Radiolytic Degradation of Soil Carbon from the Mojave Desert by 60Co Gamma Rays: Implications for the Survival of Martian Organic Compounds Due to Cosmic Radiation.

The martian surface has been continuously exposed to galactic cosmic radiation. Since organic compounds are degraded by ionizing radiation, knowledge of their decay constants is fundamental to predicting their stability on the martian surface. In this study, we report the radiolysis constant for the destruction of soil organic compounds at a starting concentration of ∼2011 µg C/gsoil from the Mojave Desert. The soils were exposed to gamma irradiation with absorbed doses of up to 19 MGy at room temperature, representing ∼250 million years of exposure to galactic cosmic rays. The destruction of total soil organic carbon and the formation of gases were investigated by a sequential on-line analytical array coupled to gas chromatography-mass spectrometry. Soil inorganic and organic carbon were degraded exponentially with a radiolysis constant 0.3 MGy-1(30%) producing mostly carbon dioxide (93.2%), carbon monoxide (6.2%), and methane (0.6%). Using the dose rate measured by the Radiation Assessment Detector on board the Curiosity rover, we make predictions on the survival of organic compounds in the cold martian subsurface. It is estimated that soil organic compounds with initial concentrations as those found today at the Mojave Desert would have been destroyed to levels <1 ppb at 0.1 m in depth in ∼2000 Myr. Pristine organic compounds are expected to be present at a depth of ∼1.5 m. These results are relevant for the search of organic compounds in past, present, and future missions to Mars. In particular, we predict that the upcoming ExoMars will encounter pristine organic compounds at this depth.

Transitory microbial habitat in the hyperarid Atacama Desert.

Traces of life are nearly ubiquitous on Earth. However, a central unresolved question is whether these traces always indicate an active microbial community or whether, in extreme environments, such as hyperarid deserts, they instead reflect just dormant or dead cells. Although microbial biomass and diversity decrease with increasing aridity in the Atacama Desert, we provide multiple lines of evidence for the presence of an at times metabolically active, microbial community in one of the driest places on Earth. We base this observation on four major lines of evidence: (i) a physico-chemical characterization of the soil habitability after an exceptional rain event, (ii) identified biomolecules indicative of potentially active cells [e.g., presence of ATP, phospholipid fatty acids (PLFAs), metabolites, and enzymatic activity], (iii) measurements of in situ replication rates of genomes of uncultivated bacteria reconstructed from selected samples, and (iv) microbial community patterns specific to soil parameters and depths. We infer that the microbial populations have undergone selection and adaptation in response to their specific soil microenvironment and in particular to the degree of aridity. Collectively, our results highlight that even the hyperarid Atacama Desert can provide a habitable environment for microorganisms that allows them to become metabolically active following an episodic increase in moisture and that once it decreases, so does the activity of the microbiota. These results have implications for the prospect of life on other planets such as Mars, which has transitioned from an earlier wetter environment to today's extreme hyperaridity.

Cyanobacteria and chloroflexi-dominated hypolithic colonization of quartz at the hyper-arid core of the Atacama Desert, Chile.

Quartz stones are ubiquitous in deserts and are a substrate for hypoliths, microbial colonists of the underside of such stones. These hypoliths thrive where extreme temperature and moisture stress limit the occurrence of higher plant and animal life. Several studies have reported the occurrence of green hypolithic colonization dominated by cyanobacteria. Here, we describe a novel red hypolithic colonization from Yungay, at the hyper-arid core of the Atacama Desert in Chile. Comparative analysis of green and red hypoliths from this site revealed markedly different microbial community structure as revealed by 16S rRNA gene clone libraries. Green hypoliths were dominated by cyanobacteria (Chroococcidiopsis and Nostocales phylotypes), whilst the red hypolith was dominated by a taxonomically diverse group of chloroflexi. Heterotrophic phylotypes common to all hypoliths were affiliated largely to desiccation-tolerant taxa within the Actinobacteria and Deinococci. Alphaproteobacterial phylotypes that affiliated with nitrogen-fixing taxa were unique to green hypoliths, whilst Gemmatimonadetes phylotypes occurred only on red hypolithon. Other heterotrophic phyla recovered with very low frequency were assumed to represent functionally relatively unimportant taxa.

Hypolithic cyanobacteria supported mainly by fog in the coastal range of the Atacama Desert.

The Atacama Desert is one of the driest places on Earth, with an arid core highly adverse to the development of hypolithic cyanobacteria. Previous work has shown that when rain levels fall below ~1 mm per year, colonization of suitable quartz stones falls to virtually zero. Here, we report that along the coast in these arid regions, complex associations of cyanobacteria, archaea, and heterotrophic bacteria inhabit the undersides of translucent quartz stones. Colonization rates in these areas, which receive virtually no rain but mainly fog, are significantly higher than those reported inland in the hyperarid zone at the same latitude. Here, hypolithic colonization rates can be up to 80%, with all quartz rocks over 20 g being colonized. This finding strongly suggests that hypolithic microbial communities thriving in the seaward face of the Coastal Range can survive with fog as the main regular source of moisture. A model is advanced where the development of the hypolithic communities under quartz stones relies on a positive feedback between fog availability and the higher thermal conductivity of the quartz rocks, which results in lower daytime temperatures at the quartz-soil interface microenvironment.

Characterization of organics, microorganisms, desert soils, and Mars-like soils by thermal volatilization coupled to mass spectrometry and their implications for the search for organics on Mars by Phoenix and future space missions.

