humans to high-energy particles in space is an enhanced risk of cancer. Thus, certain areas of interest to astrobiology overlap with subjects of fundamental interest to NIH. NASA and the National Cancer Institute fund the development of nanoscale biomedical technologies that detect, diagnose, and battle radiation exposure, cancer, and other diseases at the cellular level. Consideration could also be given to the effect that astrophysical irradiation has on molecules other than DNA—for instance, on the structure of protein molecules. Finding. Understanding the origins, nature, and control of DNA damage repair is also important for understanding the response of organisms to solar and cosmic UV and ionizing radiation and to geological background radiation. These studies are also important for understanding certain biomedical problems, including the genesis and treatment of cancer, genetic diseases, and certain aspects of aging. Recommendation. NASA, other funding agencies, and the research community should devote funding and effort to exploring the variability of damaging UV and ionizing radiation over the course of life on Earth and how such conditions might be manifested on other life-hosting bodies. Radiation Health and Safety One area where cosmic irradiation intersects practical issues of health and safety is the exposure of humans in space to photon and particle radiation. This is an issue for astronauts serving on the International Space Station, and former NASA administrator Sean O’Keefe listed it as one of the three major open problems (along with propulsion and adequate on-board power) facing human exploration of Mars. In the absence of adequate shielding, astronauts on a return trip to Mars would receive something like 400 times the yearly average dose for U.S. citizens. Essentially every cell in the human body would be hit once by an ionizing photon, proton, or heavier particle. NASA funds ground-based experiments using radiation sources and analysis tools like PET and MRI scans and DNA sequencing to better understand the effects when living tissue is exposed to cosmic radiation. Such experimentation is taking place in the Space Radiation Laboratory at Brookhaven 20   A. Sarasin. 2003. “An Overview of the Mechanisms of Mutagenesis and Carcinogenesis.” Mutation Research/Reviews in Mutation Research 544:99-106.

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The Astrophysical Context of Life National Laboratory. A principal focus of these studies is the interaction with tissue of energetic particles from cosmic radiation, about which much less is known than the interaction with tissue of particles from natural terrestrial radiation, which are mostly gamma rays. The goal is to better understand the biological mechanisms of radiation damage and repair. At issue are questions such as whether exposure to proton damage will weaken the response of cells to occasional heavy ions like iron and whether proton irradiation will trigger cell defense mechanisms, making them more robust to heavy ion damage. Finding. There are areas of potential interaction between astronomers who study the sources and composition of cosmic radiation and physicists and biologists who are attempting to understand the nature of irradiation damage in the context of human survival in space. Irradiation and Geology Heat from natural radioactivity plays a role in the geological forces that shape the Earth, and those geological forces in turn affect the distribution of natural long-lived radioactive elements. The geological record may also provide indications of past astronomical events. One issue that combines astronomy and geology is the question of whether other habitable planets will have plate tectonics. Plate tectonics might be an inevitable outcome for rocky planets that have substantial internal heat sources and liquid water at their surfaces to cool magma and lubricate plate movement. An internal heat source does seem to be a necessary requirement for a habitable planet, since some form of volcanism is necessary to recycle carbonate rocks, as well as other life-supporting elements like nitrogen and phosphorus. An internal heat source, however, is something that is almost unavoidable on any large planet. Planets that formed too early or too late in the history of the Galaxy may lack the radioactive elements (uranium, potassium, and thorium) that help to generate heat within Earth’s interior, but roughly half the geothermal heat flow comes from heat that was generated during accretion. A planet that was somewhat more massive than Earth might not need any radioactive elements to maintain plate tectonics. Radiation exposure from sources in the crust varies strongly with time and position on the surface owing to geological effects and the chemical evolution of a planet’s crust, oceans, and atmosphere. The chemical, geochemical, and mechanical processes that lead to concentrations of natural radioactivity include the fractional crystallization of magma chambers, concentration of uranium-bearing sediments in placer deposits, recycling of eroded crustal materials, and precipitation of dissolved uranium at oxidation-reduction fronts. All of these processes are affected by a planet’s geological activity, including volcanism, tectonics, and erosion. Differences in planetary parameters can thus combine to influence the radiation environment in which the biota live and evolve. Through time, Earth’s crust has become steadily enriched in elements with large ionic radii, which tend to exclude these elements from the crystal structures of minerals, such as olivine, that crystallize first in a magma melt. These elements include uranium, potassium, and thorium, the primordial radionuclides responsible for much of the natural radioactivity on Earth. One of the chain of decay products of uranium is the radioactive gas radon (86Rn). The alpha decay of radon to polonium is the second leading cause of lung cancer after smoking. Radiation doses to organisms living in contact with rocks will depend on the radionuclide concentrations and the time since those radionuclides were first formed. Geological models that would help to understand under what conditions volcanism and tectonics are possible in exoplanets would be very valuable in general. Models could be also developed for the concentrations of long-lived radioactive species on Earth and on exoplanets, considering the recycling

