Testimony of Jack D. Farmer: “Life in the Universe” – hearings before the House Subcommiteee on Space and Aeronautics

Growth of Molecular Biology: Earth’s Microbial Biosphere

Recent advances in molecular biology have radically altered our view of the biosphere and the contribution of microbial life to overall planetary biodiversity. In contrast to the outdated five kingdom view of the biosphere (Animals, Plants, Fungi, Protists and Monera), multicellular plants and animals being given prominence, genetic sequence comparisons have shown there are actually three major domains (Archaea, Bacteria and Eukarya), consisting of dozens of kingdoms, nearly all of which are microbial (Figure 4). It is important to keep in mind that although we have sampled a wide range of environments, only a small fraction (1-2%) of the total biodiversity on Earth has so far been sampled (Pace 1996). While periodic discoveries of new organisms have increased the number of branches in the universal tree, the basic three domain structure has remained stable. Perhaps one of the most fundamental things we have recognized from this work is the fact that we live on a microbial planet where microscopic life fully dominated the first 85% of biospheric history. The pathways followed during the evolution of the biosphere appear to have been shaped by periodic environmental changes driven by basic processes of biological and planetary evolution. The occurred quite late in the history of our planet. Their explosive appearance of complex, multicellular animals about 600 million years ago, appears to have been triggered by the slow buildup of molecular oxygen in the oceans and atmosphere to the threshold level (about 10% PAL) required for oxidative metabolism. This event, which ultimately paved the way for human intelligence, has been attributed to the invention of microbial photosynthesis.

Expanding the Environmental Limits for Life

In the past decade or so, our knowledge of the environmental limits of life on Earth has expanded dramatically, primarily through the development of new sampling techniques and their application over a broad range of environmental extremes. A brief summary of some of the known environmental limits to terrestrial life is given in Table 1 (see also Figs. 2-3). Microbial species are known to occupy almost the entire range of pH from 1.4 (extremely acid) to 13.5 (extremely alkaline). Similarly, life also thrives over extremes in temperature, with some species showing growth up to ~114 ^oC (thermal springs at Vulcano, Italy and deep sea vents; Stetter 1996) and other species surviving down to -15 ^oC (brine films in Siberian permafrost; Gilichinsky, 1995). Life also occupies an equally broad range of salinity, ranging from fresh water up to sodium chloride saturation (~300 percent), where salt precipitates. One thing seems clear: life occupies virtually every imaginable habitat on Earth where liquid water, an energy source and basic nutrients coexist.

In addition to environmental adaptation, some microbial species also show evidence of remarkably prolonged viability. In even the driest deserts on Earth, some species survive by living inside porous rocks where they find a safe haven from UV radiation, springing to life only occasionally, when water needed for growth becomes available. Even more interesting are bacteria that have been germinated from spores preserved in Dominican amber dated at >30 million years old. Microbes have also been isolated from Siberian permafrost where they have remained in deep freeze for >3 million years, and other salt-loving microbes have been cultured from rock salt dated at hundreds of millions of years old (Figure 6). Given this propensity for prolonged survival, could life still persist on planets like Mars where Earth-like conditions once prevailed?

Energy Requirements for Life

In addition to the need for liquid water, the distribution and productivity of life is also determined by the amount of energy available for sustaining metabolism and growth. Most important is photosynthesis, which directly powers >99% of the biosphere’s productivity. This observation is easily understood when we realize that energy from the sun, per unit area of the Earth’s surface, is several hundred times more abundant than the thermal and chemical energy coming from within the Earth. Not surprisingly, life thrives virtually anywhere on the Earth that sunlight and liquid water co-exist. However, the story does not end there. In 1979, oceanographer and explorationist Robert Ballard and biologist J. Frederick Grassle piloted the deep submersible, Gilliss, to sites more than a mile and a half deep on the sea floor, near the Galapagos Islands. The mission was to relocate and describe in detail, warm vents and their associated faunas from several previously discovered sites. At these locations, scientists got a first glimpse of living ecosystems based entirely on chemical energy, instead of sunlight (Figs 1 and 15). Finding such complex ecosystems, with large, multi-celled animals, all ultimately sustained by the chemical energy provided by the hot vents, was quite unexpected. As our exploration of “inner space” continued, we eventually discovered examples of these complex vent communities in virtually every ocean basin, proving the remarkable ability of these organisms to colonize even the most widely dispersed “island” habitats. There are now hints of primitive, pigmented photosynthetic organisms living at similar vent sites, which are able to utilize the weak thermoluminescent radiation given off by the hot vents (Blankenship et al. 2000). This has opened up the intriguing possibility that like chemotrophy, photosynthesis may also have evolutionary roots in deep sea vent settings.

