Project Leader, Antarctic Astrobiology, British Antarctic Survey, Cambridge 1946–2002

David Donaldson Wynn-Williams, born 16th July, 1946, in West Kirby, Cheshire, UK and Founding Editor of the International Journal of Astrobiology, met an ‘untimely and unjust death’ (W. Block, Independent, 4th April, 2002) on 24th March, 2002, which left his colleagues and family deeply saddened.

Several viable halophilic archaebacteria were isolated previously from rock salt of Permo-Triassic age in an Austrian salt mine; one of these strains was the first to be recognized as a novel species from subterranean halite and was designated Halococcus salifodinae. The halophilic microorganisms have apparently survived in the salt sediments over extremely long periods of time. Halobacteria could therefore be suitable model organisms for exploring the possibility of long-term survival of microbes on other planets, in particular, since extraterrestrial halite has been detected in meteorites and is assumed to be present in the subsurface ocean on Europa. Our efforts are directed at the identification of the microbial content of ancient rock salt and the development of procedures for the investigation of the halobacterial response to extreme environmental conditions. Using modified culture media, further halophilic strains were isolated from freshly blasted rock salt and bore cores; in addition, growth of several haloarchaea was substantially improved. Molecular methods indicated the presence of at least 12 different 16S rRNA gene species in a sample of Alpine rock salt, but these strains have not been cultured yet. The exploration of Mars is a target of space missions in the 21st century; therefore, testing the survival of haloarchaea under conditions comparable to present-day Mars, using a simulation chamber, was begun. Preliminary results with Halococcus and Halobacterium species suggested at least tenfold higher survival rates when cells were kept in liquid brines than under dry conditions; staining of cells with the LIVE–DEAD kit, which discriminates between damaged and intact membranes, corroborated these data.

The lichen symbiotic organisms Fulgensia bracteata and Xanthoria elegans as well as their isolated photobionts and mycobionts were exposed to conditions simulating the extreme parameters of outer space in order to assess their limits of survival, e.g. during a potential interplanetary transfer or on the surface of an extraterrestrial body. Using the space simulation facilities at DLR, the test parameters under investigation were vacuum (10−3 Pa) and ultraviolet (UV) radiation at wavelength ranges from vacuum-UV to UV-A, applied separately or in combination. An analysis of vitality was made using confocal laser scanning microscopy and LIVE/DEAD staining using FUN I or SYTOX green. Intact lichens were extremely resistant to vacuum exposure as well as to UV radiation up to doses of about 160 kJ m−2 (200<λ<400 nm). Removal of the upper-cortex structure significantly increased the sensitivity of the lichens to the space parameters: already a relatively short treatment of about 5 h and a UV dose of about 50 kJ m−2 reduced the vitality rate to nearly 50%; however, the dose effect curves levelled off and continued treatment did not reduce the vitality further. Similar survival curves levelling off at higher UV doses were observed for the isolated photobionts; however, in the latter cases, the saturation occurred at five times lower doses (full UV spectrum). Also spores of the mycobionts showed a remarkable UV (254 nm) resistance up to doses of about 3 kJ m−2. The data suggest that the symbiotic features peculiar to lichens allow them to cope with the extreme conditions of outer space or even with Martian surface conditions provided suitable niche habitats are available to serve as refuges and complementary endogenous or exogenous protection mechanisms are established.

The discovery of subsurface communities has encouraged speculation that such communities might be present on planetary bodies exposed to harsh surface conditions, including the early Earth. While the astrobiology community has focused on the deep subsurface, near-subsurface environments are unique in that they provide some protection while allowing partial access to photosynthetically active radiation. Previously we identified near-surface microbial communities based on photosynthesis. Here we assess the productivity of such an ecosystem by measuring in situ carbon fixation rates in an intertidal marine beach through a diurnal cycle, and find them surprisingly productive. Gross fixation along a transect (99×1 m) perpendicular to the shore was highly variable and depended on factors such as moisture and mat type, with a mean of ~41 mg C fixed m−2 day−1. In contrast, an adjacent well-established cyanobacterial mat dominated by Lyngbya aestuarii was ~12 times as productive (~500 mg C fixed m−2 day−1). Measurements made of the Lyngbya mat at several times per year revealed a correlation between total hours of daylight and gross daily production. From these data, annual gross fixation was estimated for the Lyngbya mat and yielded a value of ~1.3×105 g m−2 yr−1. An analysis of pulse-chase data obtained in the study in conjunction with published literature on similar ecosystems suggests that subsurface interstitial mats may be an overlooked endogenous source of organic carbon, mostly in the form of excreted fixed carbon.

