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Vacant habitats in the Universe
Opinion
Vacant habitats in the Universe Charles S. Cockell CEPSAR, Open University, Milton Keynes, UK, MK7 6AA
The search for life on other planets usually makes the assumption that where there is a habitat, it will contain life. On the present-day Earth, uninhabited habitats (or vacant habitats) are rare, but might occur, for example, in subsurface oils or impact craters that have been thermally sterilized in the past. Beyond Earth, vacant habitats might similarly exist on inhabited planets or on uninhabited planets, for example on a habitable planet where life never originated. The hypothesis that vacant habitats are abundant in the Universe is testable by studying other planets. In this review, I discuss how the study of vacant habitats might ultimately inform an understanding of how life has influenced geochemical conditions on Earth.
The search for vacant habitats The motivation to explore other planets for the presence of life is to test the hypothesis that life has arisen on planetary bodies other than Earth and, if it does exist elsewhere, to investigate its ubiquity. These scientific objectives have become something of a one-sided quest, focussing on the search for the presence of life, rather than its absence. This is unsurprising, as investigating lifeless locations does not engage the public imagination; neither does it, at first glance, appear to be a promising avenue of scientific research. The discovery of life beyond Earth would open up a variety of scientific possibilities. For instance, if the newly discovered life was related to life on Earth, island biogeography would develop an interplanetary scope [1] and so, therefore, would the science of ecology. Such a scenario could plausibly be the case for a Martian biota composed of the descendants or the ancestors of terrestrial biota, resulting from the transfer of material in asteroid and comet impacts from Earth to Mars and vice versa [2,3]. If the extraterrestrial life derived from an independent origin, either discovered in our Solar System or remotely on extrasolar planets (see Glossary) orbiting distant stars, then new vistas of astronomy, biogeochemistry, biology and many other fields would open up in investigating the structure and behaviour of this other life [4]. However, an unbiased study of the factors required for the development of life in the Universe must also examine environments that are lifeless and explore the reasons for their lack of life. One obvious way in which other planetary bodies can be rendered lifeless is by environmental conditions that are too extreme to sustain any type of biology. To assess the plausibility of this scenario, one needs to Corresponding author: Cockell, C.S. ([email protected]).
compare the conditions required for the growth and reproduction of life on Earth with the measured physical and chemical parameters in any extraterrestrial environment, accepting that this is a conservative assessment based on the one type of life that is currently known [5–7]. In this review, I focus on another type of lifeless environment: one in which there is no life, but where life could be sustained. These places have been called uninhabited habitable habitats (sensu [8]), but because a habitat is, by definition, habitable then the middle qualifier is redundant and they are better referred to as ‘uninhabited habitats’. Here, I call them ‘vacant habitats’. I am generally referring to sterile habitats, but they could also include habitats that contain inactive life on an otherwise inhabited planet. Thus, the term ‘vacant’ means vacant of metabolically active life. A ‘vacant habitat’ is also distinguished from a ‘vacant niche’ [9–12]. The former is a physical space that could support life, but has none in it, whereas the latter is a functional definition of a specific set of energy and nutrient availabilities that could be used by life, but are not. Clearly, if a habitat is vacant, it implies that it must contain empty niche(s). Vacant habitats occur at different scales. They could exist on a planetary scale, in the case of an uninhabited, but habitable planet. They can also occur at the micron scale. For example, a habitable unoccupied micron-sized space between two microorganisms in soil would be a vacant habitat. Vacant habitats at these scales might be common, although short-lived. In this paper I am primarily concerned with vacant habitats at macroscopic scales.
Glossary Astrobiology: the area of scientific enquiry that lies at the interface between biological sciences and planetary sciences or astronomy. Banded iron formation: mineral formation found in rocks aged between 2.5 billion and 1.8 billion years old. It is made of alternating bands of iron oxides and silica-rich rocks. Biosignature: any phenomenon produced by life; particularly mineral signatures in the case of astrobiology. Exoplanet or extrasolar planet: a planet orbiting a star other than the Sun. Extremophile: an organism (particularly microorganisms) that inhabit extremes of chemical or physical conditions. Heterotroph: an organism that obtains its energy from organic carbon, particularly that produced by other organisms. Iron-oxidizing bacteria: bacteria that use reduced iron (Fe2+) as an electron donor to generate energy for growth. Jovian moons: the moons of the giant gas planet, Jupiter. Planetary protection: the prevention of the contamination of other planetary bodies (termed ‘forward contamination’) or the contamination of the Earth with extraterrestrial organisms (termed ‘back contamination’). Redox couple: an oxidizing and reducing agent that together can be used by microorganisms to conserve energy for growth. Subglacial environment: environment under glaciers or ice sheets. Vacant (or uninhabited) habitat: a habitat that can theoretically sustain life, but in which there are no active organisms.
0169-5347/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2010.11.004 Trends in Ecology and Evolution, February 2011, Vol. 26, No. 2
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Opinion To define a habitat as ‘vacant’ requires the identification of a species that can be shown, experimentally or theoretically, to be capable of living in that habitat, a point of logic previously raised with respect to the notion of ‘vacant niches’ [11,12]. The assessment of the extent of vacant habitats (and vacant niches) is therefore necessarily conservative and bounded by what is known about life. Environments classified as uninhabitable might be suitable for life with appropriate biochemistries that are yet to evolve, that have not yet been discovered, or that do not exist on present-day Earth. Thus, the set of vacant habitats that is catalogued is a minimum set. Vacant habitats on Earth Are there any examples of vacant habitats on Earth? Certainly, these places do not obviously constitute a large area of the planet and their rarity might contribute to the widely held assumption that life will be found in any location where physical and chemical conditions are conducive to it. A more reductionist assumption goes one step further and posits that where there is merely water, there is likely to be life. Indeed, this dogma has been used to guide the search for life on other planets; a ‘follow the water’ approach to life detection [13,14] (although, of course, not all liquid water is habitable because of inappropriate temperatures, water activities, etc. [15,16]). The presumed ubiquity of life in habitable places is based on a prejudice derived from our experiences of life on Earth. In most habitats on Earth that are connected to the surface photosynthetic biosphere, and where physical and chemical conditions are conducive to microbial growth, there are microorganisms. Photosynthesis generates a vast quantity of carbon, approximately 1 x 1016 mole C per year [17,18]. This carbon leaches into most available habitat space and provides energy for heterotrophs. These organisms can be aerobic, using oxygen as the electron acceptor, yet another easily diffused waste product of the photosynthetic biosphere. Alternatively, they can ferment or use other electron acceptors coupled to anaerobic metabolisms. The pervasive nature of carbon on Earth leads to the observation that all habitable spaces are colonized [19]. Along with other elements and compounds from rocks and dead biota, this carbon usually contaminates water bodies, however transient, leading to the further observation (and thus dogma) that where there is liquid water, there is life. On Earth, one way to achieve a vacant habitat over a significant length of time is for a habitable space to be separated from the surface photosynthetic biosphere, sterilized and then for it to remain disconnected from the surface. These conditions are rare, but where they do exist they are most likely to be in the deep subsurface, an environment only recently explored for its microbial diversity [20–22].There is some tantalizing evidence for such habitats. Petroleum engineers are interested in the microbial degradation of oils, because these processes affect the quality of crude oil and the products derived from it by causing a net destruction of saturated hydrocarbons. The state of oil biodegradation can be regarded as a proxy for microbial activity in any subsurface oil reservoir. For example, the Peace River and Athabasca tar sands in Alberta, Canada contain over 1.3 trillion barrels of tar 74