As our methods of exploration and observation have improved, life’s environmental limits have continued to expand. And we have not yet reached the limits! More recently it was discovered that life also thrives in deep subsurface environments where interactions between water and rock yield available energy (e.g. Gold, 1992; Fredrickson and Onstott, 1996). Also, we now think that Lake Vostoc, a subglacial lake lying deep beneath the Antarctic ice cap, may harbor a microbial ecosystem.

While many subsurface organisms utilize the “filtered-down” organic compounds produced by photosynthetic surface life, some species are able to make their own organic molecules from the purely inorganic substrates that come from simple weathering reactions between groundwater and rock (Stevens and McKinley, 1996). Such subsurface organisms hold special importance with regard to potential habitats for life elsewhere in the Solar System. For example, we must now seriously consider the possibility of a subsurface biosphere on Mars or Europa, where a subsurface hydrosphere may exist.

Impact Frustration of Early Biosphere Development

An important legacy of the Apollo missions was the development of a detailed cratering history for the moon. This led to the view that during early accretion, prior to ~4.4 billion years ago, surface conditions on the Earth were unfavorable for the origin of life (Chang, 1994). Frequent giant impacts would have produced widespread oceans of molten rock at the Earth’s surface. Easily vaporized compounds, like water and biologically-important elements like carbon, hydrogen, oxygen, nitrogen, sulfur and phosphorous (necessary for life) would have been lost to space through a combination of volatile escape and impact erosion.

Models for the early accretion of the Earth suggest that by about 4.0 billion years ago, the rate and size of impacts dropped off to a point where the water and organics delivered to the Earth by comets and other icy objects, would have been retained. During this time (4.4 – 4.2 billion years ago), a stable atmosphere and ocean could have developed, providing the first suitable environments for pre-biotic chemistry and life. However, models also suggest that as late as 3.8 billion years ago, the emerging biosphere may have experienced one or more giant impacts. These impactors would have been capable of vaporizing the oceans, while sterilizing surface environments (Sleep et al. 1989; Zahnle et al. 1988). Such events would have “frustrated” the development of an early biosphere. The most protected habitat during this early period would have been in the deep subsurface, where as we have seen previously, life could have easily survived under hydrothermal conditions up to ~114 ^oC.

Late, Giant Impacts and Early Biosphere Evolution

Using the genetic information encoded in the cells of living organisms, molecular biologists have been able to assemble a kind of “family tree” by comparing all of the species so far sequenced (Figure 4). This tree is based on genetic information stored in the RNA of ribosomes, small structures in cells that synthesize proteins. Because protein synthesis is extremely important in living systems, ribosomes appear to have been very conservative during their evolution, having sustained comparatively few mutations. Even minor mistakes in protein synthesis usually spell disaster to an organism and most mutations would not survive. Conservatism in the ribosomal genome has allowed it to retain more information about the evolutionary events that occurred during the early history of the biosphere.

On the basis of ribosomal RNA sequence comparisons, the first universal tree of life was published by Carl Woese (Univ. of Illinois) in 1987. It became quite evident at that time that the deepest branches of the tree, those presumably lying closest to the common ancestor of life, all shared an interesting property: a preference for very high (hydrothermal) temperatures exceeding 80 ^oC. For some scientists this implied that life probably got started at high temperatures, perhaps within deep sea vent environments, as discussed above.  For others (myself included) it seemed more likely that what we were seeing was not the environment of life’s origin, but rather environments that prevailed after the last giant impact. Figure 5, which is based on the work of Kevin Zahnle (NASA Ames) and colleagues, summarizes the effects of a 400 km-diameter impact. Perhaps the most astounding effect predicted by his model is the complete evaporation of the oceans and the creation of a steam atmosphere. The most deeply rooted forms may simply be the descendants of organisms that were able to survive a comparable devastating late impact by hiding out in subsurface hydrothermal environments. Unlike today, such environments would have probably been widespread globally, following such an impact.

