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Mars exploration motivates the search for extraterrestrial life, the development of space technologies, and the design of human missions and habitations. Here, we seek new insights and pose unresolved questions relating to the natural history of Mars, habitability, robotic and human exploration, planetary protection, and the impacts on human society. Key observations and findings include:
– high escape rates of early Mars' atmosphere, including loss of water, impact present-day habitability;
– putative fossils on Mars will likely be ambiguous biomarkers for life;
– microbial contamination resulting from human habitation is unavoidable; and
– based on Mars' current planetary protection category, robotic payload(s) should characterize the local martian environment for any life-forms prior to human habitation.
Some of the outstanding questions are:
– which interpretation of the hemispheric dichotomy of the planet is correct;
– to what degree did deep-penetrating faults transport subsurface liquids to Mars' surface;
– in what abundance are carbonates formed by atmospheric processes;
– what properties of martian meteorites could be used to constrain their source locations;
– the origin(s) of organic macromolecules;
– was/is Mars inhabited;
– how can missions designed to uncover microbial activity in the subsurface eliminate potential false positives caused by microbial contaminants from Earth;
– how can we ensure that humans and microbes form a stable and benign biosphere; and
– should humans relate to putative extraterrestrial life from a biocentric viewpoint (preservation of all biology), or anthropocentric viewpoint of expanding habitation of space?
Studies of Mars' evolution can shed light on the habitability of extrasolar planets. In addition, Mars exploration can drive future policy developments and confirm (or put into question) the feasibility and/or extent of human habitability of space.
Geomorphological studies of the hidden and protected subsurface environments are crucial to obtain a greater insight into the evolution of planetary landforms, hydrology, climate, geology and mineralogy. From an astrobiological point of view subsurface environments are of interest for their potential habitability as they are local environments that are partially or fully shielded from the high levels of space and solar radiation. Furthermore, in the case of Mars, there is an increasing interest in searching for the presence of past or extant life in its subsurface. These applications make it mandatory to investigate equipment and instrumentation that allow for the study of subsurface geomorphology, as well as organic chemical biomarkers, such as biomolecules, carbon, nitrogen and sulphur isotopes, and other biologically significant minerals and gases. Mines on Earth can be used as analogues to investigate the geomorphology of Martian subsurface environments and perform astrobiology studies. With that goal, we have developed a low-cost, robust, remotely operable subsurface rover called KORE (KOmpact Rover for Exploration). This work illustrates the studies of a terrestrial analogue for the exploration of Mars using KORE during the Mine Analogue Research 6 (MINAR 6) campaign with the low-cost 3D mapping technology InXSpace 3D (In situ 3D mapping tool eXploration of space 3D). InXSpace 3D utilizes an RGB-D camera that captures depth information in addition to the RGB data of an image, operating based on the structured light principle capable of providing depth information in mm scale resolution at sub 3 m mapping range. InXSpace 3D is used to capture point clouds of natural and artificial features, thereby obtaining information about geologically relevant structures and also to incorporate them in earth mining safety. We tested two of the dense simultaneous localization and mapping (SLAM) algorithms: Kintinuous and Real-Time Appearance-Based Mapping (RTAB-Map) to check the performance of InXSpace 3D in a dark mine environment. Also, the air accumulation of volatiles such as methane and formaldehyde due to thermogenic and mining process was measured with the environmental station payload on the rover platform, which caters to both astrobiological significance and mine safety. The main conclusions of this work are: (1) a comparison made between the RTAB-Map algorithm and Kintinuous algorithm showed the superiority of Kintinuous algorithm in providing better 3D reconstruction; although RTAB-Map algorithm captured more points than the Kintinuous algorithm in the dark mine environment; (2) a comparison of point cloud images captured with and without lighting conditions had a negligible effect on the surface density of the point clouds; (3) close-range imaging of the polygonal features occurring on the halite walls using InXSpace 3D provided mm-scale resolution to enable further characterization; (4) heuristic algorithms to quickly post-process the 3D point cloud data provided encouraging results for preliminary analyses; (5) we successfully demonstrated the application of KORE to mine safety; and (6) the multi-sensors platform on KORE successfully monitored the accumulated volatiles in the mine atmosphere during its operation. The findings obtained during this KORE campaign could be incorporated in designing and planning future subsurface rover explorations to potential planetary bodies such as Mars with synergistic applications to subsurface environments in mines on Earth.