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The Astrophysical Context of Life of continental crust materials under a variety of weathering and erosion rates, subduction rates, sedimentation, and initial radionuclide concentrations. Dose rates from geologic materials vary spatially over at least two orders of magnitude on Earth today. The processes outlined above have acted to concentrate radioactive elements into the Earth’s crust and to create radiological hot spots from an initially homogeneous Earth.21 Such processes have led, for example, to rich sedimentary uranium ore deposits in South Africa, Texas, and Australia, as well as to the formation of the extinct Oklo natural nuclear reactor in the nation of Gabon, in western Africa. At a somewhat milder, but still significant level, the state of Kerala, in India, has one of the highest levels of natural radioactivity on record. The dose rate of about 10 mSv per year is about 10 times the worldwide background. A study of DNA mutations in Kerala showed not only that the mitochondrial DNA (mtDNA) has higher levels of germ-point mutations but also that the radioactivity accelerates mutations at nucleotide positions that have been evolutionary hot spots for at least 60,000 years.22 The question of how evolution might respond to the spatially variable radiation environment as it evolved on Earth and as it would evolve on other planets must center on the relative significance of mutations induced by background radiation and those caused endogenously. Finding. Natural background radioactivity is expected to vary with time and space on Earth and other geologically active bodies. The degree and variation of the background radioactivity will be a function of geological activity, including volcanism, tectonics, and erosion. Recommendation. NASA, other funding agencies, and the research community should devote funding and effort to the development of planetary geology models to better understand the presence and nature of volcanism and tectonics on other planets as a function of the age of formation of the planet, the initial concentration of long-lived radioactive species, the accretion history, and the mass of the planet. Recommendation. NASA, other funding agencies, and the research community should devote funding and effort to geological field work and models (1) to characterize the rates of damage and mutation due to background radioactivities on evolving Earth and other potentially life-hosting bodies and (2) to compare them with the rates due to other endogenous and exogenous radioactivities. In addition to their insults to the biosphere, cosmic rays produce observable signatures of their present and past intensity at Earth. Cosmic ray nuclear interactions transmute elements in the atmosphere, producing cosmogenic nuclei, some of which are radioactive. It is this process that is the source of 14C and provides the means for carbon dating. In addition to this short-lived isotope, longer-lived species are also created cosmogenically; these precipitate out of the atmosphere and are stored in natural archives such as ice cores and ocean sediments, which contain a record of certain aspects of the astronomical environment. For example, the measured concentrations of 10Be (with a half-life of 1.5 million years) in ice cores give a record of the cosmic ray flux incident on Earth for the past 100,000 years. The concentrations vary as the solar cycle modulates the protective heliosphere. Cosmic rays can also be modulated during 21   G. Faure. 1986. Principles of Isotope Geology, 2nd ed. John Wiley and Sons, New York, N.Y. 22   L. Forster, P. Forster, S. Lutz-Bonengel, H. Willkomm, and B. Brinkmann. 2002. “Natural Radioactivity and Human Mitochondrial DNA Mutations.” Proceedings of the National Academy of Sciences U.S.A. 99(21): 13950-13954.

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The Astrophysical Context of Life Earth and the Moon. Better Mars impact age dates should also become attainable in the context of the President’s new plan. Sample return by Stardust50 from Comet Wild 2 in January 2006 will give fresh insight into the composition of comet material that might be delivered to Earth. The ejection of comet interior material expected from the Deep Impact mission,51 scheduled for July 2005, will allow measuring the composition of the interior of the crater and its ejecta in Comet 9P/Tempel 1. An important complement to spacecraft missions is terrestrial drilling programs. Relevant activities are supported by the NAI, Japanese research organizations, and the Agouron Institute, a nonprofit research organization in Pasadena and La Jolla that sponsors innovative research in geobiology. Recommendation. NASA should develop missions that return to the Moon to acquire more lunar samples to help determine when the “impact frustration” of life’s origin ended by sampling more sites—particularly sites that are older than the six sites sampled by the Apollo astronauts and the three sites sampled by the Soviet robotic sample-return missions and, especially, the oldest and largest impact basin on the Moon, the South Pole-Aitken Basin. PREBIOTIC CHEMISTRY AND PHOTOSYNTHESIS Current Work and Gaps A major unsolved problem of astrobiology is the transition from prebiotic chemistry to life. This issue abuts with astronomy because, as outlined in the section “Interstellar and Protostellar Nebular Chemistry,” accretion from the interstellar medium to protostellar systems and thence to planet surfaces is one possible source of the biomolecules that may be the raw material from which life arose. An important question faced by the field of prebiotic chemistry is whether astrochemistry is a contributor to the origination of life or a detriment to it. Over 130 compounds have been detected to date (see the section “Interstellar and Protostellar Nebular Chemistry”), and the list continues to grow as the sensitivity of detection improves. Embedded within the list are numerous compounds of clear biological interest—but it remains unclear whether these compounds could have been transported intact to the surface of early Earth in significant amounts and, even if they were, whether they would have been important in subsequent chemical transformations leading to the origination of life. The central unsolved problem of prebiotic chemistry is that all such experimentally observed syntheses result in complex mixtures of compounds—tarry gunk, in short. In contrast, replicating chemical systems would seem to require for their emergence simple mixtures of a few relatively pure compounds. The low-temperature ion-molecule chemistry that mediates astrochemical synthesis confronts kinetic barriers to some reaction pathways in the low temperature of the interstellar medium but nevertheless generates a large range of compounds formed from small numbers of carbon, hydrogen, nitrogen, and oxygen atoms. Until interstellar chemistry is better understood, the problem of combinatorial chemical complexity will not be fully solved. This problem is not unique to astrochemistry. The classic example in prebiotic chemistry is the formose reaction, in which formaldehyde under alkaline aqueous conditions spontaneously forms sugars—not just the ribose needed to make RNA but every possible isomer of every sugar, 50   “Stardust: NASA’s Comet Sample Return Mission.” Available at <http://stardust.jpl.nasa.gov/>. Accessed April 27, 2005. 51   “Deep Impact.” Available at <http://deepimpact.jpl.nasa.gov/>. Accessed April 27, 2005.

