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1.  Biosignatures on Mars: What, Where, and How? Implications for the Search for Martian Life 
Astrobiology  2015;15(11):998-1029.
The search for traces of life is one of the principal objectives of Mars exploration. Central to this objective is the concept of habitability, the set of conditions that allows the appearance of life and successful establishment of microorganisms in any one location. While environmental conditions may have been conducive to the appearance of life early in martian history, habitable conditions were always heterogeneous on a spatial scale and in a geological time frame. This “punctuated” scenario of habitability would have had important consequences for the evolution of martian life, as well as for the presence and preservation of traces of life at a specific landing site. We hypothesize that, given the lack of long-term, continuous habitability, if martian life developed, it was (and may still be) chemotrophic and anaerobic. Obtaining nutrition from the same kinds of sources as early terrestrial chemotrophic life and living in the same kinds of environments, the fossilized traces of the latter serve as useful proxies for understanding the potential distribution of martian chemotrophs and their fossilized traces. Thus, comparison with analog, anaerobic, volcanic terrestrial environments (Early Archean >3.5–3.33 Ga) shows that the fossil remains of chemotrophs in such environments were common, although sparsely distributed, except in the vicinity of hydrothermal activity where nutrients were readily available. Moreover, the traces of these kinds of microorganisms can be well preserved, provided that they are rapidly mineralized and that the sediments in which they occur are rapidly cemented. We evaluate the biogenicity of these signatures by comparing them to possible abiotic features. Finally, we discuss the implications of different scenarios for life on Mars for detection by in situ exploration, ranging from its non-appearance, through preserved traces of life, to the presence of living microorganisms. Key Words: Mars—Early Earth—Anaerobic chemotrophs—Biosignatures—Astrobiology missions to Mars. Astrobiology 15, 998–1029.
PMCID: PMC4653824  PMID: 26575218
2.  Reduction of the Temperature Sensitivity of Halomonas hydrothermalis by Iron Starvation Combined with Microaerobic Conditions 
The limits to biological processes on Earth are determined by physicochemical parameters, such as extremes of temperature and low water availability. Research into microbial extremophiles has enhanced our understanding of the biophysical boundaries which define the biosphere. However, there remains a paucity of information on the degree to which rates of microbial multiplication within extreme environments are determined by the availability of specific chemical elements. Here, we show that iron availability and the composition of the gaseous phase (aerobic versus microaerobic) determine the susceptibility of a marine bacterium, Halomonas hydrothermalis, to suboptimal and elevated temperature and salinity by impacting rates of cell division (but not viability). In particular, iron starvation combined with microaerobic conditions (5% [vol/vol] O2, 10% [vol/vol] CO2, reduced pH) reduced sensitivity to temperature across the 13°C range tested. These data demonstrate that nutrient limitation interacts with physicochemical parameters to determine biological permissiveness for extreme environments. The interplay between resource availability and stress tolerance, therefore, may shape the distribution and ecology of microorganisms within Earth's biosphere.
PMCID: PMC4345356  PMID: 25595757
3.  An Estimate of the Total DNA in the Biosphere 
PLoS Biology  2015;13(6):e1002168.
Modern whole-organism genome analysis, in combination with biomass estimates, allows us to estimate a lower bound on the total information content in the biosphere: 5.3 × 1031 (±3.6 × 1031) megabases (Mb) of DNA. Given conservative estimates regarding DNA transcription rates, this information content suggests biosphere processing speeds exceeding yottaNOPS values (1024 Nucleotide Operations Per Second). Although prokaryotes evolved at least 3 billion years before plants and animals, we find that the information content of prokaryotes is similar to plants and animals at the present day. This information-based approach offers a new way to quantify anthropogenic and natural processes in the biosphere and its information diversity over time.
The diversity of life on Earth is typically considered in terms of the total number of species. However, this essay, by estimating the total amount of DNA in the biosphere at 5.4 x 1031 megabases, offers an information-based view of biodiversity.
PMCID: PMC4466264  PMID: 26066900
4.  Nonphotosynthetic Pigments as Potential Biosignatures 
Astrobiology  2015;15(5):341-361.
Previous work on possible surface reflectance biosignatures for Earth-like planets has typically focused on analogues to spectral features produced by photosynthetic organisms on Earth, such as the vegetation red edge. Although oxygenic photosynthesis, facilitated by pigments evolved to capture photons, is the dominant metabolism on our planet, pigmentation has evolved for multiple purposes to adapt organisms to their environment. We present an interdisciplinary study of the diversity and detectability of nonphotosynthetic pigments as biosignatures, which includes a description of environments that host nonphotosynthetic biologically pigmented surfaces, and a lab-based experimental analysis of the spectral and broadband color diversity of pigmented organisms on Earth. We test the utility of broadband color to distinguish between Earth-like planets with significant coverage of nonphotosynthetic pigments and those with photosynthetic or nonbiological surfaces, using both 1-D and 3-D spectral models. We demonstrate that, given sufficient surface coverage, nonphotosynthetic pigments could significantly impact the disk-averaged spectrum of a planet. However, we find that due to the possible diversity of organisms and environments, and the confounding effects of the atmosphere and clouds, determination of substantial coverage by biologically produced pigments would be difficult with broadband colors alone and would likely require spectrally resolved data. Key Words: Biosignatures—Exoplanets—Halophiles—Pigmentation—Reflectance spectroscopy—Spectral models. Astrobiology 15, 341–361.