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sand oil and have therefore attracted considerable economic, and thus scientific, attention [23–25]. Oil quality is known to increase from the eastern regions of these sands to the western; in the former case, oils are often completely depleted in saturated hydrocarbons, whereas in the west, the oils contain 55% saturated hydrocarbons and exhibit minimal degradation. Modelling of the burial history of the oils suggests that oils in the eastern tar sands never reached temperatures greater than 655 8C and so would have been subject to microbial degradation [25]. However, the models also suggest that the oils in the western sands were heated to above the 80 8C pasteurization temperature 85 million to 90 million years ago and could have reached temperatures up to 100 8C, effectively sterilizing them and accounting for their good preservation. Any process that can deliver a localized pulse of sterilizing energy into an inhabited deep subsurface location, which subsequently remains isolated, can potentially yield vacant habitats. Asteroid and comet impacts are one such mechanism. The kinetic energy of these objects, a proportion of which is converted to thermal energy during impact [26], can render the immediate surroundings sterile. The pulse of energy can be sufficiently large that the target rocks can be heated for many thousands to millions of years after impact, depending on the size of the impactor [27–39]. If the period when temperatures exceed the upper temperature limit for life coincides with the time when local geological rearrangements isolate some of the target rocks, then a vacant habitat could be formed. This might have been the case in the deep subsurface of the Chesapeake Bay Impact Structure in the eastern USA (Box 1). These examples are, however, rare, and the extent of the sterility and the period of sterilization uncertain. However, these uncertainties serve to underline the paucity of identifiable vacant habitats on Earth. Vacant habitats can potentially exist transiently on Earth where a sudden geological disturbance occurs, producing a fresh and sterile substrate. For example, a newly formed molten and sterile volcanic lava flow will eventually cool down to below the upper temperature limit for life. There might be a period that defines this place as a vacant habitat between the instant at which the temperature drops below the critical threshold and the instant at which the first microorganisms land on the rock [30,31] and begin to be metabolically active. For most substrates, this period will be short because of the presence of airborne or waterborne microorganisms, which will be delivered rapidly onto the surface of the substrate. However, the subsurface of the substrate, for example the interior of newly formed vesicular volcanic rock, could well remain a vacant habitat for longer compared with the surface environment. Vacant habitats beyond Earth The observation that most habitable places on Earth are inhabited might easily lead to the hypothesis that metabolically active life occurs everywhere that it can be supported. This might be more colloquially stated as the hypothesis that ‘where there are habitats, there is life’. For reasons discussed in the previous section, this hypothesis is supported in most known habitats on Earth, but
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Box 1. Asteroid impacts and vacant habitats
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structure showed that the sediment could support microbial growth. Thus, the microbial impoverishment is not caused by chemical conditions in the sediment. Other factors might contribute to low microbial numbers at depth. For example, the salt concentrations, which approach twice that of seawater at some depths, might influence the gradient of microbial enumerations. However, hydrological data gathered from the drill cores show that the permeability of this section is low and that water within the section is a relic of the immediate post-impact environment [82,83]. The rocks below the section show an average temperature at the time of deposition of >350oC [84]. All of these data are consistent with a scenario that includes sterilization of the section by impact-induced heating (either directly or as a result of heat from the impact rocks below the section). The data might therefore provide evidence that the effects of low rate of water movement coupled with thermal sterilization by the impact resulted in a vacant habitat.
The Chesapeake Bay Impact Structure (Figure I) is an 85-km-diameter buried impact structure on the eastern seaboard of the USA that formed in a shallow marine environment during the late Eocene (35.3 Myr ago). During 2005 and 2006, it was cored to a composite depth of 1.76 km in a joint US Geological Survey–International Continental Scientific Drilling Program (USGS–ICDP) project [77–79]. Microbiological contamination control was used [80] to collect cores from the crater and enumerate prokaryote numbers throughout the length of each core. Microbial numbers declined logarithmically with depth, similar to results recorded from other deep subsurface sites. However, the gradient of decline was much steeper, with a biologically impoverished zone reported at depths of 867 and 1096 m in a section corresponding to sediments (tsunami deposits) laid down in the crater cavity formed after the impact [81]. At these depths, there were abundant redox couples (including dissolved organic carbon and sulfate) that could provide energy for microbial growth. Experiments using isolates from higher in the impact
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Figure I. Location of the Chesapeake Bay Impact Structure. Adapted from [81].
there are reasons why the hypothesis could break down on other planetary bodies. There are several plausible scenarios by which vacant habitats might exist on other planetary bodies (Figure 1). They can be broadly split into two categories. First, a planet wholly devoid of life, but which has available habitats; and second, a planet with life, but which has localized vacant habitats (Earth, as described above, could be such an example). An uninhabited planet with vacant habitats might occur as a result of one of the following five scenarios: (i) The planet is too young for an origin of life to have occurred, but contains habitable environments. This
assumes that an origin of life can occur some time after the appearance of habitable environments and is not always conterminous with the appearance of habitable environments. Not enough is currently known about the origin of life to assess this possibility [32–35]. This scenario assumes that life is not transferred into vacant habitats from another life-bearing planet [2,3]. (ii) The origin of life is extremely rare. Other planets might have habitable conditions for life, but life never originated to take advantage of the conditions available because the origin of life is just an unusual event [36,37]. This scenario also assumes that life is not transferred into vacant habitats from 75
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Planet too young for origin of life, but habitable environments exist Origin of life rare No conditions for origin of life
No origin of life
Conditions for origin of life too transient Origin of life occurs
Cataclysm
Planet devoid of life
Vacant habitats on an uninhabited planet Vacant habitats on an inhabited planet Insufficient evolutionary developments for colonization of certain habitats
Origin of life occurs
Habitats become sterilized and cut off, e.g. subsurface Transient habitats that are not colonized Newly formed habitats that are transiently vacant
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Figure 1. A categorization of vacant habitats.