We examined the environmental stresses experienced by cyanobacteria living in endolithic gneissic habitats in the Haughton impact structure, Devon Island, Canadian High Arctic (75° N) and compared them with the endolithic habitat at the opposite latitude in the Dry Valleys of Antarctica (76° S). In the Arctic during the summer, there is a period for growth of approximately 2.5 months when temperatures rise above freezing. During this period, freeze–thaw can occur during the diurnal cycle, but freeze–thaw excursions are rare within higher-frequency temperature changes on the scale of minutes, in contrast with the Antarctic Dry Valleys. In the Arctic location rainfall of approximately 3 mm can occur in a single day and provides moisture for endolithic organisms for several days afterwards. This rainfall is an order of magnitude higher than that received in the Dry Valleys over 1 year. In the Dry Valleys, endolithic communities may potentially receive higher levels of ultraviolet radiation than the Arctic location because ozone depletion is more extreme. The less extreme environmental stresses experienced in the Arctic are confirmed by the presence of substantial epilithic growth, in contrast to the Dry Valleys. Despite the more extreme conditions experienced in the Antarctic location, the diversity of organisms within the endolithic habitat, which includes lichen and eukaryotic algal components, is higher than observed at the Arctic location, where genera of cyanobacteria dominate. The lower biodiversity in the Arctic may reflect the higher water flow through the rocks caused by precipitation and the more heterogeneous physical structure of the substrate. The data illustrate an instance in which extreme climate is anti-correlated with microbial biological diversity.

The polar desert is one of the most extreme environments on Earth. Endolithic organisms can escape or mitigate the hazards of the polar desert by using the resources available in the interior of rocks. We examined endolithic communities within crystalline rocks that have undergone shock metamorphism as a result of an asteroid or comet impact. Specifically, we present a characterization of the heterotrophic endolithic community and its environment in the interior of impact-shocked gneisses and their host polymict breccia from the Haughton impact structure on Devon Island, Nunavut, Canadian High Arctic. Microbiological colonization of impact-shocked rocks is facilitated by impact-induced fissures and cavities, which occur throughout the samples, the walls of which are lined with high abundances of biologically important elements owing to the partial volatilization of minerals within the rock during the impact. 27 heterotrophic bacteria were isolated from these shocked rocks and were identified by 16S rDNA sequencing. The isolates from the shocked gneiss and the host breccia are similar to each other, and to other heterotrophic communities isolated from polar environments, suggesting that the interiors of the rocks are colonized by microorganisms from the surrounding country rocks and soils. Inductively coupled plasma–atomic emission spectroscopy (ICP-AES), scanning electron microscopy (SEM) and energy dispersive X-ray (EDX) analysis were used to identify the chemical composition of the shocked materials and to document the in situ growth of microbes in their interiors. The identification of these heterotrophic communities within impact-shocked crystalline rocks extends our knowledge of the habitable biosphere on Earth. The colonization of the interiors of these samples has astrobiological applications both for considering terrestrial, microbiological contamination of meteorites from the Antarctic ice sheet and for investigating possible habitats for microbial organisms on the early Earth, and more speculatively, on Mars and other planetary bodies.

The Fourier transform-Raman spectra of two lacustrine sediment cores from Antarctic sites are reported. The Lake Hoare specimens were predominantly calcium carbonate, quartz and β-carotene, with chlorophyll and calcium sulphate being noted as minor components. No evidence was found for iron (III) oxide or oxy-hydroxide bands. The Lake Nella specimens, in contrast, contain chlorophyll and quartz predominantly, but the absence of β-carotene is noteworthy. Here, the presence of haematite and a haematite–goethite mixture have been identified, with weaker features such as those of scytonemin, characteristic of cyanobacterial mats. The Raman spectra indicate that two different types of lake chemistry have been operating and several reasons are proposed for this.

The vital ultraviolet- (UV-) protective and photosynthetic pigments of cyanobacteria and lichens (microbial symbioses) that dominate primary production in Antarctic desert ecosystems auto-fluoresce at short wavelengths. We therefore use a long-wavelength (1064 nm) infrared laser for non-intrusive in situ Raman spectrometry of their ecologically significant compounds (especially pigments). To confirm that the power loss at this longer wavelength is justified to avoid swamping by background fluorescence, we compared Raman spectra obtained with excitation at 1064, 852, 830, 785, 633 and 515 nm. These are typical of lasers used for Raman spectroscopy. We analysed communities of the cyanobacterium Nostoc commune and the highly pigmented lichens Acarospora chlorophana and Caloplaca saxicola. These require screening compounds (e.g. pigments such as scytonemin in cyanobacteria and rhizocarpic acid in the fungal symbiont of lichens). They are augmented by quenching pigments (e.g. carotenoids) to dissipate the energy of free radicals generated by penetrating UV. We also analysed organisms having avoidance strategies (e.g. endolithic communities within translucent rocks, including the common cyanobacterium Chroococcidiopsis). These require accessory pigments for photosynthesis at very low light intensities. Although some organisms gave useable Raman spectra with short-wavelength lasers, 1064 nm was the only excitation that was consistently excellent for all organisms. We conclude that a 1064 nm Raman spectrometer, miniaturized using an InGaAs detector, is the optimal instrument for in situ studies of pigmented microbial communities at the limits of life on Earth. This has practical potential for the quest for biomolecules residual from any former surface life on Mars.