PMCID: PMC4442567  PMID: 25941875
5.  Habitable worlds with no signs of life 
‘Most habitable worlds in the cosmos will have no remotely detectable signs of life’ is proposed as a biological hypothesis to be tested in the study of exoplanets. Habitable planets could be discovered elsewhere in the Universe, yet there are many hypothetical scenarios whereby the search for life on them could yield negative results. Scenarios for habitable worlds with no remotely detectable signatures of life include: planets that are habitable, but have no biosphere (Uninhabited Habitable Worlds); planets with life, but lacking any detectable surface signatures of that life (laboratory examples are provided); and planets with life, where the concentrations of atmospheric gases produced or removed by biota are impossible to disentangle from abiotic processes because of the lack of detailed knowledge of planetary conditions (the ‘problem of exoplanet thermodynamic uncertainty’). A rejection of the hypothesis would require that the origin of life usually occurs on habitable planets, that spectrally detectable pigments and/or metabolisms that produce unequivocal biosignature gases (e.g. oxygenic photosynthesis) usually evolve and that the organisms that harbour them usually achieve a sufficient biomass to produce biosignatures detectable to alien astronomers.
PMCID: PMC3982426  PMID: 24664917
habitability; exoplanets; life; biosignatures; microorganisms
6.  Archaea in Past and Present Geobiochemical Processes and Elemental Cycles 
Archaea  2013;2013:930493.
PMCID: PMC3697276  PMID: 23843726
7.  Exposure of phototrophs to 548 days in low Earth orbit: microbial selection pressures in outer space and on early earth 
The ISME Journal  2011;5(10):1671-1682.
An epilithic microbial community was launched into low Earth orbit, and exposed to conditions in outer space for 548 days on the European Space Agency EXPOSE-E facility outside the International Space Station. The natural phototroph biofilm was augmented with akinetes of Anabaena cylindrica and vegetative cells of Nostoc commune and Chroococcidiopsis. In space-exposed dark controls, two algae (Chlorella and Rosenvingiella spp.), a cyanobacterium (Gloeocapsa sp.) and two bacteria associated with the natural community survived. Of the augmented organisms, cells of A. cylindrica and Chroococcidiopsis survived, but no cells of N. commune. Only cells of Chroococcidiopsis were cultured from samples exposed to the unattenuated extraterrestrial ultraviolet (UV) spectrum (>110 nm or 200 nm). Raman spectroscopy and bright-field microscopy showed that under these conditions the surface cells were bleached and their carotenoids were destroyed, although cell morphology was preserved. These experiments demonstrate that outer space can act as a selection pressure on the composition of microbial communities. The results obtained from samples exposed to >200 nm UV (simulating the putative worst-case UV exposure on the early Earth) demonstrate the potential for epilithic colonization of land masses during that time, but that UV radiation on anoxic planets can act as a strong selection pressure on surface-dwelling organisms. Finally, these experiments have yielded new phototrophic organisms of potential use in biomass and oxygen production in space exploration.
PMCID: PMC3176519  PMID: 21593797
algae; bacteria; cyanobacteria; epilith; low Earth orbit; space exploration
9.  Isolation of Novel Extreme-Tolerant Cyanobacteria from a Rock-Dwelling Microbial Community by Using Exposure to Low Earth Orbit▿ † 
Many cyanobacteria are known to tolerate environmental extremes. Motivated by an interest in selecting cyanobacteria for applications in space, we launched rocks from a limestone cliff in Beer, Devon, United Kingdom, containing an epilithic and endolithic rock-dwelling community of cyanobacteria into low Earth orbit (LEO) at a height of approximately 300 kilometers. The community was exposed for 10 days to isolate cyanobacteria that can survive exposure to the extreme radiation and desiccating conditions associated with space. Culture-independent (16S rRNA) and culture-dependent methods showed that the cyanobacterial community was composed of Pleurocapsales, Oscillatoriales, and Chroococcales. A single cyanobacterium, a previously uncharacterized extremophile, was isolated after exposure to LEO. We were able to isolate the cyanobacterium from the limestone cliff after exposing the rock-dwelling community to desiccation and vacuum (0.7 × 10−3 kPa) in the laboratory. The ability of the organism to survive the conditions in space may be linked to the formation of dense colonies. These experiments show how extreme environmental conditions, including space, can be used to select for novel microorganisms. Furthermore, it improves our knowledge of environmental tolerances of extremophilic rock-dwelling cyanobacteria.