another life-bearing planet [2,3]. (iii) The conditions for the origin of life do not exist. The origin of life might require prebiotic reactions to occur in conditions that are different from those suitable for life (e.g. in the interior of hydrothermal vents, well above the upper temperature limit for life [38–40]). If such environments did not exist on a planet, then one could imagine that conditions could be clement for life, but where local environments were never satisfactory for life to originate. This scenario also assumes that life is not transferred into vacant habitats from another life-bearing planet [2,3]. (iv) The conditions for the origin of life exist, but they are too transient. A planet with fluctuating geochemical and environment extremes might have transient conditions suitable for the origin of life and its subsequent propagation, but their duration is too short to enable life to emerge. This scenario again assumes that life is not transferred into vacant habitats from another life-bearing planet [2,3]. (v) Life originated, but a major transient cataclysm (e.g. a moonforming impact) wiped it out and it never re-established despite the planet subsequently being favourable for it. This scenario would also require that life did not originate again (which might result from a combination of situations ii– iv above) and that there was no re-establishment of life from surviving propagules [41] or from elsewhere [2,3]. Earth itself might have suffered early bombardments that were sufficient to affect early ecosystems severely, although they were not sufficient to extinguish life completely [42]. 76
Vacant habitats could also exist on inhabited planets. There are four circumstances in which they can be envisaged: (i) A planet where local habitats become sterilized and cut off from other inhabited regions, rendering them vacant. Subsurface examples of this category might exist on present-day Earth, as discussed above. (ii) A planet where habitable environments become available, but they are too transient to be colonized. An example could be permafrost melted on a cold planet, for example by small asteroid and comet impacts, which would provide a shortlived liquid water habitat, but the duration might be too short for colonization. (iii) A planet where sterile materials are formed by geological processes, such as asteroid and comet impacts and volcanic eruptions. These materials experience a period when they are habitable, but vacant. Examples on Earth include new lava flows. The distinction from (ii) is that the habitats are long lived, but the period of being vacant is short, whereas in (ii), the habitat itself is transient. (iv) A planet where habitats of a particular type are available, but the biochemical systems required to deal with the physical or chemical characteristics within them have not yet evolved, rendering the habitats vacant. An example in Earth history might be large areas of early land masses before the evolution of desiccation tolerance in microorganisms (assuming that they first evolved in the oceans) [43,44]. This category of vacant habitat has the clearest overlap with the biochemical reasons for vacant niches (i.e. evolutionary limitations).
Opinion Testing the ‘where there are habitats, there is life’ hypothesis The hypothesis, ‘where there are habitats, there is life’, is testable on a universal scale by studying planets in our Solar System and elsewhere. In the forthcoming decades, increasingly powerful telescopes both on the ground and in space will be constructed to detect earth-like planets around distant stars (e.g. [45–47]). The potential habitability of extrasolar planets can then be assessed using such telescopes [48,49]. If the atmospheric composition is determined by spectroscopy, models can be developed to predict the surface temperature on the planet. This requires knowledge of the characteristics of the parent star (i.e. the energetic and wavelength distribution of its radiation output), which can be obtained by direct observation. The presence of water might be observed in the atmospheric spectrum and inferred from the estimated temperature conditions on the planetary surface [50]. Spectroscopy will be used to look for several biosignatures of life [51–56], including high abundances of oxygen (although this presupposes the evolution of oxygenic photosynthesis), other gases such as methane and nitrous oxide out of equilibrium with purely geochemical processes, and/or the presence of surface-reflected spectra of pigments from organisms on the planetary surface [57,58]. Such biosignatures can be observed in the terrestrial spectrum [59,60]. If the hypothesis is true that where habitats exist, life will also be found, then one would expect to detect biosignatures of life on any extrasolar planets that appear to exhibit the necessary conditions for habitability. However, there are four caveats to testing the hypothesis in this way: (i) researchers have to assume that extraterrestrial life performs the same sort of biogeochemical transformations as terrestrial life and could therefore be detected. Perhaps one would fail to detect something that had a different biochemistry. However, a plausible rejoinder is that redox couples for life are universal (because the periodic table is universal) and, thus, one would expect life of any architecture to modify its planetary atmosphere in some way that would influence major carbon, nitrogen and oxygen-bearing gases, for instance. In other words, one would expect vacant niches for the cycling of major gases to be filled; (ii) a planet might appear to be habitable and exhibit no signal of life and then be categorized as a ‘vacant habitat’. However, it might in reality be uninhabitable because of a lifelimiting chemical extreme that cannot be detected from a distance with a telescope. For example, the low water activity associated with salts on Mars has been proposed as a serious potential limitation to the habitability of that planet [61], but the salts cannot be readily detected in the spectrum of light reflected from the planet; (iii) life might be present in all of the habitats available on an extrasolar planet, but at very low biomass such that planetary atmospheric conditions were not altered sufficiently to be detectable to astronomers. This would cause a false detection of a planetary-scale vacant habitat. This scenario could also be caused by biosignatures present at concentrations below the detectability of the telescope; and (iv) extrasolar planet detection can only be used to assess planetary-scale vacant habitats. It cannot rule out locally vacant habitats
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on an inhabited or apparently uninhabitable planetary body. Despite these caveats, if vacant habitats are a common phenomenon in the Universe, one would expect the study of extrasolar planets in the coming decades to result in a large catalogue of planets that by all available criteria are habitable, but where none, or few, exhibit biosignatures of life. In each specific case, the four caveats above could be assessed in more detail. With enough data points, researchers would eventually expect to have enough examples to be able to say either that one or more of the four caveats was relevant for a given planet, or that there is a suspiciously large number of apparently habitable planets that appear to lack any evidence of life. This would allow for a reasonably confident conclusion that the Universe does indeed contain many planets that are vacant habitats. In our Solar System, the comprehensive study of other planetary environments might yield candidate past or present-day vacant habitats with which to test the hypothesis. For example, on Mars, past obliquity changes might have yielded conditions conducive to the melting of ice [62]. If the conditions were transitory, vacant habitats could have been created. In some locations, they might even exist on that planet today, in so-called ‘Special Regions’ [63] (Box 2) or in permafrost [64] melted by asteroid and comet impacts. The ice-covered water bodies of the Jovian moon, Europa [65], and the Saturnian moon, Enceladus [66] are Outer Solar System targets that will be explored and will provide further information