Recent advances in nucleic acid extraction and sequencing have changed and expanded our understanding of the diversity of life in the terrestrial and marine subsurface. This chapter highlights recent developments in sequencing genetic material from the deep biosphere (spurred in part by the Census of Deep Life) and new bioinformatics approaches to present a synthesis of our current understanding of the biogeography of life in the deep biosphere. Building from this data framework, this chapter also explores emerging trends in understanding the ecology and evolution of subsurface life.
Autonomous exploration requires the use of movable platforms that carry a payload of instruments with a certain level of autonomy and communication with the operators. This is particularly challenging in subsurface environments, which may be more dangerous for human access and where communication with the surface is limited. Subsurface robotic exploration, which has been to date very limited, is interesting not only for science but also for cost-effective industrial exploitation of resources and safety assessments in mines. Furthermore, it has a direct application to exploration of extra-terrestrial subsurface environments of astrobiological and geological significance such as caves, lava tubes, impact or volcanic craters and subglacial conduits, for deriving in-situ mineralogical resources and establishing preliminary settlements. However, the technological solutions are generally tailor-made and are therefore considered as costly, fragile and environment-specific, further hindering their extensive and effective applications. To demonstrate the advantages of rover exploration for a broad-community, we have developed KORE (KOmpact Rover for Exploration); a low-cost, re-usable, rover multi-purpose platform. The rover platform has been developed as a technological demonstration for extra-terrestrial subsurface exploration and terrestrial mining operations pertaining to geomorphological mapping, environmental monitoring, gas leak detections and search and rescue operations in case of an accident. The present paper, the first part of a series of two, focuses on describing the development of a robust rover platform to perform dedicated geomorphological, astrobiological and mining tasks. KORE was further tested in the Mine Analogue Research 6 (MINAR6) campaign during September 2018 in the Boulby mine (UK), the second deepest potash mine in Europe at a subsurface depth of 1.1 km, the results of which will be presented in the second paper of this series. KORE is a large, semi-autonomous rover weighing 160 kg with L × W × H dimensions 1.2 m × 0.8 m × 1 m and a payload carrying capacity of 100 kg using 800 W traction power that can power to a maximum speed of 8.4 km h−1. The rover can be easily dismantled in three parts facilitating its transportation to any chosen site of exploration. Presently, the main scientific payloads on KORE are: (1) a three-dimensional mapping camera, (2) a methane detection system, (3) an environmental station capable of monitoring temperature, relative humidity, pressure and gases such as NO2, SO2, H2S, formaldehyde, CO, CO2, O3, O2, volatile organic compounds and particulates and (4) a robotic arm. Moreover, the design of the rover allows for integration of more sensors as per the scientific requirements in future expeditions. At the MINAR6 campaign, the technical readiness of KORE was demonstrated during 6 days of scientific research in the mine, with a total of 22 h of operation.
The deep subsurface of other planetary bodies is of special interest for robotic and human exploration. The subsurface provides access to planetary interior processes, thus yielding insights into planetary formation and evolution. On Mars, the subsurface might harbour the most habitable conditions. In the context of human exploration, the subsurface can provide refugia for habitation from extreme surface conditions. We describe the fifth Mine Analogue Research (MINAR 5) programme at 1 km depth in the Boulby Mine, UK in collaboration with Spaceward Bound NASA and the Kalam Centre, India, to test instruments and methods for the robotic and human exploration of deep environments on the Moon and Mars. The geological context in Permian evaporites provides an analogue to evaporitic materials on other planetary bodies such as Mars. A wide range of sample acquisition instruments (NASA drills, Small Planetary Impulse Tool (SPLIT) robotic hammer, universal sampling bags), analytical instruments (Raman spectroscopy, Close-Up Imager, Minion DNA sequencing technology, methane stable isotope analysis, biomolecule and metabolic life detection instruments) and environmental monitoring equipment (passive air particle sampler, particle detectors and environmental monitoring equipment) was deployed in an integrated campaign. Investigations included studying the geochemical signatures of chloride and sulphate evaporitic minerals, testing methods for life detection and planetary protection around human-tended operations, and investigations on the radiation environment of the deep subsurface. The MINAR analogue activity occurs in an active mine, showing how the development of space exploration technology can be used to contribute to addressing immediate Earth-based challenges. During the campaign, in collaboration with European Space Agency (ESA), MINAR was used for astronaut familiarization with future exploration tools and techniques. The campaign was used to develop primary and secondary school and primary to secondary transition curriculum materials on-site during the campaign which was focused on a classroom extra vehicular activity simulation.