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The Astrophysical Context of Life sugar alcohol, and sugar acid. The synthesis of mixtures of stereoisomers is merely a particularly difficult subset of this larger problem: the synthesis of intractable mixtures in which the biologically desirable compounds are but a tiny proportion of the material. Why is the synthesis of complex mixtures such a problem? Consider the problem of the prebiotic synthesis of a genetic polymer such as RNA. We know from molecular studies of cellular biochemistry, including the structure of the ribosome, that RNA must have played a key role at some stage in the early evolution of life, but the origins of the RNA world remain obscure, and the synthesis of a polymer of the complexity and chemical fragility of RNA remains a daunting problem, made much worse by the fact that an RNA-like polymer assembled from nucleotides formed with a mixture of different sugars would be of little use. If the presence of L-isomers in the prebiotic world had the same effect it does in current biochemistry, even the presence of the ribose stereoisomer L-ribose (instead of the normal D-ribose) would be fatal, as such isomers are known to poison nonenzymatic, template-directed RNA replication in laboratory studies. The presence of other sugars would lead to the synthesis of polymers with different sugars at different positions in the polymer chain. Such molecules are probably not replicable. Even if they were, this positional information could not be copied, making the emergence of a self-replicating autocatalytic system difficult, if not impossible. There is no known pathway that would lead to the prebiotic synthesis of chemically homogeneous nucleotides. To address the problem of the origin of life in a credible way, the difficulties associated with accreting interstellar matter must be tackled and not ignored. The problem has generated two philosophically distinct responses. One camp has been convinced that further study would reveal chemical pathways, catalysts, and purification and concentration processes that would resolve the issue, such that the formation of undesirable mixtures could either be avoided in the first place or resolved subsequently. An example might be the recent discovery by Ricardo et al.52 that the addition of borate minerals favor the synthesis of pentose sugars, including ribose. The second response has been to argue that processes leading to such complex mixtures were not relevant to the origin of life, and that self-organizing autocatalytic and/or surface-catalyzed processes starting from the simplest, most basic precursors (H2O, CO2, CH4, NH3, and so forth) would produce primitive metabolic systems, which over time would grow in complexity until biomolecules complex enough to give rise to cellular life were generated in situ. Neither approach has fully solved the problem, but in recent years several advances have been made through novel experimental approaches. There is a growing appreciation of the useful potential of mineral surface catalysis, and its coordination with ions in solution, for both the primary synthesis of small-molecule building blocks and their subsequent reaction to generate larger and more complex molecular structures. It is clear that there is a great deal to be done in this area and that many new ideas will be needed to solve this central problem. The NAI could play a crucial role by fostering creative new approaches to this problem, for until it is solved we will not know the relevance of astrochemistry to the origin of life. Finding. There is no known pathway that would lead from complex interstellar molecules to the prebiotic synthesis of chemically homogeneous nucleotides. Ultimately, life requires a continuous input of chemical energy and a mechanism for forming the required building blocks from simple precursors. This process must have begun fairly early in the history of Earth’s biosphere. Oxygenic photosynthesis is currently the predominant source of energy 52   A. Ricardo, M.A. Carrigan, A.N. Olcott, and S.A. Benner. 2004. “Borate Minerals Stabilize Ribose.” Science 303:196.

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The Astrophysical Context of Life and of reduced carbon compounds for life on Earth. When and how did this capacity emerge? Presumably it involved a progression of simpler steps that preceded the highly complex system of today’s oxygen-producing phototrophs and the structured biosphere that is dependent on them. We would like to know more about the possible chemistries and steps leading to the development of oxygenic photosynthesis and the corresponding changes in the biosphere that occurred during this transition. A terrestrial planet offers opportunities for an additional universe of chemistry not available in interstellar space or protostellar nebulae: chemistry in aqueous solution. Oceans, lakes, and ponds could contain a suite of organic chemicals and the ionic residues of weathered minerals. This mixture of organic compounds, cations, and a flux of photons of appropriate wavelengths to excite chemical bonds could produce new compounds, some of which might be useful to early life forms; other compounds might eventually return to the atmosphere or be decomposed in another part of the ocean. For example, tars and recalcitrant materials might be deposited on exposed surfaces, where they could be photodegraded to small molecules that could return to the upper atmosphere to participate anew in polymerization reactions. An alternative route might involve chemical processes at hydrothermal systems. Heat and pressure at volcanic spreading zones could provide free energy and catalytic conditions for very different reactions than might occur at the ocean surface. Such a system of linked processes located in different parts of the planet might form prebiotic chemical cycles of the biogenic elements that could provide a continuous turnover of feedstocks for early life forms. Recommendation. NASA, other funding agencies, and the research community should devote funding and effort to better understand how carbon, nitrogen, and sulfur cycles might work on a prebiotic planet with an ocean and an incident flux of photons and particles, and how these cycles might couple with primitive life forms to provide feedstocks for their formation and energy for their metabolism. A related issue is the production of the thermodynamic gradients that are required to sustain metabolic processes. The thermodynamic gradients that drive the present biosphere are largely sustained by atmospheric oxygen, itself a product of photosynthesis. The photosynthetic energy initially used in the synthesis of compounds can be remobilized by reoxidizing the compounds or products derived from them at locations and times remote from the initial synthesis. Even the metabolism of deep-sea vent communities now depends on the supply of oxygen from photosynthesis. While the concentration of oxygen in the atmosphere has remained stable over millions of years, the metabolic flux of oxygen is sufficient that the total complement of O2 turns over in about 1,200 years53—an instant in geologic time. This illustrates that an active biosphere would rather quickly consume vestigial thermodynamic energy gradients present in the original charge of organics from space, and primitive metabolic systems would ultimately become dependent on a renewable energetic system. Photons from the central star are the most plausible source of such energy, and photosynthesis of some form is likely to have started early in the history of our biosphere. While it is natural to think of photosynthesis as a biological process, it may be useful to consider that light-driven synthetic reactions may have preceded life. The solution-phase photochemical transformation of organic molecules, especially in combination with ions of transition elements in seawater, could have been driven by the absorption of photons of visible light from the Sun or other host star. Inputs of 53   M. Bender, T. Sowers, and L. Labeyrie. 1994. “The Dole Effect and Its Variations During the Last 130,000 Years as Measured in the Vostok Ice Core.” Global Biochemical Cycles 8:363-376.