with which to assess the distribution of vacant habitats. Vacant habitats in ecology and evolutionary biology If extraterrestrial vacant habitats are discovered, what would this mean for ecology and evolutionary biology? Terrestrial ecology, particularly biogeochemistry, might have much to learn from these environments. Geochemical processes on Earth have been inextricably linked to life. The earliest carbon, sulfur and iron cycles on Earth were influenced by microbiota [67–69]. Biogeochemistry lacks a good set of abiotic controls with which to extract a true understanding of the influence and magnitude of these biotic contributions. Many problems exacerbate this challenge. Abiotic processes can themselves be influenced by biotic interactions. For instance, the oxidation of reduced iron in pyrite can be catalysed by iron oxides that have been produced by iron-oxidizing bacteria, confounding interpretation of the influence of biological and abiotic iron oxidation reactions on the formation of iron oxides [70]. This complicates attempts to study the provenance of iron oxides in the geological record, such as in ancient banded iron formations [71,72]. It is not sufficient to take a subtractive approach of merely identifying reactions directly mediated by a biota to understand the role of abiotic reactions. Although abiotic and biotic reactions can sometimes be separated (e.g. by investigating fractionation patterns of certain elements [73,74]) it is still difficult to develop a truly comprehensive understanding of the geochemical role of biota in different environments and under the influence of many geochemical cycles, particularly those that occurred in the past. 77
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Box 2. Ethics and vacant habitats Preventing human and robotic space missions from contaminating a potential extraterrestrial biota (or conversely, an extraterrestrial biota contaminating Earth) has occupied considerable thought in the various space programs across the world. Missions are categorized accordingly to planetary protection protocols devised by the Committee on Space Research (COSPAR) [85–87]. Missions with a low risk of contaminating a biota (such as missions to the planet Mercury, which has no appreciable atmosphere and is unlikely to harbour life) are categorized as Category I. Conversely, missions involving access to Mars ‘Special Regions’ (which are places on Mars experiencing temperatures greater than –25 8C for a few hours a year and a water activity of >0.5, and are thus deemed to be potentially habitable) [64] are categorized as Category IVc and require sterilization of the spacecraft or the parts of a spacecraft entering the region. All of these previous planetary protection considerations are based on the assumption that planets are either lifeless because they cannot support life or they have habitable environments that must be assumed to be inhabited. Before their biological exploration, the latter assumption is a reasonable and conservative approach to exploration. However, during the course of planetary exploration, vacant habitats might be discovered. They might also be artificially created. For example, a crashed spacecraft, particularly one containing a radioisotope thermoelectric generator (RTG) to produce power,
Vacant habitats in which geochemical processes occur without a biota, but in which the physical environmental conditions approximate to conditions in past or present terrestrial habitats, would offer an outstanding set of controlled comparisons. One example (depending on whether the planet has life) might be subglacial environments on Mars, where, for instance, the interactions of glaciers with volcanic substrates could provide a new understanding of the rate of chemical reactions at rock– ice and rock–water interfaces without the confounding effects of biology [75]. Sulfur, nitrogen and carbon cycles in the oceans of ice-covered moons [76] might similarly provide insights into the aquatic fate of these compounds on Earth and the pathways of abiotic processing. From the point of view of ecologies elsewhere, the search for the distribution of vacant habitats is an essential task in understanding what controls the distribution of life: what conditions preclude life elsewhere or limit its ubiquity? The distribution of vacant habitats will yield insights into the conditions required for the origin of life and the frequency with which these conditions are met. Vacant habitats will provide a better understanding of the uniqueness of Earth as an experiment in biological evolution. In summary, the extent of vacant habitats in the Universe is conjecture at the time of writing. The ubiquity of life on present-day Earth makes rare the conditions that result in vacant habitats. However, there are scenarios on other planetary bodies that might make them more abundant. The study of other planets will enable assessment of the abundance of vacant habitats in the Universe. Vacant habitats can potentially provide useful information on the role of a biota in biogeochemical processes on Earth and the factors that control the distribution of life in the Universe. Acknowledgements I thank John Raven and Harriet Jones for reading through the article and for their valuable comments. 78
might melt ice on a planetary body such as Mars or Europa, producing a locally habitable environment. The purposeful melting of ice might even be done to create a vacant habitat. Is the deliberate inoculation of these vacant habitats acceptable? There are practical reasons why one might want to introduce life into such habitats. It would be a remarkable scientific experiment, offering the opportunity to study organismal succession and community development in a habitat completely devoid of life. How biogeochemical cycles become established and how the vacant niches within the vacant habitat become filled could be investigated. However, there is an obvious ethical dilemma associated with vacant habitats and their constituent vacant niches. On the one hand, the introduction of life into a vacant habitat on another planetary body provides an opportunity to expand the boundaries of life on other planetary surfaces, something that one might regard as beneficial to propagating the wider abundance of life in the Universe, particularly when one considers that the contaminant organisms are not threatening indigenous organisms in that habitat. On the other hand, it is possible the habitat will eventually become colonized by an indigenous biota or by a biota yet to originate. Thus, the introduction of organisms would compromise the future potential of an indigenous biosphere. Vacant habitats pose an ethical problem, which will impinge directly on practical policies concerning the sterilization of spacecraft entering or sampling vacant habitats.
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Trends in Ecology and Evolution February 2011, Vol. 26, No. 2 51 Lovelock, J. (1975) Thermodynamics and recognition of alien biospheres. Proc. R. Soc. B 189, 167–181 52 Le´ger, A. et al. (1993) Search for primitive life on a distant planet: relevance of O2 and O3 detection. Astron. Astrophys. 277, 309–313 53 Wolstencroft, R.D. and Raven, J.A. (2002) Photosynthesis: likelihood of occurrence and possibility of detection on Earth-like planets. Icarus 157, 535–548 54 Segura, A. et al. (2005) Biosignatures from Earth-like planets around M dwarfs. Astrobiology 5, 706–725 55 Kaltenegger, L. and Selsis, F. (2007) Biomarkers set in context. In Extrasolar Planets: Formation, Detection and Dynamics (Dvorak, R., ed.), pp. 79–97, Wiley 56 Kaltenegger, L. and Selsis, F. (2009) Characterising extrasolar planets using spectral fingerprints. Comptes Rendus Palevol. 