While this scenario is quite consistent with independent geological evidence for the early Earth (the rocks tell us it was hotter, that large impacts were more frequent and that volcanic activity was more widespread), recent discoveries in molecular biology have cast doubt on the reliability of the observed patterns in universal tree. It now seems clear that even for the conservative ribosomal tree, branching patterns have been complicated by the process of lateral gene transfer. This process involves the exchange of genetic information between branches and across the three domains of the tree (Doolittle, 1998). At one extreme, some workers have suggested that the three domains have no evolutionary meaning and are simply groups of organisms that have exchanged genetic material more often during evolution. In that case, no phylogenetic relationships would be preserved. More optimistically, it could be that instead of a branching tree, ancestor-descendant relationships are rather represented by a complex web of genetic exchanges that have occurred between species periodically throughout evolutionary history. Rapid advances are taking place in this area of science, and it is unclear what the outcome will be. But I still find the general consistency between the environmental predictions based on the RNA tree and the geological record quite compelling, and think the tree may preserve important information about biological evolution.

Evidence from Paleontology

The other way to look at evolutionary history is by reading patterns preserved in the fossil record. During Darwin’s time, there was limited awareness of the importance of microbial life in the evolutionary history of the biosphere. The oldest fossils known were shelled invertebrates that appeared at the base of the Cambrian Period (now dated at ~540 million years). The first stromatolites (biolaminated sediments produced by microbial communities) were described around 1850, at about the same time Darwin’s Origin of Species was published. But the significance of these structures basically went unappreciated until the late 1800’s and the interval of Earth history preceding the Cambrian (called the Precambrian) was regarded as being largely devoid of fossils and life. However, new discoveries around the turn of the century began to add the dimension of deep time to paleontology, eventually pushing back the fossil record of microbial life billions of years (Barghoorn 1971). In 1993, J. William Schopf (UCLA) reported bacterial microfossils from stromatolite-bearing sequences in western Australia dated at nearly 3.5 billion years. (Those microfossils have now been shown to reside in hydrothermal veins; Van Kranendonk personal communication, 2001). Then in 1996, Steven Mojzsis (University of Colorado) and colleagues described possible chemical signatures for life from rocks in Greenland dated at almost 3.9 billion years. These are the current record holders for oldest probable fossils on Earth.

These advances in Precambrian paleontology have pushed back the record of life on our planet to within half a billion years of the time we believe the first viable habitats existed on Earth. This suggests that once the conditions necessary for life’s origin were in place, it arose very quickly. Exactly how quickly, we don’t yet know, but certainly on a geologic time scale, it was much shorter than previously thought. This view significantly improves the possibility that life could have originated on another planet like Mars, where liquid surface water may have only been present at the surface for a few hundred million years early in the planet’s history. However, there is an interesting caveat here. If there has always been a subsurface hydrosphere on Mars, the widespread success of the subterranean biosphere on Earth suggests martian life could have originated in subsurface environments at any time during the planet’s history and persisted there until the present time (see below). The same also holds true for icy satellites with subsurface oceans, like Europa!

Exploring for an Extant Martian Biosphere

We began our exploration for life elsewhere in the Solar System more than twenty years ago with the Viking mission. Fixed robotic landers were delivered to two sites on the Northern Plains of Mars where they conducted biology experiments to explore for life. These experiments were designed to search for living organisms within surface soils. By adding water and nutrients to soil samples, it was anticipated that any organisms present would begin to grow and give off waste products that could be detected with the instruments on board (Klein 1998). After nearly two decades of analysis, the results of the Viking biology experiments have been widely attributed to inorganic processes. This is perhaps not surprising given that liquid water, regarded as essential for living systems, is unstable at the surface of Mars today because of the low atmospheric density (~7.5 millibars at the equivalent of sea level). While we know there is water on the surface of Mars today, it exists primarily in a frozen state, or as minute amounts of vapor in the atmosphere.