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The Astrophysical Context of Life light energy could thus have driven cycling between different redox states of metal ions and organic compounds in a prebiotic ocean. The central role of iron and manganese in the molecular mechanisms used by current photosynthetic organisms may give clues to the prebiotic chemistries that preceded biological photosynthesis. Photosynthetic mechanisms of the vast array of photosynthetic organisms of Earth’s biosphere and the evolutionary relationships between these mechanisms has been a major area of research for many decades, an area that beautifully exemplifies the integration of disciplines, from solid state physics through biochemistry to ecology and Earth-system science. Arizona State University, one of the first teams of the NAI, focused on the evolution of photosynthesis and its role in Earth’s history. The importance of understanding the photochemistry that could occur on a prebiotic planet cannot be understated. Areas of Relevant Independent Astronomical Research Interstellar chemistry itself may offer some alternative perspectives on the problem of tars and recalcitrant matter that may not be conducive to the origin of life. Unlike typical organic reactions, which take place at room temperature or higher, most chemical reactions in interstellar gas must take place at between 10 K and 100 K. Such reaction barriers will limit the pathways normally available at higher temperatures. In this sense, interstellar chemistry is more selective than terrestrial chemistry. One example is found in the interstellar isomers that have the general chemical formula C2H4O2. While methyl formate (HCOOCH3) is a very abundant molecule in dense clouds with a spectrum that exhibits hundreds of lines, glycolaldehyde (CHOCH2OH) and acetic acid (CH3COOH) are barely detectable in the same regions. Glycoaldehyde is a good sugar precursor, but methyl formate has no obvious utility in biochemistry. Finding. The kinetically controlled chemistry in the interstellar medium may lead to selection of products that would not be favored under conditions of thermodynamic control. In addition to better understanding the inventory of compounds available from the interstellar medium, much work must be done to understand what fraction of these compounds survives the accretion processes into protostellar nebulae and thence onto planetary surfaces and how long they survive on the planetary surface. The first two challenges are in the realm of astronomy, the last is undoubtedly in an interdisciplinary realm because it requires an understanding of photochemistry under the influence of the host star flux and myriad other physical and chemical processes. The fundamental question is whether organic compounds present in interstellar clouds contribute to the organic chemistry of presolar nebulas and then, perhaps in a series of stages, to a young planet’s inventory of organic compounds conducive to the formation of life. These issues overlap and draw on many of the topics discussed throughout this document. Questions of material transport and processing (see the section “Interstellar and Protostellar Nebular Chemistry”) are amenable to study by computational modeling at a variety of stages, from the condensation of molecular clouds into presolar nebulas to the impact of comets onto inner rocky planets (see the section “Bombardment”). Laboratory studies can also contribute at a variety of stages. Spectra measured in the laboratory are essential for the interpretation of radioastronomy observations (see the section “Interstellar and Protostellar Nebular Chemistry”), and laboratory studies of chemical transformations during high-velocity impacts provide essential data for the modeling of cometary impact processes (see the section “Bombardment”). Infrared spectra data of dusty circumstellar disks are already beginning to provide interesting information.