8, 679–691 57 Kiang, N.Y. et al. (2007) Spectral signatures of photosynthesis. I. Review of Earth organisms. Astrobiology 7, 222–251 58 Kiang, N.Y. et al. (2007) Spectral signatures of photosynthesis. II. Coevolution with other stars and the atmosphere on extrasolar worlds. Astrobiology 7, 252–274 59 Sagan, C. et al. (1993) A search for life on Earth from the Galileo spacecraft. Nature 365, 715–722 60 Segura, A. (2010) Earth as an exoplanet. Revista Mexicana de Ciencias Geol. 27, 374–385 61 Tosca, N.J. et al. (2008) Water activity and the challenge for life on early Mars. Science 320, 1204–1207 62 Jakosky, B.M. et al. (2003) Subfreezing activity of microorganisms and the potential habitability of Mars’ polar regions. Astrobiology 3, 343–350 63 Balme, M.R. and Gallagher, C. (2009) An equatorial periglacial landscape on Mars. Earth Planet. Sci. Lett. 285, 1–15 64 Kminek, G. et al. (2010) Report on the COSPAR Mars Special Regions Colloquium. Adv. Space Res. 46, 811–829 65 Marion, G.M. et al. (2003) The search for life on Europa: limiting environmental factors, potential habitats, and Earth analogues. Astrobiology 3, 785–811 66 McKay, C.P. et al. (2008) The possible origin and persistence of life on Enceladus and detection of biomarkers in the plume. Astrobiology 8, 909–919 67 Canfield, D.E. et al. (2006) Early anaerobic metabolisms. Phil. Trans. Royal. Soc. 361, 1819–1836 68 Sleep, N.H. and Bird, D.K. (2007) Niches of the pre-photosynthetic biosphere and geologic preservation of Earth’s earliest ecology. Geobiology 5, 101–107 69 Lyons, T.W. and Gill, B.C. (2010) Ancient sulphur cycling and oxygenation of the early biosphere. Elements 6, 93–99 70 Emerson, D. et al. (2010) Iron-oxidizing bacteria: an environmental and genomic perspective. Ann. Rev. Microbiology 64, 561–583 71 Kappler, A. et al. (2005) Deposition of banded iron formations by anoyxgenic phototrophic Fe(II)-oxidising bacteria. Geology 33, 865–868 72 Croal, L.R. et al. (2009) Phototrophic Fe(II) oxidation in an atmosphere of H2: implications for archean banded iron formations. Geobiology 7, 21–24 73 Horita, J. (2005) Some perspectives on isotope biosignatures for early life. Chem. Geology 218, 171–186 74 Thomazo, C. et al. (2009) Biological activity and the Earth’s surface evolution: insights from carbon, sulphur, nitrogen and iron stable isotopes in the rock record. Comptes Rendus Palevol. 8, 665–678 75 Cockell, C.S. et al. Subglacial environments and the search for life beyond the Earth. Antarctic Subglacial Aquatic Environments (Siegert, M., Kennicutt, M., Bindschadler, R). American Geophys Union (in press) 76 Strazzulla, G. et al. (2009) The origin of sulphur-bearing species on the surfaces of icy satellites. Adv. Space Res. 43, 1442–1445 77 Poag, C.W. (1999) The Chesapeake Invader, Princeton University Press 78 Poag, C.W. et al. (1992) Deep Sea Drilling Project Site 612 bolide event: new evidence of a late Eocene impact-wave deposit and a possible impact site, U.S. east coast. Geology 10, 771–774 79 Gohn, G.S. et al. (2008) Deep drilling of the Chesapeake Bay impact structure. Science 320, 1740–1745 80 Gronstal, A.L. et al. (2009) Contamination assessment in biological sampling of the Eyreville core, Chesapeake Bay impact structure. In: Gohn, G.S. et al., (ed.), Deep Drilling in the Chesapeake Bay Impact Structure, pp. 951–964, Geological Society of America Special Paper 458 81 Cockell, C.S. et al. (2009) Microbial abundance in the deep subsurface of the Chesapeake Bay impact structure: relationship to lithology and
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Opinion impact processes. In Deep Drilling in the Chesapeake Bay Impact Structure (Gohn, G.S. et al., eds), pp. 941–950, Geological Society of America Special Paper 458 82 Sanford, W.E. (2005) A simulation of the hydrothermal response to the Chesapeake Bay bolide impact. Geofluids 5, 185–201 83 Sanford, W.E. et al. (2009) Pore-water chemistry from the ICGP-USGS core hole in the Chesapeake Bay impact structure – implications for paleohydrology, microbial habitat, and water resources. In Deep Drilling in the Chesapeake Bay Impact Structure (Gohn, G.S. et al., eds), pp. 867–890, Geological Society of America Special Paper 458 84 Malinconico, M.L. et al. (2009) Post-impact heat conduction and compaction-driven fluid flow in the Chesapeake Bay impact
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Vacant habitats in the Universe Charles S. Cockell CEPSAR, Open University, Milton Keynes, UK, MK7 6AA
The search for life on other planets usually makes the assumption that where there is a habitat, it will contain life. On the present-day Earth, uninhabited habitats (or vacant habitats) are rare, but might occur, for example, in subsurface oils or impact craters that have been thermally sterilized in the past. Beyond Earth, vacant habitats might similarly exist on inhabited planets or on uninhabited planets, for example on a habitable planet where life never originated. The hypothesis that vacant habitats are abundant in the Universe is testable by studying other planets. In this review, I discuss how the study of vacant habitats might ultimately inform an understanding of how life has influenced geochemical conditions on Earth.
The search for vacant habitats The motivation to explore other planets for the presence of life is to test the hypothesis that life has arisen on planetary bodies other than Earth and, if it does exist elsewhere, to investigate its ubiquity. These scientific objectives have become something of a one-sided quest, focussing on the search for the presence of life, rather than its absence. This is unsurprising, as investigating lifeless locations does not engage the public imagination; neither does it, at first glance, appear to be a promising avenue of scientific research. The discovery of life beyond Earth would open up a variety of scientific possibilities. For instance, if the newly discovered life was related to life on Earth, island biogeography would develop an interplanetary scope [1] and so, therefore, would the science of ecology. Such a scenario could plausibly be the case for a Martian biota composed of the descendants or the ancestors of terrestrial biota, resulting from the transfer of material in asteroid and comet impacts from Earth to Mars and vice versa [2,3]. If the extraterrestrial life derived from an independent origin, either discovered in our Solar System or remotely on extrasolar planets (see Glossary) orbiting distant stars, then new vistas of astronomy, biogeochemistry, biology and many other fields would open up in investigating the structure and behaviour of this other life [4]. However, an unbiased study of the factors required for the development of life in the Universe must also examine environments that are lifeless and explore the reasons for their lack of life. One obvious way in which other planetary bodies can be rendered lifeless is by environmental conditions that are too extreme to sustain any type of biology. To assess the plausibility of this scenario, one needs to Corresponding author: Cockell, C.S. ([email protected]).
compare the conditions required for the growth and reproduction of life on Earth with the measured physical and chemical parameters in any extraterrestrial environment, accepting that this is a conservative assessment based on the one type of life that is currently known [5–7]. In this review, I focus on another type of lifeless environment: one in which there is no life, but where life could be sustained. These places have been called uninhabited habitable habitats (sensu [8]), but because a habitat is, by definition, habitable then the middle qualifier is redundant and they are better referred to as ‘uninhabited habitats’. Here, I call them ‘vacant habitats’. I am generally referring to sterile habitats, but they could also include habitats that contain inactive life on an otherwise inhabited planet. Thus, the term ‘vacant’ means vacant of metabolically active life. A ‘vacant habitat’ is also distinguished from a ‘vacant niche’ [9–12]. The former is a physical space that could support life, but has none in it, whereas the latter is a functional definition of a specific set of energy and nutrient availabilities that could be used by life, but are not. Clearly, if a habitat is vacant, it implies that it must contain empty niche(s). Vacant habitats occur at different scales. They could exist on a planetary scale, in the case of an uninhabited, but habitable planet. They can also occur at the micron scale. For example, a habitable unoccupied micron-sized space between two microorganisms in soil would be a vacant habitat. Vacant habitats at these scales might be common, although short-lived. In this paper I am primarily concerned with vacant habitats at macroscopic scales.