Certainly the general absence of liquid water in modern surface environments on Mars poses a formidable barrier to the development and survival of life there today. But other important factors could also play a role in limiting habitability. First, the rusty, iron-rich soils of Mars are colored red because they are highly oxidized. The fact that Viking found no evidence for organic compounds in martian soils, even though they are constantly being delivered to the surface by interplanetary dust particles, suggests that the surface soils are chemically harsh environments that are destructive to organic molecules. In addition, the thin, CO2-rich atmosphere lacks molecular oxygen and an attending ozone shield to protect the surface from ultraviolet radiation. Many microorganisms on Earth are known to survive in high radiation environments by living within rocks, or by producing pigments that act as sunscreens. But UV radiation reaching the martian surface is several times that considered lethal to most terrestrial organisms. True, some terrestrial microbes are able to survive in the high radiation environment of a nuclear reactor core by possessing extremely rapid DNA repair mechanisms. By itself, the surface radiation environment on Mars is probably not enough to limit the potential for life there. But, in combination these factors comprise a formidable barrier for life and it remains problematic whether biological systems could have adapted to such conditions. So if the surface soils sampled by Viking are not a favorable environment for life, where should we look for living organisms?

The subsurface of Mars offers a compelling environment for extant martian life because models support the potential for an extensive subsurface ground water system located at a depth of several kilometers below the surface (Clifford 1993). This suggestion was recently bolstered by the discovery of fluid seeps at the surface (discussed below). To access the deep subsurface of Mars will require larger and more sophisticated robotic platforms than are currently available. Alternatively, deep drilling might be accomplished by human astronauts. Clearly we will not send humans to Mars before we can be reasonably confident of their safe return. To gain this confidence, there are still many “tall poles” we must meet. Recent studies indicate it will take a decade of well-funded research to be in a position to decide the feasibility of human missions to Mars and another decade beyond that before we can actually mount a human mission.

Recently, the Mars Global Surveyor mission detected sites on Mars where water appears to have seeped out of the subsurface, forming small, very young channels (Fig. 7; Malin and Edgett 2000). Interestingly, these seeps are only found on pole-ward facing slopes at high latitudes, perhaps the least likely places we would expect to find liquid water. The existence of these seeps suggests a source of groundwater very near the surface. But shallow crustal temperatures at these sites should be far below the freezing point of water. One way out of this dilemma is to appeal to brines (salt lowers the freezing point of water), or to subsurface hydrothermal circulation that would bring warm water to the surface at these sites. If liquid water (even hot, salty water!) is eventually proven to be agent that formed these features, then the biological potential for Mars will have been dramatically enhanced.

Exploring for a Fossil Record of Martian Life

At the same time the Viking landers were carrying out their biology experiments at the surface, images were being obtained from orbit that revealed a Mars more Earth-like early in the planet’s history. Geomorphic evidence suggested that water was once widespread over the surface. Other geological arguments suggested that liquid water disappeared from the surface ~3.0 billion years ago. The loss of surface water has since been attributed to the gradual sequestering of the CO₂-rich Martian atmosphere in the crust as weathering products. In the absence of a recycling process, such as plate tectonics, the atmosphere would literally be drawn down into the crust and combined as mineral products. If surface life developed on Mars during the early Earth-like period of the planet’s history, it is quite likely to have left behind a fossil record. As on Earth, this record should be preserved in ancient water-formed sedimentary deposits. On Earth we have found biosignatures in sedimentary rocks going as far back as we have intact sequences available to sample. By finding places on the martian surface where we know water was once abundant, we should be able to access potentially fossiliferous deposits during the robotic phase of exploration. And by studying processes that govern the preservation of fossil biosignatures in analog environments on Earth, we have been able to define “rules” for preservation that can help us select the best sites on Mars to explore with future missions (Farmer 1999; Farmer and Des Marais 1999). This concept is an important part of the rationale for the current robotic program.

An Exploration Strategy for Mars

Given the complexity and scale of the problem, we cannot expect to land just anywhere on Mars and find evidence of past or present life. In formulating a strategy to explore for past or present Martian life, the Astrobiology community has recommended a phased approach where global reconnaissance is interleaved with precursor surface missions, in order to target the best sites for detailed surface reconnaissance and sample return (NASA,1995). The basic goal is to target sites where there is evidence of past or present water activity and the right kinds of geologic environments (i.e., those favorable for the capture and preservation of biosignatures). In exploring for extant life forms, there is an obvious interest in finding habitable zones of liquid water in the subsurface. In exploring for a record of ancient life, we are more interested in targeting water-formed sedimentary deposits laid down by ancient hydrothermal systems (Fig. 9) or paleolake basins (Figs. 8, 15). Key to this endeavor is understanding the mineralogy of the martian surface. Recent discoveries by the Thermal Emission Spectrometer instrument, currently mapping at Mars, emphsizes the point. Coarse-grained (“specular”) hematite deposits detected at Sinus Meridiani strongly suggest the activity water. This is a site was previously identified as a paleolake basin based on geomorphology. This kind of synergy between instruments is exactly what we need to effectively “follow the water”. This site has been short-listed as a potential landing site for the 2003 mission.