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The Astrophysical Context of Life Recommendation. NASA, other funding agencies, and the research community should devote funding and effort to carry out coordinated theoretical, laboratory, and observational studies of interstellar chemistry, accretion, condensation, and transport processes to determine the inventory of compounds that was delivered to a young planet, when they were available, where they were available, and in what quantities. Areas of Potential Interdisciplinary Interaction Even if the inventory of astrochemical compounds on the surface of a young planet could be determined, the main challenge is to determine the chemistry that would lead to life. There are relatively few established chemists working in the area of prebiotic chemistry, and yet these few have recently made important advances, such as the synthesis of pyrimidines,54 of ribose,55 and of alternatives to RNA.56 The committee feels that encouraging creative chemists to enter this field and bring in new approaches is the only way for progress to be made—certainly, abandoning the field will not accelerate progress. This work should complement, not compete with, efforts to explore the chemistry of environments such as cometary ice crusts, which may shed light on early nebular chemistry. Consideration could also be given to the assembly of molecules by mechanisms other than gene mutation.57 There is potential here to explore fundamental principles relating to solid-phase biochemistry (e.g., using clay minerals) on the one hand and solution chemistry on the other and to explore how the galactic environment might impact molecular diversity using synthesis routes other than DNA. This regime might best first be explored with models. There should be support for studies to explore how diversity could be generated within prenucleotide chemical reactions and how nongenetic selection might take place, perhaps through basic structural principles such as energy and architectural constraints. The power of molecular biology, including directed evolution of catalytic RNAs and in vitro synthesis of proteins, could be leveraged in this context. Recommendation. NASA and other interested agencies should develop and support programs that encourage basic research on prebiotic chemistry. Among the interdisciplinary issues relevant for prebiotic chemistry are the effects of photochemistry on the production of biogenic compounds; physical and chemical processes such as evaporation, absorption on mineral surfaces, polymerization within membrane vesicles, and photopolymerization on ices that would concentrate the abundances of key precursors to life; and studies of energy inputs that would establish the thermodynamic gradients that lead to life. More attention should be given to phosphorous chemistry as well as organic chemistry. Phosphorus is key to life as we know it, although relatively obscure in terms of its astronomical nucleosynthesis. Ions of many elements now essential for life may have played key catalytic roles in primordial chemistry. Transition elements (iron, manganese, copper, and cobalt) could have played important roles in redox 54   J.P. Ferris, R.A. Sanchez, and L.E. Orgel. 1968. “Studies in Prebiotic Synthesis. III. Synthesis of Pyrimidines from Cyanoacetylene and Cyanate.” Journal of Molecular Biology 33(3): 693-704. 55   A. Ricardo, M.A. Carrigan, A.N. Olcott, and S.A. Benner. 2004. “Borate Minerals Stabilize Ribose.” Science 303:196. 56   A. Eschenmoser. 1994. “Chemistry of Potentially Prebiological Natural Products.” Origins of Life and Evolution of the Biosphere 24:238-240. 57   D.E. Ingber. 2000. “The Origin of Cellular Life.” BioEssays 22:1160-1170.

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The Astrophysical Context of Life reactions and could have played a role similar to that currently played by oxygen in producing thermodynamic gradients. Astronomical studies can help to constrain the abundance and distribution of critical trace elements (phosphorus, iron, manganese, copper, and cobalt) and the spectrum and intensity of light from a variety of host stars early in their evolution, all of which could affect the processes of photochemistry described here. To further these studies, stronger links need to be developed between astrochemistry and organic chemistry to evaluate the mechanisms of gas-phase chemistry, gas-phase/surface chemistry, radical chemistry, and photochemistry in the production of interstellar molecules. Interstellar chemists and planetary scientists need to interact closely in order to make better connections between interstellar, cometary, and meteoritic molecular abundances, including isotope ratios. Better connections need to be made between chemists and those modeling planetary disks in order to properly evaluate transport of the chemical products to the planet surface. Finding. Chemists, atmospheric scientists, biologists, and geophysicists need to interact in order to understand the chemical environments and geochemical cycles of carbon, oxygen, nitrogen, sulfur, phosphorus, and metal ions on prebiotic Earth and how these processes might be related to the formation of biomolecules and primitive metabolic systems. Recommendation. NASA, other funding agencies, and the research community should devote funding and effort to pursue studies of abiotic photochemistry in concert with astronomical sources of trace elements and energy to determine whether trace elements play a role in photochemical sources of organic compounds and/or high-energy activated compounds. One distinguishing characteristic of terrestrial life is that the function of biopolymers relies on the exclusive one-handedness of their monomeric components—that is, all protein amino acids have an L-configuration, while sugars in RNA, DNA, and polysaccharides have a D-configuration. Substitutions along the polymers with enantiomers of opposite handedness usually result in loss of function. The unknown origin of this homochirality has been the subject of debate, speculation, and studies for well over a century since Pasteur first elucidated the chirality concept. The scope and rationale of these investigations have paralleled a more general query about the origin of life: Was biological homochirality the product of prebiotic processes or the result of selection brought about by life itself? Was it due to choice or chance? Was it at first broad-scaled or of limited extent? A trait so pervasive as to define life processes has elicited many universal theories to explain the underlying physical process that could have caused the original chiral symmetry to break. Chiral effects due to randomness and chance; parity violation of subatomic weak interactions, such as in -decay; circular dichroism toward photolyzing light;58 and magnetochiral dichroism of irradiated chiral molecules in magnetic fields59 have been invoked in this context, and some of them have been extensively studied. The finding in meteorites of some amino acids carrying an excess of the L-enantiomer, the same form as in terrestrial protein,60 has further encouraged the idea of a prebiotic origin for chiral asymmetry. 58   J. Bailey, A. Chrisostomou, J.H. Hough, T.M. Gledhill, A. McCall, S. Clark, F. Menard, and M. Tamura. 1998. “Circular Polarization in Star Formation Regions: Implications for Biomolecular Homochirality.” Science 281:672-674. 59   G.L.J.A. Rikken and E. Raupach. 2000. “Enantioselective Magnetochiral Photochemistry.” Nature 405:932-935. 60   J.R. Cronin and S. Pizzarello. 1997. “Enantiomeric Excesses in Meteoritic Amino Acids.” Science 275:951-955.