To test the rate at which a lifeless but habitable environment (uninhabited habitat) can be colonized, artificial endolithic habitats were constructed in the laboratory and exposed to the natural environment. They were composed of sterile stacked sintered glass discs (stacks) containing CHNOPS elements, liquid water, energy and a carbon source, making them habitable for aerobic respiring organisms and phototrophs. One set of stacks was exposed fully to atmospheric conditions and one set was covered from direct overhead atmospheric input and precipitation. The process of colonization was heterogeneous across the stacks. After 3 months, all uninhabited habitats were colonized at all depths in both fully exposed and covered stacks. However, uninhabited habitable conditions persisted in covered stacks after 1 month, demonstrating the importance of the hydrological cycle in the connection between inhabited habitats and uninhabited habitats. Low porosity rocks were found to retard the extent of colonization compared with higher porosity rocks. Examination of genomic DNA demonstrated that the habitats were colonized by a community dominated by Proteobacteria. Covered stacks had a higher abundance of fungal sequences among eukaryotic colonizers. These data demonstrate the tight coupling between the appearance of habitable conditions and life and the reasons for the rarity of uninhabited habitats on the present-day Earth. On other planetary bodies, such as Mars, with more inclement atmospheres and less vigorous hydrological cycles or a lack of life, uninhabited habitats could persist for longer with consequences for the interpretation of data sent back by planetary science missions.
A number of natural events can cause ozone depletion, including asteroid and comet impacts, large-scale volcanism involving the stratospheric injection of chlorine, and close cosmic events such as supernovae. These events have previously been postulated to have been sole or contributory causes of mass extinctions. Following such events, UV-B radiation would have been elevated at the surface of the earth. The possibilities for detecting elevated UV-B as a kill mechanism in the fossil record are discussed. In the case of impact events and large-scale volcanism, the taxa affected by increases in UV-B radiation are likely to be similar to those affected by cooling and by the initial drop in irradiance caused by stratospheric dust injection. Thus UV-B may synergistically exacerbate the effects of these other environmental changes and contribute to stress in the biosphere, although UV-B alone is unlikely to cause a mass extinction. By the same token, however, this similarity in affected taxa is likely to make delineating the involvement of UV-B radiation in the fossil record more difficult. Cosmic events such as supernovae may produce smaller extinction events, but ones that are “cleaner” UV catastrophes without the involvement of other environmental changes.
The subsurface exploration of other planetary bodies can be used to unravel their geological history and assess their habitability. On Mars in particular, present-day habitable conditions may be restricted to the subsurface. Using a deep subsurface mine, we carried out a program of extraterrestrial analog research – MINe Analog Research (MINAR). MINAR aims to carry out the scientific study of the deep subsurface and test instrumentation designed for planetary surface exploration by investigating deep subsurface geology, whilst establishing the potential this technology has to be transferred into the mining industry. An integrated multi-instrument suite was used to investigate samples of representative evaporite minerals from a subsurface Permian evaporite sequence, in particular to assess mineral and elemental variations which provide small-scale regions of enhanced habitability. The instruments used were the Panoramic Camera emulator, Close-Up Imager, Raman spectrometer, Small Planetary Linear Impulse Tool, Ultrasonic drill and handheld X-ray diffraction (XRD). We present science results from the analog research and show that these instruments can be used to investigate in situ the geological context and mineralogical variations of a deep subsurface environment, and thus habitability, from millimetre to metre scales. We also show that these instruments are complementary. For example, the identification of primary evaporite minerals such as NaCl and KCl, which are difficult to detect by portable Raman spectrometers, can be accomplished with XRD. By contrast, Raman is highly effective at locating and detecting mineral inclusions in primary evaporite minerals. MINAR demonstrates the effective use of a deep subsurface environment for planetary instrument development, understanding the habitability of extreme deep subsurface environments on Earth and other planetary bodies, and advancing the use of space technology in economic mining.
Recently, the Kepler Space Telescope has detected several planets in orbit around a close binary star system. These so-called circumbinary planets will experience non-trivial spatial and temporal distributions of radiative flux on their surfaces, with features not seen in their single-star orbiting counterparts. Earth-like circumbinary planets inhabited by photosynthetic organisms will be forced to adapt to these unusual flux patterns. We map the flux received by putative Earth-like planets (as a function of surface latitude/longitude and time) orbiting the binary star systems Kepler-16 and Kepler-47, two star systems which already boast circumbinary exoplanet detections. The longitudinal and latitudinal distribution of flux is sensitive to the centre-of-mass motion of the binary, and the relative orbital phases of the binary and planet. Total eclipses of the secondary by the primary, as well as partial eclipses of the primary by the secondary add an extra forcing term to the system. We also find that the patterns of darkness on the surface are equally unique. Beyond the planet's polar circles, the surface spends a significantly longer time in darkness than latitudes around the equator, due to the stars’ motions delaying the first sunrise of spring (or hastening the last sunset of autumn). In the case of Kepler-47, we also find a weak longitudinal dependence for darkness, but this effect tends to average out if considered over many orbits. In the light of these flux and darkness patterns, we consider and discuss the prospects and challenges for photosynthetic organisms, using terrestrial analogues as a guide.