Glossary Astrobiology: the area of scientific enquiry that lies at the interface between biological sciences and planetary sciences or astronomy. Banded iron formation: mineral formation found in rocks aged between 2.5 billion and 1.8 billion years old. It is made of alternating bands of iron oxides and silica-rich rocks. Biosignature: any phenomenon produced by life; particularly mineral signatures in the case of astrobiology. Exoplanet or extrasolar planet: a planet orbiting a star other than the Sun. Extremophile: an organism (particularly microorganisms) that inhabit extremes of chemical or physical conditions. Heterotroph: an organism that obtains its energy from organic carbon, particularly that produced by other organisms. Iron-oxidizing bacteria: bacteria that use reduced iron (Fe2+) as an electron donor to generate energy for growth. Jovian moons: the moons of the giant gas planet, Jupiter. Planetary protection: the prevention of the contamination of other planetary bodies (termed ‘forward contamination’) or the contamination of the Earth with extraterrestrial organisms (termed ‘back contamination’). Redox couple: an oxidizing and reducing agent that together can be used by microorganisms to conserve energy for growth. Subglacial environment: environment under glaciers or ice sheets. Vacant (or uninhabited) habitat: a habitat that can theoretically sustain life, but in which there are no active organisms.
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Opinion To define a habitat as ‘vacant’ requires the identification of a species that can be shown, experimentally or theoretically, to be capable of living in that habitat, a point of logic previously raised with respect to the notion of ‘vacant niches’ [11,12]. The assessment of the extent of vacant habitats (and vacant niches) is therefore necessarily conservative and bounded by what is known about life. Environments classified as uninhabitable might be suitable for life with appropriate biochemistries that are yet to evolve, that have not yet been discovered, or that do not exist on present-day Earth. Thus, the set of vacant habitats that is catalogued is a minimum set. Vacant habitats on Earth Are there any examples of vacant habitats on Earth? Certainly, these places do not obviously constitute a large area of the planet and their rarity might contribute to the widely held assumption that life will be found in any location where physical and chemical conditions are conducive to it. A more reductionist assumption goes one step further and posits that where there is merely water, there is likely to be life. Indeed, this dogma has been used to guide the search for life on other planets; a ‘follow the water’ approach to life detection [13,14] (although, of course, not all liquid water is habitable because of inappropriate temperatures, water activities, etc. [15,16]). The presumed ubiquity of life in habitable places is based on a prejudice derived from our experiences of life on Earth. In most habitats on Earth that are connected to the surface photosynthetic biosphere, and where physical and chemical conditions are conducive to microbial growth, there are microorganisms. Photosynthesis generates a vast quantity of carbon, approximately 1 x 1016 mole C per year [17,18]. This carbon leaches into most available habitat space and provides energy for heterotrophs. These organisms can be aerobic, using oxygen as the electron acceptor, yet another easily diffused waste product of the photosynthetic biosphere. Alternatively, they can ferment or use other electron acceptors coupled to anaerobic metabolisms. The pervasive nature of carbon on Earth leads to the observation that all habitable spaces are colonized [19]. Along with other elements and compounds from rocks and dead biota, this carbon usually contaminates water bodies, however transient, leading to the further observation (and thus dogma) that where there is liquid water, there is life. On Earth, one way to achieve a vacant habitat over a significant length of time is for a habitable space to be separated from the surface photosynthetic biosphere, sterilized and then for it to remain disconnected from the surface. These conditions are rare, but where they do exist they are most likely to be in the deep subsurface, an environment only recently explored for its microbial diversity [20–22].There is some tantalizing evidence for such habitats. Petroleum engineers are interested in the microbial degradation of oils, because these processes affect the quality of crude oil and the products derived from it by causing a net destruction of saturated hydrocarbons. The state of oil biodegradation can be regarded as a proxy for microbial activity in any subsurface oil reservoir. For example, the Peace River and Athabasca tar sands in Alberta, Canada contain over 1.3 trillion barrels of tar 74
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sand oil and have therefore attracted considerable economic, and thus scientific, attention [23–25]. Oil quality is known to increase from the eastern regions of these sands to the western; in the former case, oils are often completely depleted in saturated hydrocarbons, whereas in the west, the oils contain 55% saturated hydrocarbons and exhibit minimal degradation. Modelling of the burial history of the oils suggests that oils in the eastern tar sands never reached temperatures greater than 655 8C and so would have been subject to microbial degradation [25]. However, the models also suggest that the oils in the western sands were heated to above the 80 8C pasteurization temperature 85 million to 90 million years ago and could have reached temperatures up to 100 8C, effectively sterilizing them and accounting for their good preservation. Any process that can deliver a localized pulse of sterilizing energy into an inhabited deep subsurface location, which subsequently remains isolated, can potentially yield vacant habitats. Asteroid and comet impacts are one such mechanism. The kinetic energy of these objects, a proportion of which is converted to thermal energy during impact [26], can render the immediate surroundings sterile. The pulse of energy can be sufficiently large that the target rocks can be heated for many thousands to millions of years after impact, depending on the size of the impactor [27–39]. If the period when temperatures exceed the upper temperature limit for life coincides with the time when local geological rearrangements isolate some of the target rocks, then a vacant habitat could be formed. This might have been the case in the deep subsurface of the Chesapeake Bay Impact Structure in the eastern USA (Box 1). These examples are, however, rare, and the extent of the sterility and the period of sterilization uncertain. However, these uncertainties serve to underline the paucity of identifiable vacant habitats on Earth. Vacant habitats can potentially exist transiently on Earth where a sudden geological disturbance occurs, producing a fresh and sterile substrate. For example, a newly formed molten and sterile volcanic lava flow will eventually cool down to below the upper temperature limit for life. There might be a period that defines this place as a vacant habitat between the instant at which the temperature drops below the critical threshold and the instant at which the first microorganisms land on the rock [30,31] and begin to be metabolically active. For most substrates, this period will be short because of the presence of airborne or waterborne microorganisms, which will be delivered rapidly onto the surface of the substrate. However, the subsurface of the substrate, for example the interior of newly formed vesicular volcanic rock, could well remain a vacant habitat for longer compared with the surface environment. Vacant habitats beyond Earth The observation that most habitable places on Earth are inhabited might easily lead to the hypothesis that metabolically active life occurs everywhere that it can be supported. This might be more colloquially stated as the hypothesis that ‘where there are habitats, there is life’. For reasons discussed in the previous section, this hypothesis is supported in most known habitats on Earth, but
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Box 1. Asteroid impacts and vacant habitats
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structure showed that the sediment could support microbial growth. Thus, the microbial impoverishment is not caused by chemical conditions in the sediment. Other factors might contribute to low microbial numbers at depth. For example, the salt concentrations, which approach twice that of seawater at some depths, might influence the gradient of microbial enumerations. However, hydrological data gathered from the drill cores show that the permeability of this section is low and that water within the section is a relic of the immediate post-impact environment [82,83]. The rocks below the section show an average temperature at the time of deposition of >350oC [84]. All of these data are consistent with a scenario that includes sterilization of the section by impact-induced heating (either directly or as a result of heat from the impact rocks below the section). The data might therefore provide evidence that the effects of low rate of water movement coupled with thermal sterilization by the impact resulted in a vacant habitat.