Placing an emphasis on understanding the past and present aqueous environments on Mars, will position us to target well-equipped robotic rovers to the best sites for in situ surface science and sample return. Ultimately this approach may afford us the opportunity to conduct in situ life detection experiments far more sophisticated than those of Viking, at sites that are much more likely to harbor evidence of past of present life. And by the careful selection of samples for return to our Earth-based labs, we will be able to carry out the types of sophisticated analyses that may be required to address the question of Martian life.

Life in a Martian Meteorite?

In 1996, a team lead by David McKay at Johnson Space Center posed a very intriguing hypothesis regarding the possible biological origin of about a half dozen features observed in martian meteorite, ALH 84001. This now infamous igneous rock contains tiny grains of iron-rich carbonate, an aqueous mineral that precipitated in subsurface fractures as fluids flowed through. NASA wisely decided to open up the debate, providing grant funding to many leading scientists in this country and around the world to test the proposed hypothesis. This provided a remarkable opportunity to: 1) engage the public in the process of scientific inquiry and 2) bring the best minds together to tackle the problem. After several years of work, the community has systematically addressed all of the original lines of evidence posed. To date only one has survived detailed scrutiny. The remaining line of evidence is in many ways, perhaps the most intriguing. This involves tiny grains of the mineral magnetite (as the name implies, a naturally magnetic mineral) which is common in basalt (a high temperature volcanic rock that makes up oceanic crust). However, some bacteria have also “learned” to make minute grains of geochemically pure, low temperature magnetite, which they organize into chains within their cells and use as a kind of directional compass. This enables the cells to move about in their environment, tracking favorable environmental conditions. Some (about 20%) of the magnetites found in the Allan Hills meteorite bear a strong resemblance to the biologically-formed magnetites formed by terrestrial bacteria. But is the population of magnetites in the meteorite a reliable indicator of life? The community is still busy testing this idea by characterizing a broad range of naturally-occurring and synthetic forms of magnetite. Hopefully they will have a definitive answer soon.

If the last line of evidence for life in ALH 84001 comes up negative, what will this imply about the possibility of life on Mars? Remember that the Allan Hills meteorite was delivered happen-stance to the Earth millions of years after a random impact knocked it off the Martian surface and sent it hurdling toward the Earth. Another happen-stance discovery in Antarctica during a 1984 expedition eventually delivered the meteorite to the hands of scientists. Clearly there was not a lot of site selection involved in this process. I believe that for an adequate test of the hypothesis of martian life we will need to have samples from sites where we are certain that conditions are/were right for the capture and preservation of biosignatures. This will take careful, systematic work. That is what the current Mars Program is striving to provide.

Our experience with the Allan Hills meteorite has served a crucial role in helping the scientific community to learn how to reliably test for signs of life in ancient rocks. This has been a great warm-up for analyzing the types of samples we hope to return from Mars during the next decade. But studies of ALH 84001 have also provided another important perspective. The ancient age of this meteorite, dated at 4.56 billion years, indicates that the ancient, heavily cratered highlands of Mars are likely to harbor a rock record that extends back in time to the very earliest period of the planet’s history. On Earth, rocks of comparable geologic age have long since been destroyed by tectonic cycling, weathering and erosion. The fact that Mars never developed a vigorous plate tectonic cycle means that ancient crustal sequences are unlikely to have been deeply buried and metamorphosed. The loss of liquid water from the martian surface early in the planet’s history and the limited water-mediated weathering and erosion since that time, has also conspired to preserve an extraordinary record of early planetary conditions, and perhaps of life itself! The path we are on with the present Mars program, which emphasizes systematic exploration from orbit, interleaved with landed missions, should produce the important clues we need for selecting the best sites for detailed surface studies and sample return.