The FT-Raman spectra of an Antarctic endolith from the LTER site at Lake Hoare are reported. The specimen provides an unusual occurrence of endolithic colonization of an igneous rock substratum, which analyses as microcline feldspar. The presence of aragonite in the red biological stratum and calcite in a fissure of the rock which has not been subjected to colonization can be attributed to the penetration of calcareous deposits from shallow ground water in an earlier environment in the Dry Valleys. The green biological layer is composed of chlorophyll and β-carotene. Comparison with previous Raman spectroscopic work on endoliths in sedimentary Beacon sandstone is effected.

A study of Rivularia stromatolites demonstrated seasonal and non-seasonal banding patterns of calcification, ‘sun-screen’ scytonemin pigment and nitrogen-fixing heterocysts. Calcification was controlled by seasonal events with abiogenic ‘winter’ deposition and biogenic ‘summer’ deposition. Scytonemin was produced as a series of complex bands, probably as a response to summer Atlantic weather systems. Its production was also correlated in part with the appearance of heterocysts. The heterocysts were produced in bands, the pattern of which was probably controlled by an internal regulatory system. Raman spectra of modern and ancient (up to 4000 year old) Rivularia showed that scytonemin and carotenoid pigment can persist in dried material for >100 yr. The 4000 year old fossils did not reveal any useful biomarkers.

In this paper, in this edition of the Journal commemorating the life and work of David Wynn-Williams, we consider approaches to the astrobiological investigation of Mars. We provide a brief account of the scientific rationale behind the approach presented here. In particular, we outline the capabilities of the Raman spectrometer for the detection of biomarkers. David Wynn-Williams was an active champion of this instrument who was keen to field-qualify a version in Antarctica with a view to flying a Raman instrument onboard a Mars-bound space mission. We examine a scenario for the deployment of such an instrument in conjunction with other instrumentation and argue that subsurface deployment of scientific instruments is essential if we are to succeed in detecting any evidence that may exist for former life on Mars. We outline a mission scenario – Vanguard – which represents a novel but low-risk, low-cost approach to Mars exploration that was conceived and developed jointly by one of the authors (Ellery) and the late David Wynn-Williams.

Paleolimnology provides information on the past chemical, physical and biological nature of water bodies. In polar regions, where global climatic changes can be exacerbated compared with lower latitudes, the science has become important for reconstructing past changes and in so doing, predicting possible effects of future changes. Owing to the association of life with water bodies, particularly stable water bodies sustained over many millennia, paleolake regions on the surface of Mars are of exobiological importance. In this mini-review, we use experience gathered in the High Arctic to describe the importance of paleolimnology in the Earth's polar regions as it pertains to the future application of this science to robotic and human exploration missions to the planet Mars.

The search for organic molecules and traces of life on Mars has been a major topic in planetary science for several decades. 26 years ago Viking, a mission dedicated to the search for life on Mars, detected no traces of life. The search for extinct or extant life on Mars is the future perspective of several missions to the red planet, for example Beagle 2, the lander of the Mars Express mission. In order to determine what those missions should be looking for, laboratory experiments under simulated Mars conditions are crucial. This review paper describes ongoing experiments that are being performed in support of future Mars spacecraft missions. Besides the description of the experiments, the experimental hardware and set-up, this paper also gives the scientific rationale behind those experiments. The historical background of the search for life on Mars is outlined, followed by a description of the Viking Lander biology and molecular analysis experiments and their results, as well as a summary of possible reasons why no organic compounds have been detected. A section concerning organic compounds in space and related experiments discusses the organic molecules we will use in simulation experiments. The set-up is discussed briefly in the following section. We conclude with an overview of future missions, stressing the relation between these missions and our laboratory experiments. The research described in this article has been developed as part of a Mars Express Recognized Cooperating Laboratory (RCL), and for planned future Mars missions such as the PASTEUR lander.

The biogeochemical dynamics of Si in temperate lakes is well documented and the role of biological uptake and recycling is well known. In this paper we examine the Si dynamics of a series of ice-covered, closed-basin lakes in the McMurdo Dry Valley region (~78° S) of Antarctica. Our data and calculations indicate that biological uptake of Si is not a major process in these lakes. Mass balance considerations in Lake Hoare, the youngest and the freshest lake, suggest that annual stream input during relatively low-flow years is minor and that Si dynamics is greatly influenced by hydrological variation and hence climatic changes affecting stream flow and lake level. The data imply that the Si input during high-flow years must dominate the system. Subtle changes in climate have a major control on Si input into the lake, and Si dynamics are not controlled by biogeochemical processes as in temperate systems.