The Chesapeake Bay Impact Structure (Figure I) is an 85-km-diameter buried impact structure on the eastern seaboard of the USA that formed in a shallow marine environment during the late Eocene (35.3 Myr ago). During 2005 and 2006, it was cored to a composite depth of 1.76 km in a joint US Geological Survey–International Continental Scientific Drilling Program (USGS–ICDP) project [77–79]. Microbiological contamination control was used [80] to collect cores from the crater and enumerate prokaryote numbers throughout the length of each core. Microbial numbers declined logarithmically with depth, similar to results recorded from other deep subsurface sites. However, the gradient of decline was much steeper, with a biologically impoverished zone reported at depths of 867 and 1096 m in a section corresponding to sediments (tsunami deposits) laid down in the crater cavity formed after the impact [81]. At these depths, there were abundant redox couples (including dissolved organic carbon and sulfate) that could provide energy for microbial growth. Experiments using isolates from higher in the impact
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Figure I. Location of the Chesapeake Bay Impact Structure. Adapted from [81].
there are reasons why the hypothesis could break down on other planetary bodies. There are several plausible scenarios by which vacant habitats might exist on other planetary bodies (Figure 1). They can be broadly split into two categories. First, a planet wholly devoid of life, but which has available habitats; and second, a planet with life, but which has localized vacant habitats (Earth, as described above, could be such an example). An uninhabited planet with vacant habitats might occur as a result of one of the following five scenarios: (i) The planet is too young for an origin of life to have occurred, but contains habitable environments. This
assumes that an origin of life can occur some time after the appearance of habitable environments and is not always conterminous with the appearance of habitable environments. Not enough is currently known about the origin of life to assess this possibility [32–35]. This scenario assumes that life is not transferred into vacant habitats from another life-bearing planet [2,3]. (ii) The origin of life is extremely rare. Other planets might have habitable conditions for life, but life never originated to take advantage of the conditions available because the origin of life is just an unusual event [36,37]. This scenario also assumes that life is not transferred into vacant habitats from 75
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Planet too young for origin of life, but habitable environments exist Origin of life rare No conditions for origin of life
No origin of life
Conditions for origin of life too transient Origin of life occurs
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Vacant habitats on an uninhabited planet Vacant habitats on an inhabited planet Insufficient evolutionary developments for colonization of certain habitats
Origin of life occurs
Habitats become sterilized and cut off, e.g. subsurface Transient habitats that are not colonized Newly formed habitats that are transiently vacant
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Figure 1. A categorization of vacant habitats.
another life-bearing planet [2,3]. (iii) The conditions for the origin of life do not exist. The origin of life might require prebiotic reactions to occur in conditions that are different from those suitable for life (e.g. in the interior of hydrothermal vents, well above the upper temperature limit for life [38–40]). If such environments did not exist on a planet, then one could imagine that conditions could be clement for life, but where local environments were never satisfactory for life to originate. This scenario also assumes that life is not transferred into vacant habitats from another life-bearing planet [2,3]. (iv) The conditions for the origin of life exist, but they are too transient. A planet with fluctuating geochemical and environment extremes might have transient conditions suitable for the origin of life and its subsequent propagation, but their duration is too short to enable life to emerge. This scenario again assumes that life is not transferred into vacant habitats from another life-bearing planet [2,3]. (v) Life originated, but a major transient cataclysm (e.g. a moonforming impact) wiped it out and it never re-established despite the planet subsequently being favourable for it. This scenario would also require that life did not originate again (which might result from a combination of situations ii– iv above) and that there was no re-establishment of life from surviving propagules [41] or from elsewhere [2,3]. Earth itself might have suffered early bombardments that were sufficient to affect early ecosystems severely, although they were not sufficient to extinguish life completely [42]. 76
Vacant habitats could also exist on inhabited planets. There are four circumstances in which they can be envisaged: (i) A planet where local habitats become sterilized and cut off from other inhabited regions, rendering them vacant. Subsurface examples of this category might exist on present-day Earth, as discussed above. (ii) A planet where habitable environments become available, but they are too transient to be colonized. An example could be permafrost melted on a cold planet, for example by small asteroid and comet impacts, which would provide a shortlived liquid water habitat, but the duration might be too short for colonization. (iii) A planet where sterile materials are formed by geological processes, such as asteroid and comet impacts and volcanic eruptions. These materials experience a period when they are habitable, but vacant. Examples on Earth include new lava flows. The distinction from (ii) is that the habitats are long lived, but the period of being vacant is short, whereas in (ii), the habitat itself is transient. (iv) A planet where habitats of a particular type are available, but the biochemical systems required to deal with the physical or chemical characteristics within them have not yet evolved, rendering the habitats vacant. An example in Earth history might be large areas of early land masses before the evolution of desiccation tolerance in microorganisms (assuming that they first evolved in the oceans) [43,44]. This category of vacant habitat has the clearest overlap with the biochemical reasons for vacant niches (i.e. evolutionary limitations).
Opinion Testing the ‘where there are habitats, there is life’ hypothesis The hypothesis, ‘where there are habitats, there is life’, is testable on a universal scale by studying planets in our Solar System and elsewhere. In the forthcoming decades, increasingly powerful telescopes both on the ground and in space will be constructed to detect earth-like planets around distant stars (e.g. [45–47]). The potential habitability of extrasolar planets can then be assessed using such telescopes [48,49]. If the atmospheric composition is determined by spectroscopy, models can be developed to predict the surface temperature on the planet. This requires knowledge of the characteristics of the parent star (i.e. the energetic and wavelength distribution of its radiation output), which can be obtained by direct observation. The presence of water might be observed in the atmospheric spectrum and inferred from the estimated temperature conditions on the planetary surface [50]. Spectroscopy will be used to look for several biosignatures of life [51–56], including high abundances of oxygen (although this presupposes the evolution of oxygenic photosynthesis), other gases such as methane and nitrous oxide out of equilibrium with purely geochemical processes, and/or the presence of surface-reflected spectra of pigments from organisms on the planetary surface [57,58]. Such biosignatures can be observed in the terrestrial spectrum [59,60]. If the hypothesis is true that where habitats exist, life will also be found, then one would expect to detect biosignatures of life on any extrasolar planets that appear to exhibit the necessary conditions for habitability. However, there are four caveats to testing the hypothesis in this way: (i) researchers have to assume that extraterrestrial life performs the same sort of biogeochemical transformations as terrestrial life and could therefore be detected. Perhaps one would fail to detect something that had a different biochemistry. However, a plausible rejoinder is that redox couples for life are universal (because the periodic table is universal) and, thus, one would expect life of any architecture to modify its planetary atmosphere in some way that would influence major carbon, nitrogen and oxygen-bearing gases, for instance. In other words, one would expect vacant niches for the cycling of major gases to be filled; (ii) a planet might appear to be habitable and exhibit no signal of life and then be categorized as a ‘vacant habitat’. However, it might in reality be uninhabitable because of a lifelimiting chemical extreme that cannot be detected from a distance with a telescope. For example, the low water activity associated with salts on Mars has been proposed as a serious potential limitation to the habitability of that planet [61], but the salts cannot be readily detected in the spectrum of light reflected from the planet; (iii) life might be present in all of the habitats available on an extrasolar planet, but at very low biomass such that planetary atmospheric conditions were not altered sufficiently to be detectable to astronomers. This would cause a false detection of a planetary-scale vacant habitat. This scenario could also be caused by biosignatures present at concentrations below the detectability of the telescope; and (iv) extrasolar planet detection can only be used to assess planetary-scale vacant habitats. It cannot rule out locally vacant habitats