Exploring for Life in the Outer Solar System

Measurements of the magnetic field of Europa (a satellite of Jupiter) obtained during the Galileo mission, have strengthened arguments for the existence of a salty ocean lying beneath an exterior shell of water ice. (Similar arguments have now also been made for Ganymede and Callisto). This idea of a subsurface brine ocean is also supported by infrared spectroscopic signatures which suggest the presence of magnesium and/or sodium sulfates in the surface ices of Europa. It has been postulated that the postulated europan ocean is maintained by heating of the moon’s interior through tidal friction, a process that could melt rock and drive a crustal heat exchange system. Indeed, the complexly fractured and largely, uncratered surface of Europa suggests that a form of ice “tectonics” involving the periodic upflow of liquid water from beneath the europan crust, has constantly renewed the surface (Fig. 11-12). As the plates of ice diverged, water welled up from below, freezing out to form long, narrow ridges. Over time, ice plates shifted, offsetting older ridge segments along faults. At a finer scale, blocks of fractured crust foundered, tilted and became frozen in the leads between diverging plates. In addition to the long ridges separating plates, smaller, mounded features also formed where ice “volcanoes” erupted water, or ice.

In assessing the potential for life on Europa, certainly the presence of liquid water is crucial, both from the standpoint of providing a medium for biochemical processes, but also as a source of the chemical energy necessary to sustain it. A recent model by Chyba and Hand (2001) suggested that while photosynthesis does not provide a plausible energy source for life, radiation processing of Europa’s ice and water, in combination with the decay of radioactive potassium, could decompose water to hydrogen and oxygen, with the hydrogen escaping to space. The chemical disequilibrium created by this process could be exploited for energy by organisms.

Exploration Strategies for Europa

On Earth, refrigeration is known to be an effective means for the preservation of organisms in high latitude and recently glaciated terranes. Sagan (1971) first suggested that microorganisms from an earlier, clement period in martian history might still exist there today in a perpetually frozen state, preserved in ground ice. Could the same hold true for Europa? It seems quite plausible that where water has welled up from below, it may have carried organisms, or their by-products, from an underlying ocean or interstitial brine, eventually freezing and cryopreserving these materials in ices at or near the surface.

What are the chances that life could survive once entombed and frozen in ice? Terrestrial microbes have been shown to retain viability down to sub-zero temperatures by exploiting thin films of brine on the surfaces of mineral particles in permafrost soils (Gilichinsky et al. 1993). As mentioned previously, terrestrial organisms appear to have survived in a frozen state within Siberian permafrost for millions of years. Some have questioned the long-term viability of microorganisms in ice due to the destructive effects of prolonged exposure to background radiation, in the absence of active DNA repair mechanisms. Similarly, in the radiation-rich environment of Europa, this could also be a problem for long-term suvival of organisms. But viability arguments aside, as a potential fossil repository, ice could provide an equally important environment for preserving a fossil record of life on Europa. In exploring for cryopreserved life in europan ices, sites where water/ice has recently erupted at the surface have obvious priority.

The next Europa mission is planned for launch sometime after 2007. This mission is expected to carry high resolution spectrometers to map the surface and determine the mineralogical and organic composition of the ice. In addition, radar sounding will be used to probe the subsurface from orbit in search of zones of liquid water. This will allow a more thorough test of the hypothesis of a subsurface ocean and help identify the best sites for surface exploration by robotic landers that will search for biosignatures cryopreserved in ices. If we are able to prove the existence of a subsurface ocean, the next step could be to deploy small ‘cryobots’ that will melt their way through the ice, deploying mini-subs to explore for signs of life in the “inner space” of the europan ocean (Fig. 13). At present such ideas are just fanciful speculation. We lack the basic technology needed for this kind of exploration. But such ideas do provide a compelling vision for the future that inspires us to want to penetrate the icy veil of this strange world.

Summary

Recent scientific advances have greatly expanded our knowledge of the nature and evolution of terrestrial life, while opening up new possibilities for the existence of extraterrestrial life. These developments have laid the foundation for a new interdisciplinary scientific discipline called astrobiology, which studies the origin, evolution, distribution and destiny of life in the Cosmos.

Some important developments that have influenced the way we think about the exploration for extraterrestrial life in the Solar System include the following:

• Advances in molecular biology and paleontology have revealed that most of Earth’s biodiversity is microbial. Microbiological processes drive many important biogeochemical cycles and have helped shape the global planetary environment during its history.

• The path of evolution followed by the biosphere was largely opportunistic, being intimately tied to processes of planetary evolution. But biological processes have also played a role. For example, the complex multicellular animals on the evolutionary path to humans, arose very late in biosphere history in response to the build-up of photosynthetic oxygen.