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The Astrophysical Context of Life Finding. Star-forming regions could provide circular polarization and so, indirectly, relate to the origin of biomolecular homochirality. Recommendation. NASA, other funding agencies, and the research community should devote funding and effort to pursue the unanswered questions about the extent to which the astrophysical environment could have fostered the breaking of symmetry in prebiotic organic pools. Missions, Role of Other Agencies NASA flight missions will contribute by returning comet samples, and sophisticated in situ chemical analysis of icy bodies left over from the formation of the solar system will tell us a great deal about the sources and processing of organic compounds during the early history of the solar system. Both the Terrestrial Planet Finder (TPF) and the Darwin mission will attempt to find earthlike planets and examine them for evidence of life. Atmospheric oxygen, in particular ozone, O3, is the most easily recognizable sign of life on Earth that could be identified remotely. The evidence that this oxygen is biogenic would be strongly bolstered by detecting the presence of a reduced biogenic gas, such as methane. There are substances that could be detected that are associated with life on Earth, such as H2O and CO2, but that need not be biogenic. The issue of false positives remains a serious one. There is also a potential puzzle about the delay in developing an oxygen atmosphere on Earth. Some photosynthetic organisms may have been operating as early as 3.7 billion years ago,61 yet Earth did not develop an oxygen atmosphere as a result of photosynthesis for another approximately 1.2 billion years or so. This raises interesting questions about the biological and geological processes that contributed to this lag. The prevailing theory is that the crust is a very efficient repository for oxygen and that time is required to oxidize soluble Fe2+ to insoluble Fe3+ oxides. The crust eventually gets saturated and further oxygen production increases the atmospheric oxygen. An important question is, then, When is O3 a sign of photosynthesis and when of geological processes? This question is interesting in its own right but also has significant repercussions for the design of TPF and Darwin. It is important to consider other possible atmospheric gases (perhaps CH4 and NO2) that might indicate the presence of a photosynthetic biosphere on another planet with a geological and biological history different from that of Earth. Sample return by the Stardust mission and analysis of the comet impact by the Deep Impact mission (see the section “Bombardment”) will also give insight into prebiotic chemistry. Another relevant body for research on prebiotic chemistry is Titan, whose atmosphere is comparable in column density to that of Earth and is bathed in solar photons—albeit at 1 percent the flux density of Earth. The atmospheric chemistry of Titan is dominated by photochemical reactions involving N2 and CH4 and the consequent production of complex hydrocarbons and nitriles. Since some CO2 exists in the atmosphere, Titan’s atmosphere is often thought of as intermediate between that of Mars and that of primordial Earth, implying abiotic organic synthesis, which is relevant for the origin of microbial life. Models of the photochemistry of the Titan atmosphere and its interaction with surface processes is an active area of research. Because the input of stellar radiation is likely to be irregular owing to frequent flares in young and low-mass stars, one goal would be to study the stochastic chemistry of a simple N2-CO2 atmosphere (including relevant by-products) and its attenuation properties, in order to estimate the surficial and suboceanic flux distribution (in wavelength and time) of a prebiotic 61   M.T. Rosing and R. Frei. 2004. “U-rich Archaean Sea-floor Sediments from Greenland—Indications of >3700 Mya Oxygenic Photosynthesis.” Earth and Planetary Science Letters 217:237-244.

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The Astrophysical Context of Life terrestrial planet. When fully analyzed, the data collected during the passage of the Huygens probe of the Cassini mission through Titan’s atmosphere in January 2005 will offer an initial test of models. Recommendation. NASA should carry out missions to asteroids, comets, moons such as Titan, and, possibly, Saturn’s rings to sample and analyze the surface organic chemistry. MOLECULAR EVOLUTION IN A VARIABLE ASTRONOMICAL CONTEXT Current Work and Gaps As part of their perspective, the University of Washington NAI team asks whether mass extinctions are “fertilizer or poison or both in the garden of complex organisms?” The issue is much broader and more fundamental than mass extinctions. The life processes we witness on Earth now are daunting in their complexity. It is beyond the pale to attempt to predict what life would be like elsewhere, but we can attempt to define basic principles that life would obey, and we can begin to explore the range of variation that is possible, given other astronomical environments and the possibility of, for instance, other coding systems. How might the rate or modes of evolution at the cellular level change if the host star experienced constant flares, as the Sun did in its youth, or if the coding bases did not absorb strongly in the UVC and UVB spectral regions, or if different biochemical pathways were made available or suppressed? Do strong fluctuations in the thermal and radiation environment enhance or suppress the rate of development of complexity at the genomic and cellular level? Which genetic processes are especially robust in, or even best suited for, strongly fluctuating environments? Of fundamental importance is to understand what level of disturbance is beneficial for the origin and development of complexity of life. Is a truly quiescent portion of the Galaxy attainable for any host star, including the Sun, and, even if so, is that the optimal condition for the evolution of complex life? How evolving populations react to environmental variability, especially extreme stress, remains an unsolved problem. The mechanisms underlying the robustness of organisms are diverse; they include error correction machinery at the level of DNA, physiological plasticity at the level of individual traits or behaviors, and hypermutability at the level of entire populations. There are several lines of argument that suggest that diversity and hence evolution might be enhanced by an environment that is complex, whether in space or time or some material properties. Pseudomonas fluorescens evolves rapidly to generate many mutants under novel environmental conditions, resulting in the evolution of niche specialists.62 Directed in vitro and in silico (artificial life) evolution experiments both indicate that genome lengths (one metric of complexity) grow only in information-rich environments.63 The effect of harsh and fluctuating environments on the diversity of ecological communities, especially the “intermediate disturbance” hypothesis—that maximum diversity occurs at intermediate frequencies of disturbance—has been discussed extensively.64 A relevant example may be the apparent increase in mutation rates in stationary-phase cultures experiencing the stress of overcrowding and nutrient starvation. There is 62   P.B. Rainey and M. Travisano. 1998. “Adaptive Radiation in a Heterogeneous Environment.” Nature 394:69-72. 63   C. Adami, C. Ofria, and T.C. Collier. 2000. “Evolution of Biological Complexity.” Proceedings of the National Academy of Sciences U.S.A. 97:4463-4468. 64   P. Chesson and N. Huntly. 1997. “The Roles of Harsh and Fluctuating Conditions in the Dynamics of Ecological Communities.” American Naturalist 150:519-553.