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on an inhabited or apparently uninhabitable planetary body. Despite these caveats, if vacant habitats are a common phenomenon in the Universe, one would expect the study of extrasolar planets in the coming decades to result in a large catalogue of planets that by all available criteria are habitable, but where none, or few, exhibit biosignatures of life. In each specific case, the four caveats above could be assessed in more detail. With enough data points, researchers would eventually expect to have enough examples to be able to say either that one or more of the four caveats was relevant for a given planet, or that there is a suspiciously large number of apparently habitable planets that appear to lack any evidence of life. This would allow for a reasonably confident conclusion that the Universe does indeed contain many planets that are vacant habitats. In our Solar System, the comprehensive study of other planetary environments might yield candidate past or present-day vacant habitats with which to test the hypothesis. For example, on Mars, past obliquity changes might have yielded conditions conducive to the melting of ice [62]. If the conditions were transitory, vacant habitats could have been created. In some locations, they might even exist on that planet today, in so-called ‘Special Regions’ [63] (Box 2) or in permafrost [64] melted by asteroid and comet impacts. The ice-covered water bodies of the Jovian moon, Europa [65], and the Saturnian moon, Enceladus [66] are Outer Solar System targets that will be explored and will provide further information with which to assess the distribution of vacant habitats. Vacant habitats in ecology and evolutionary biology If extraterrestrial vacant habitats are discovered, what would this mean for ecology and evolutionary biology? Terrestrial ecology, particularly biogeochemistry, might have much to learn from these environments. Geochemical processes on Earth have been inextricably linked to life. The earliest carbon, sulfur and iron cycles on Earth were influenced by microbiota [67–69]. Biogeochemistry lacks a good set of abiotic controls with which to extract a true understanding of the influence and magnitude of these biotic contributions. Many problems exacerbate this challenge. Abiotic processes can themselves be influenced by biotic interactions. For instance, the oxidation of reduced iron in pyrite can be catalysed by iron oxides that have been produced by iron-oxidizing bacteria, confounding interpretation of the influence of biological and abiotic iron oxidation reactions on the formation of iron oxides [70]. This complicates attempts to study the provenance of iron oxides in the geological record, such as in ancient banded iron formations [71,72]. It is not sufficient to take a subtractive approach of merely identifying reactions directly mediated by a biota to understand the role of abiotic reactions. Although abiotic and biotic reactions can sometimes be separated (e.g. by investigating fractionation patterns of certain elements [73,74]) it is still difficult to develop a truly comprehensive understanding of the geochemical role of biota in different environments and under the influence of many geochemical cycles, particularly those that occurred in the past. 77
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Box 2. Ethics and vacant habitats Preventing human and robotic space missions from contaminating a potential extraterrestrial biota (or conversely, an extraterrestrial biota contaminating Earth) has occupied considerable thought in the various space programs across the world. Missions are categorized accordingly to planetary protection protocols devised by the Committee on Space Research (COSPAR) [85–87]. Missions with a low risk of contaminating a biota (such as missions to the planet Mercury, which has no appreciable atmosphere and is unlikely to harbour life) are categorized as Category I. Conversely, missions involving access to Mars ‘Special Regions’ (which are places on Mars experiencing temperatures greater than –25 8C for a few hours a year and a water activity of >0.5, and are thus deemed to be potentially habitable) [64] are categorized as Category IVc and require sterilization of the spacecraft or the parts of a spacecraft entering the region. All of these previous planetary protection considerations are based on the assumption that planets are either lifeless because they cannot support life or they have habitable environments that must be assumed to be inhabited. Before their biological exploration, the latter assumption is a reasonable and conservative approach to exploration. However, during the course of planetary exploration, vacant habitats might be discovered. They might also be artificially created. For example, a crashed spacecraft, particularly one containing a radioisotope thermoelectric generator (RTG) to produce power,
Vacant habitats in which geochemical processes occur without a biota, but in which the physical environmental conditions approximate to conditions in past or present terrestrial habitats, would offer an outstanding set of controlled comparisons. One example (depending on whether the planet has life) might be subglacial environments on Mars, where, for instance, the interactions of glaciers with volcanic substrates could provide a new understanding of the rate of chemical reactions at rock– ice and rock–water interfaces without the confounding effects of biology [75]. Sulfur, nitrogen and carbon cycles in the oceans of ice-covered moons [76] might similarly provide insights into the aquatic fate of these compounds on Earth and the pathways of abiotic processing. From the point of view of ecologies elsewhere, the search for the distribution of vacant habitats is an essential task in understanding what controls the distribution of life: what conditions preclude life elsewhere or limit its ubiquity? The distribution of vacant habitats will yield insights into the conditions required for the origin of life and the frequency with which these conditions are met. Vacant habitats will provide a better understanding of the uniqueness of Earth as an experiment in biological evolution. In summary, the extent of vacant habitats in the Universe is conjecture at the time of writing. The ubiquity of life on present-day Earth makes rare the conditions that result in vacant habitats. However, there are scenarios on other planetary bodies that might make them more abundant. The study of other planets will enable assessment of the abundance of vacant habitats in the Universe. Vacant habitats can potentially provide useful information on the role of a biota in biogeochemical processes on Earth and the factors that control the distribution of life in the Universe. Acknowledgements I thank John Raven and Harriet Jones for reading through the article and for their valuable comments. 78
might melt ice on a planetary body such as Mars or Europa, producing a locally habitable environment. The purposeful melting of ice might even be done to create a vacant habitat. Is the deliberate inoculation of these vacant habitats acceptable? There are practical reasons why one might want to introduce life into such habitats. It would be a remarkable scientific experiment, offering the opportunity to study organismal succession and community development in a habitat completely devoid of life. How biogeochemical cycles become established and how the vacant niches within the vacant habitat become filled could be investigated. However, there is an obvious ethical dilemma associated with vacant habitats and their constituent vacant niches. On the one hand, the introduction of life into a vacant habitat on another planetary body provides an opportunity to expand the boundaries of life on other planetary surfaces, something that one might regard as beneficial to propagating the wider abundance of life in the Universe, particularly when one considers that the contaminant organisms are not threatening indigenous organisms in that habitat. On the other hand, it is possible the habitat will eventually become colonized by an indigenous biota or by a biota yet to originate. Thus, the introduction of organisms would compromise the future potential of an indigenous biosphere. Vacant habitats pose an ethical problem, which will impinge directly on practical policies concerning the sterilization of spacecraft entering or sampling vacant habitats.
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