• Life has been shown to occupy a stunning array of environmental extremes, seemingly limited only by the distribution of liquid water, nutrients and sources of energy. This has opened up important options for the astrobiological exploration of the Solar System where many such environments exist.

• Complex microbial ecosystems, including large multicellular animals, were discovered living in association with hydrothermal vents on the deep sea floor. These ecosystems are unique in being sustained by inorganically-derived forms of chemical energy. This has important implications concerning the potential of such sources of chemical energy to sustain life in similar environments elsewhere in the Solar System (e.g. Europa).

• Subsurface environments on Earth harbor a vast biosphere that includes many species that can synthesize organic molecules from the simple by-products of inorganic chemical weathering. This discovery has opened up important new directions for exploring for life elsewhere in the Solar System.

• The structure of the universal tree of life, based on ribosomal RNA, suggests that the common ancestor of life lived in hydrothermal environments and utilized chemical energy. This idea is consistent with geological evidence for the early Earth, as well as with late, giant impact scenarios where low temperature surface organisms are exterminated, leaving behind only high temperature, subsurface forms. However, the relationships implied by genetic sequence comparisons have probably been complicated by lateral gene exchanges between unrelated species later in evolution, thus making it difficult to discern actual the patterns of descent. Still, the consistency with geological evidence suggests that molecular sequence data is telling us something important.

• Discoveries in paleontology have pushed back the record of life to nearly 3.5 billion years for cellular fossils and to nearly 3.8 billion years for chemical signatures of life. This shortens the time available for life’s origin to less than half a billion years, indicating that once habitable conditions existed on Earth, life arose very quickly. This improves the chances that life may have become established in surface environments on Mars during the short, early interval when water was widespread at the surface.

• The most probable environment for an extant martian biosphere is the deep subsurface where a global ground water system may still exist. Plausible metabolic strategies involve the synthesis of organic molecules from compounds liberated by inorganic rock-water interactions. Recent seep sites strengthen the case for such environments, thus bolstering the potential for life.

• Deep drilling from robotic platforms poses a major technological challenge for Mars exploration, but access to subsurface aquifers with rovers may be possible at localized seep sites where upwelling hydrothermal brines appear to have escaped from the subsurface. Access to such sites will require advances in precision landing and long-ranging rovers.

• Exploration for evidence of an ancient martian biosphere requires locating sites of ancient aqueous sedimentation, as well as paleoenvironments favorable for the capture and preservation of fossil biosignatures. A knowledge of the mineralogy of the martian surface is considered crucial for targeting sites landed missions to explore for past life.

• The current strategy for the astrobiological exploration of Mars involves a phased approach where orbital reconnaissance will be interleaved with landed missions to narrow the search to a few high priority sites where we will carry out in situ surface exploration and sample return. This phased approach is designed to focus exploration efforts on the best sites for testing the life hypothesis.

• The hypothesis of fossil biosignatures preserved in martian meteorite ALH 84001 has served as an effective catalyst in preparing the scientific community for Mars sample return by focusing the scientific community on the development of improved methods for assessing biogenicity in ancient terrestrial and extraterrestrial materials. Recent efforts have been focused on evaluating the origin of magnetite, a potential mineralogical biosignature found in the meteorite.

• Compelling evidence exists for a salty ocean beneath the icy crust of Europa. Plausible energy sources for life have been identified based on the disassociation of water by radiation processing at the surface and the decay of radioactive potassium in the subsurface.

• Future missions to Europa will test for a subsurface ocean from orbit as a basis for targeting sites of recent upwelling from the subsurface. Surface landers targeted to these sites will be able to explore for cryopreserved organic materials in surface ices and penetrate the subsurface environments where life may exist.

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Accompanying Illustrations:

Table 1: Extremes of Life

Figure 1: Deep sea vent community

Figure 2: Yellowstone hot spring

Figure 3: Mono Lake, CA

Figure 4: rRNA Tree

Figure 5: Zahnle impact scenario

Figure 6: Halobacteria in salt crystals

Figure 7: Martian seep sites

Figure 8: Gusev crater paleolake basin

Figure 9: Hydrothermal sites on Mars

Figure 10: Sinus Meridiani hematite site

Figure 11: Europa’s crust

Figure 12: Models for Europa’s interior

Figure 13: Hydrobot at Europa

Figure 14: Aquifex

Figure 15: Martian Lake beds