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The Astrophysical Context of Life evidence in mammals that a complex sensory environment triggers the expression of genes responsible for neural plasticity, opening the way for increased neural complexity. Another line of evidence for the role of environmental variability in complexity comes from considering evolution as a learning process. Experiments using neural networks as the phenotype for digital genomes show that learning is more efficient when mutation occurs in bursts rather than at a constant rate.65 Mutations that increase fitness can be regarded as random measurements of the environment and genomes can be regarded as the selection-imprinted genetic memory of past environments.66 Robust modes of inheritance can be resistant to environmental insult but may be limited in the speed with which they are able to adapt to novel environmental conditions, particularly in environments that change over time. Alternatively, some processes controlling inheritance may be adapted to respond to sudden environmental change. An example is the process associated with heat-shock proteins, which acts to buffer phenotypic variability. The result is to hide the effects of mutations, allowing genetic diversity to accumulate. That diversity can then become manifest when the environment suddenly changes as the result of a heat shock or some other insult and the hidden mutations become expressed in the phenotype. Other examples are the DNA mutases,67 which have a high error rate when they synthesize DNA, in contrast to the replicative DNA polymerases, which copy DNA sequences with high accuracy. Yet other DNA polymerases bypass specific types of DNA lesions during replication. These genetically programmed processes allow mutation when survival is threatened by increasing genetic diversity and adaptability. These polymerases are part of a process that allows them to function only when high mutation rates are valuable. That researchers recognize the existence of hypermutable states68 and are widely discussing their evolutionary significance illustrates the potential for a strong coupling between genome-level processes and environmental variability. The notion that substantial variation of the environment could be advantageous for evolution by stimulating the development of complexity stands in contrast to the perspective presented by Ward and Brownlee69 and Gonzalez et al.70—namely, that the development of complex organisms requires a substantially stable environment. Too much variability is surely detrimental to life, but given the ability of life to adapt to what were recently considered to be beyond the tolerable limits of heat, cold, acidity, radiation, salinity, and other factors, it is worth considering the possibility that environmental fluctuations within very broad but reasonable limits are conducive to the development of complexity. Planets subjected to a strongly fluctuating astronomical environment might be a favorable site for complex life. It may be true in general, as it apparently was on Earth, that complex multicellular organisms do not evolve until levels of atmospheric oxygen rise sufficiently. At that point, however, life might develop more complexity faster on planets orbiting low-mass flare stars or on planets in a galactic neighborhood with a higher supernova rate than our own solar neighborhood. The arguments given above suggest that an effort should be made to quantify the nature of astronomical fluctuations in terms of quality (heat, radiation, etc.) and intensity on all relevant timescales and to design laboratory and simulation experi- 65   D.E. Moriarty and R. Miikkulainen. 1999. “Learning Sequential Decision Tasks Through Symbiotic Evolution of Neural Networks.” Advances in the Evolutionary Synthesis of Neural Systems. V. Honavar, M. Patel, and K. Balakrishnan, eds. MIT Press, Cambridge, Mass. 66   Adami et al. 2000. Op cit. 67   M. Radman. 1999. “Mutation: Enzymes of Evolutionary Change.” Nature 401:866-869. 68   P.L. Foster. 2000. “Adaptive Mutation: Implications for Evolution.” BioEssays 22:1067-1074. 69   P.D. Ward and D. Brownlee. 2000. Rare Earth: Why Complex Life Is Uncommon in the Universe. Copernicus, New York. 70   G. Gonzalez, B. Brownlee, and P. Ward. 2001. “The Galactic Habitable Zone: Galactic Chemical Evolution.” Icarus 152:185.