PMCID: PMC2849240  PMID: 20154120
10.  The evolution of inorganic carbon concentrating mechanisms in photosynthesis 
Inorganic carbon concentrating mechanisms (CCMs) catalyse the accumulation of CO2 around rubisco in all cyanobacteria, most algae and aquatic plants and in C4 and crassulacean acid metabolism (CAM) vascular plants. CCMs are polyphyletic (more than one evolutionary origin) and involve active transport of HCO3−, CO2 and/or H+, or an energized biochemical mechanism as in C4 and CAM plants. While the CCM in almost all C4 plants and many CAM plants is constitutive, many CCMs show acclimatory responses to variations in the supply of not only CO2 but also photosynthetically active radiation, nitrogen, phosphorus and iron. The evolution of CCMs is generally considered in the context of decreased CO2 availability, with only a secondary role for increasing O2. However, the earliest CCMs may have evolved in oxygenic cyanobacteria before the atmosphere became oxygenated in stromatolites with diffusion barriers around the cells related to UV screening. This would decrease CO2 availability to cells and increase the O2 concentration within them, inhibiting rubisco and generating reactive oxygen species, including O3.
PMCID: PMC2606764  PMID: 18487130
alga; cyanobacteria; crassulacean acid metabolism; C4 photosynthesis; embryophytes; stromatolites
11.  Implications of a 3.472–3.333 Gyr-old subaerial microbial mat from the Barberton greenstone belt, South Africa for the UV environmental conditions on the early Earth 
Modelling suggests that the UV radiation environment of the early Earth, with DNA weighted irradiances of about three orders of magnitude greater than those at present, was hostile to life forms at the surface, unless they lived in specific protected habitats. However, we present empirical evidence that challenges this commonly held view. We describe a well-developed microbial mat that formed on the surface of volcanic littoral sediments in an evaporitic environment in a 3.5–3.3 Ga-old formation from the Barberton greenstone belt. Using a multiscale, multidisciplinary approach designed to strongly test the biogenicity of potential microbial structures, we show that the mat was constructed under flowing water by 0.25 μm filaments that produced copious quantities of extracellular polymeric substances, representing probably anoxygenic photosynthesizers. Associated with the mat is a small colony of rods–vibroids that probably represent sulphur-reducing bacteria. An embedded suite of evaporite minerals and desiccation cracks in the surface of the mat demonstrates that it was periodically exposed to the air in an evaporitic environment. We conclude that DNA-damaging UV radiation fluxes at the surface of the Earth at this period must either have been low (absorbed by CO2, H2O, a thin organic haze from photo-dissociated CH4, or SO2 from volcanic outgassing; scattered by volcanic, and periodically, meteorite dust, as well as by the upper layers of the microbial mat) and/or that the micro-organisms exhibited efficient gene repair/survival strategies.
PMCID: PMC1664690  PMID: 17008224
Early Mid Archaean; Barberton; microfossils; littoral zone; UV environment
12.  The origin and emergence of life under impact bombardment 
Craters formed by asteroids and comets offer a number of possibilities as sites for prebiotic chemistry, and they invite a literal application of Darwin's ‘warm little pond’. Some of these attributes, such as prolonged circulation of heated water, are found in deep-ocean hydrothermal vent systems, previously proposed as sites for prebiotic chemistry. However, impact craters host important characteristics in a single location, which include the formation of diverse metal sulphides, clays and zeolites as secondary hydrothermal minerals (which can act as templates or catalysts for prebiotic syntheses), fracturing of rock during impact (creating a large surface area for reactions), the delivery of iron in the case of the impact of iron-containing meteorites (which might itself act as a substrate for prebiotic reactions), diverse impact energies resulting in different rates of hydrothermal cooling and thus organic syntheses, and the indiscriminate nature of impacts into every available lithology—generating large numbers of ‘experiments’ in the origin of life. Following the evolution of life, craters provide cryptoendolithic and chasmoendolithic habitats, particularly in non-sedimentary lithologies, where limited pore space would otherwise restrict colonization. In impact melt sheets, shattered, mixed rocks ultimately provided diverse geochemical gradients, which in present-day craters support the growth of microbial communities.
PMCID: PMC1664688  PMID: 17008223
organics; colonization; thermophiles; asteroid; crater
14.  Antarctic Genomics 
With the development of genomic science and its battery of technologies, polar biology stands on the threshold of a revolution, one that will enable the investigation of important questions of unprecedented scope and with extraordinary depth and precision. The exotic organisms of polar ecosystems are ideal candidates for genomic analysis. Through such analyses, it will be possible to learn not only the novel features that enable polar organisms to survive, and indeed thrive, in their extreme environments, but also fundamental biological principles that are common to most, if not all, organisms. This article aims to review recent developments in Antarctic genomics and to demonstrate the global context of such studies.
PMCID: PMC2447445  PMID: 18629155

Results 1-14 (14)