The mean air temperature of the Icelandic interior is below 10 °C. However, we have previously observed 16S rDNA sequences associated with thermophilic lineages in Icelandic basalts. Measurements of the temperatures of igneous rocks in Iceland showed that solar insolation of these low albedo substrates achieved a peak surface temperature of 44.5 °C. We isolated seven thermophilic Geobacillus species from basalt with optimal growth temperatures of ~65 °C. The minimum growth temperature of these organisms was ~36 °C, suggesting that they could be active in the rock environment. Basalt dissolution rates at 40 °C were increased in the presence of one of the isolates compared to abiotic controls, showing its potential to be involved in active biogeochemistry at environmental temperatures. These data raise the possibility of transient active thermophilic growth in macroclimatically cold rocky environments, implying that the biogeographical distribution of active thermophiles might be greater than previously understood. These data show that temperatures measured or predicted over large scales on a planet are not in themselves adequate to assess niches available to extremophiles at micron scales.
On Earth, microorganisms living under intense ultraviolet (UV) radiation stress can adopt endolithic lifestyles, growing within cracks and pore spaces in rocks. Intense UV irradiation encountered by microbes leads to death and significant damage to biomolecules, which also severely diminishes the likelihood of detecting signatures of life. Here we show that porous rocks shocked by asteroid or comet impacts provide protection for phototrophs and their biomolecules during 22 months of UV radiation exposure outside the International Space Station. The UV spectrum used approximated the high-UV flux on the surface of planets lacking ozone shields such as the early Earth. These data provide a demonstration that endolithic habitats can provide a refugium from the worst-case UV radiation environments on young planets and an empirical refutation of the idea that early intense UV radiation fluxes would have prevented phototrophs without the ability to form microbial mats or produce UV protective pigments from colonizing the surface of early landmasses.
From a biological point of view, all environments in the Universe can be categorized into one of three types: uninhabitable, uninhabited habitat or inhabited habitat. This paper describes and defines different habitat types in the Universe with a special focus on environments not usually encountered on the Earth, but which might be common on other planetary bodies. They include uninhabited habitats, subtypes of which are sterile habitats and organic-free habitats. Examples of the different types of environments are provided with reference to the Eyjafjallajökull, Iceland. These habitat types are used to identify testable hypotheses on the abundance of different habitats and the distribution of life in the Universe.
The biosignatures of life on Earth do not remain static, but change considerably over the planet's habitable lifetime. Earth's future biosphere, much like that of the early Earth, will consist of predominantly unicellular microorganisms due to the increased hostility of environmental conditions caused by the Sun as it enters the late stage of its main sequence evolution. Building on previous work, the productivity of the biosphere is evaluated during different stages of biosphere decline between 1 and 2.8 Gyr from present. A simple atmosphere–biosphere interaction model is used to estimate the atmospheric biomarker gas abundances at each stage and to assess the likelihood of remotely detecting the presence of life in low-productivity, microbial biospheres, putting an upper limit on the lifetime of Earth's remotely detectable biosignatures. Other potential biosignatures such as leaf reflectance and cloud cover are discussed.