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The Astrophysical Context of Life ments that can provide insight into the basic questions of whether and how life is affected by an astronomically fluctuating environment. Most evolutionary theory assumes a steady exogenous mutation rate and asks how populations evolve as a function of the volatility and physiological impact of environmental fluctuations. Evolutionary models predict that if the genes responsible for high rates of mutation are linked to the genes that improve fitness upon mutation, endogenous mutation rates should remain relatively high when organisms frequently face novel conditions. Other models suggest that because of the high cost of further improving fidelity, endogenous mutation rates should decrease in a relatively constant environment. Still other models have shown that there are mutation rate thresholds above which populations simply cannot evolve. None of these models, however, considers mutation rates that vary over time as a result of exogenous factors. We should also consider these types of questions when the mutation rate is itself fluctuating as a result of the changing environment. Some work in this direction consists of numerical simulations suggesting that sudden large increases in mutation rates can speed the rate at which the complexity of specific phenotypes develops.71 These issues require study at the fundamental conceptual level to determine what degree of disturbance is favorable for the evolution of life and how the answer to that question might depend on the constituents and structure of life elsewhere. They could be explored both in the laboratory using the range of coding bases available today and by appropriate computer simulations, in close collaboration between biologists, computer scientists, and astronomers. Areas of Relevant Independent Astronomical Research Characterizing the galactic environment of the Sun or the astronomical environment of other potentially life-hosting bodies is relevant (see the sections “Galactic Environment” and “Cosmic, Solar, and Terrestrial Irradiation”). It is also important to understand the spatial and temporal variability of bolide impacts, which strongly perturb the thermal environment on Earth or on other potentially life-hosting bodies (see the section “Bombardment”). Areas of Potential Interdisciplinary Interaction One approach to this topic would be to attempt to understand the variety of ways life responds to realistic representations of the fluctuating astronomical thermal and radiation environments. The aim would be to better understand the evolution of organisms that are subjected to the types of thermal and radiation environments expected for planetary systems experiencing a range of bolide impact histories and planets orbiting stars of various masses and ages in different parts of the Galaxy. A variety of laboratory evolution experiments could explore the effects of irradiation on a variety of natural organisms, including well-studied microbes such as Escherichia coli.72 Given the strong expectation that the ambient radiation on young planets will be intrinsically variable, these experiments could investigate whether or not there are qualitative differences between steady and variable radiation exposures at the same mean flux level. 71   D.E. Moriarty and R. Miikkulainen. 1997. “Forming Neural Networks Through Efficient and Adaptive Co-Evolution.” Evolutionary Computation 5:373. 72   V.L. Kalinen, V.N. Petrov, and T.M. Petrova. 1981. “Isolation and Characteristics of Radioresistant Bacillus Subtilis and Bacillus Thuringiensis Mutants.” Radiobiologia 21(5): 676-682 (in Russian).

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The Astrophysical Context of Life A variable UV light source could be designed to simulate the spectrum and variability of astronomical UV radiation from stars of different characteristics, from flares, from supernovas, and so on and then used to study gene activation as a result of that radiation. Such a light source could also be used to drive directed evolution experiments in many generations exposed to this light source. Subsequent gene sequencing and structure analysis would permit study of the robustness of repair mechanisms and the possibility of novel repair pathways in extraterrestrial environments (for instance, the flare-dominated environment of a low-mass star; see the section “Cosmic, Solar, and Terrestrial Irradiation”). Coordinated experimental, theoretical, and computational work could address the interplay of astronomical and planetary environments, chemistry, mutation, diversity, fitness, and cooperation. In addition, with the invention of alternative amino acid coding systems, there is the potential to engineer microbes based on such alternative coding systems and to study their response in directed evolution experiments that simulate astronomical bolide impact and UV or ionizing radiation environments. The point of such experiments would be not to explicitly attempt to mimic life on another planet but to use these engineered microbes to begin to explore the possible range of response and sensitivity in this extension of parameter space. The goal would be to better understand the guiding principles for the character and limits of life that evolves anywhere in a naturally fluctuating astronomical environment. Artificial life experiments can explore a much wider range of parameter space than in vitro directed evolution experiments. Further study of simulated life promises to improve our understanding of the principles behind the growth of complexity in living systems. Experiments using neural networks as the phenotype for digital genomes are especially promising. Astrophysicists who work on irradiation need to team with biologists who can examine the effects of these same types and levels of irradiation on molecules and cells in defined experimental systems (e.g., using directed evolution in vitro), both in solution and in the solid phase (e.g., using clay minerals as catalysts). Similar studies could be done on prebiotic chemistry. Finding. We do not fully understand the strongly variable effects of astronomical bolide impacts or of the irradiation of the surfaces, oceans, and atmospheres of planets and moons on genetic and cellular evolution. Recommendation. NASA, other funding agencies, and the research community should devote funding and effort to promote understanding of (1) the evolution of earthlike organisms and (2) organisms with other coding mechanisms that are subjected to the fluctuating thermal and radiation environments expected for planetary systems with various impact histories and planets orbiting stars of various masses and ages in different parts of the Galaxy. Recommendation. NASA and other relevant agencies should foster in vitro and in silico studies to learn how the stochastic variability of the environment, including the mutational environment, affects the evolution of life, especially by promoting complexity and the evolution of evolvability. Programs of Other Agencies The NSF Tree of Life and DOE Genomes to Life programs will provide basic genetic information that can be used for biochemical experiments and molecular phylogenetic studies designed to learn more about the response of DNA radiation repair pathways to fluctuating thermal and radiation environments. The NIH supports biomedical studies of the origin and treatment of cancer, genetic diseases, and aging. These studies could be significant for astrobiology because they would improve our understanding of the role of variable thermal and radiation environments in the evolution of life.