The biosignatures of life on Earth are not fixed, but change with time as environmental conditions change and life living within those environments adapts to the new conditions. A latitude-based climate model, incorporating orbital parameter variations, was used to simulate conditions on the far-future Earth as the Sun enters the late main sequence. Over time, conditions increasingly favour a unicellular microbial biosphere, which can persist for a maximum of 2.8 Gyr from present. The biosignature changes associated with the likely biosphere changes are evaluated using a biosphere-atmosphere gas exchange model and their detectability is discussed. As future Earth-like exoplanet discoveries could be habitable planets nearing the end of their habitable lifetimes, this helps inform the search for the signatures of life beyond Earth
Cyanobacteria are capable of surviving the adverse conditions of low Earth orbit (LEO). We have previously demonstrated that Gloeocapsa strain OU_20, Chroococcidiopsis and akinetes of Anabaena cylindrica were able to survive 548 days of exposure to LEO. Motivated by an interest to understand how cyanobacteria can survive in LEO, we studied the strategies that Gloeocapsa strain OU_20 employs to survive in its natural environment, the upper region of the intertidal zone. Here, cyanobacteria are exposed to fluctuations in temperature, UV radiation, desiccation and salinity. We demonstrated that an increase in salinity from 6.5‰ (BG-11 medium) to 35.7‰ (similar to that of seawater), resulted in increased resistance to UV radiation (254 nm), vacuum (0.7×10−3±0.01 kPa) and cold temperatures (–20 °C). Concomitantly, biochemical analyses demonstrated that the amount of fatty acids and mycosporine-like amino acids (a UV absorbing pigment) were higher in the stressed cells. Morphological analysis demonstrated that the electron density and thickness of the mucilaginous sheath were also greater than in the control cells. Yet, the control and stressed cells both formed aggregates. As a result of studying the physiological adaptation of Gloeocapsa strain OU_20 in response to salinity, we postulate that survival in the high-intertidal zone and LEO involves a dense extracellular mucilaginous sheath and the formation of aggregates. We conclude that studying the physiological adaptation of cyanobacteria in the intertidal zone provides insight into understanding survival in LEO.
The future biosphere on Earth (as with its past) will be made up predominantly of unicellular micro-organisms. Unicellular life was probably present for at least 2.5 Gyr before multicellular life appeared and will likely be the only form of life capable of surviving on the planet in the far future, when the ageing Sun causes environmental conditions to become more hostile to more complex forms of life. Therefore, it is statistically more likely that habitable Earth-like exoplanets we discover will be at a stage in their habitable lifetime more conducive to supporting unicellular, rather than multicellular life. The end stage of habitability on Earth is the focus of this work. A simple, latitude-based climate model incorporating eccentricity and obliquity variations is used as a guide to the temperature evolution of the Earth over the next 3 Gyr. This allows inferences to be made about potential refuges for life, particularly in mountains and cold-trap (ice) caves and what forms of life could live in these environments. Results suggest that in high latitude regions, unicellular life could persist for up to 2.8 Gyr from present. This begins to answer the question of how the habitability of Earth will evolve at local scales alongside the Sun's main sequence evolution and, by extension, how the habitability of Earth-like planets would evolve over time with their own host stars.
Planetary protection regulations are in place to control the contamination of planets and moons with terrestrial micro-organisms in order to avoid jeopardizing future scientific investigations relating to the search for life. One environmental chemical factor of relevance in extraterrestrial environments, specifically in the moons of the outer solar system, is ammonia (NH3). Ammonia is known to be highly toxic to micro-organisms and may disrupt proton motive force, interfere with cellular redox reactions or cause an increase of cell pH. To test the survival potential of terrestrial micro-organisms exposed to such cold, ammonia-rich environments, and to judge whether current planetary protection regulations are sufficient, soil samples were exposed to concentrations of NH3 from 5 to 35% (v/v) at −80°C and room temperature for periods up to 11 months. Following exposure to 35% NH3, diverse spore-forming taxa survived, including representatives of the Firmicutes (Bacillus, Sporosarcina, Viridibacillus, Paenibacillus, Staphylococcus and Brevibacillus) and Actinobacteria (Streptomyces). Non-spore forming organisms also survived, including Proteobacteria (Pseudomonas) and Actinobacteria (Arthrobacter) that are known to have environmentally resistant resting states. Clostridium spp. were isolated from the exposed soil under anaerobic culture. High NH3 was shown to cause a reduction in viability of spores over time, but spore morphology was not visibly altered. In addition to its implications for planetary protection, these data show that a large number of bacteria, potentially including spore-forming pathogens, but also environmentally resistant non-spore-formers, can survive high ammonia concentrations.
Synthetic geomicrobiology is a potentially new branch of synthetic biology that seeks to achieve improvements in microbe–mineral interactions for practical applications. In this paper, laboratory and field data are provided on three geomicrobiology challenges in space: (1) soil formation from extraterrestrial regolith by biological rock weathering and/or the use of regolith as life support system feedstock, (2) biological extraction of economically important elements from rocks (biomining) and (3) biological solidification of surfaces and dust control on other planetary surfaces. The use of synthetic or engineered organisms in these three applications is discussed. These three examples are used to extract general common principles that might be applied to the design of organisms used in synthetic geomicrobiology.