A key goal for astrobiology is the search for evidence of life on Mars. Because liquid water is a fundamental environmental requirement for life, the recent set of missions to Mars have focused on a strategy known as "follow the water." Since life is made of organic molecules, a logical next step is "follow the organics." However, organics are expected to be present at very low levels on Mars, which would make their detection challenging. Viking was unable to detect organics at parts per billion (ppb), but the effective upper limit could be higher due to the low efficiency of the thermal volatilization (TV) step in releasing organics. Due to its ease of use, TV is still the method selected for current and future NASA and ESA missions. Here, we show that when organics are present in the soil at levels above 1500 parts per million (ppm), there are several characteristic organic fragments detected by TV-mass spectrometry; however, when the levels are below <150 ppm, TV oxidizes them, and no organic fragments are released. Instead, nitric oxide (NO) is produced and can be used to determine quantitatively the organic content if the C/N ratio is determined. Any atmospheric NO sorbed or mineral nitrogen (e.g., nitrates) present in the soil would release NO by TV at distinctive temperature regimes that would not overlap with the organic nitrogen source. Therefore, we suggest that monitoring NO provides the best chance for Phoenix and other future Mars missions to detect nitrogen-containing organics in the soil or ice.

Deinococcus peraridilitoris sp. nov., isolated from a coastal desert.

Three ionizing-radiation-resistant bacterial strains (designated KR-196, KR-198 and KR-200(T)) were isolated from a sample of arid soil collected from a coastal desert in Chile. The soil sample was irradiated before serial dilution plating was performed using one-tenth-strength plate count agar. Phylogenetic analysis of the 16S rRNA gene sequences showed these organisms to represent a novel species of the genus Deinococcus, having sequence similarities of 87.3-90.8 % with respect to recognized Deinococcus species. Strains KR-196, KR-198 and KR-200(T) were aerobic and showed optimum growth at 30 degrees C and pH 6.5-8.0. The major respiratory menaquinone was MK-8. The predominant fatty acids in these strains were 16 : 1 omega 7c, 16 : 0, 15 : 1 omega 6c, 17 : 0 and 18 : 0. The DNA G+C content of strain KR-200(T) was 63.9 mol%. Strains KR-196, KR-198 and KR-200(T) were found to be resistant to >10 kGy gamma radiation. On the basis of the phylogenetic, chemotaxonomic and phenotypic data, strain KR-200(T) represents a novel species of the genus Deinococcus, for which the name Deinococcus peraridilitoris sp. nov. is proposed. The type strain is KR-200(T) (=LMG 22246(T)=CIP 109416(T)).

The limitations on organic detection in Mars-like soils by thermal volatilization-gas chromatography-MS and their implications for the Viking results.

The failure of Viking Lander thermal volatilization (TV) (without or with thermal degradation)-gas chromatography (GC)-MS experiments to detect organics suggests chemical rather than biological interpretations for the reactivity of the martian soil. Here, we report that TV-GC-MS may be blind to low levels of organics on Mars. A comparison between TV-GC-MS and total organics has been conducted for a variety of Mars analog soils. In the Antarctic Dry Valleys and the Atacama and Libyan Deserts we find 10-90 mug of refractory or graphitic carbon per gram of soil, which would have been undetectable by the Viking TV-GC-MS. In iron-containing soils (jarosites from Rio Tinto and Panoche Valley) and the Mars simulant (palogonite), oxidation of the organic material to carbon dioxide (CO(2)) by iron oxides and/or their salts drastically attenuates the detection of organics. The release of 50-700 ppm of CO(2) by TV-GC-MS in the Viking analysis may indicate that an oxidation of organic material took place. Therefore, the martian surface could have several orders of magnitude more organics than the stated Viking detection limit. Because of the simplicity of sample handling, TV-GC-MS is still considered the standard method for organic detection on future Mars missions. We suggest that the design of future organic instruments for Mars should include other methods to be able to detect extinct and/or extant life.

A preliminary survey of non-lichenized fungi cultured from the hyperarid Atacama Desert of Chile.

The Atacama Desert is one of the driest environments on Earth, and has been so for over 200,000 years. Previous reports have suggested that surprisingly low numbers of culturable bacteria, counted as biomass or species diversity, are present in Atacama sands collected from the most hyperarid regions. In previous studies, the presence of eukaryotic organisms was not discussed. In this report, we describe a method of direct plating onto rich media that resulted in culturing a range of fungi from Atacama samples. All fungi identified in this preliminary survey are spore-forming saprobes that are readily dispersed by wind, a likely mechanism that accounts for their presence in the central Atacama Desert.

Hypolithic cyanobacteria, dry limit of photosynthesis, and microbial ecology in the hyperarid Atacama Desert.

The occurrence of hypolithic cyanobacteria colonizing translucent stones was quantified along the aridity gradient in the Atacama Desert in Chile, from less arid areas to the hyperarid core where photosynthetic life and thus primary production reach their limits. As mean rainfall declines from 21 to

Endolithic cyanobacteria in halite rocks from the hyperarid core of the Atacama Desert.

In the driest parts of the Atacama Desert there are no visible life forms on soil or rock surfaces. The soil in this region contains only minute traces of bacteria distributed in patches, and conditions are too dry for cyanobacteria that live under translucent stones. Here we show that halite evaporite rocks from the driest part of the Atacama Desert are colonized by cyanobacteria. This colonization takes place just a few millimeters beneath the rock surface, occupying spaces among salt crystals. Our work reveals that these communities are composed of extremely resistant Chroococcidiopsis morphospecies of cyanobacteria and associated heterotrophic bacteria. This newly discovered endolithic environment is an extremely dry and, at the same time, saline microbial habitat. Photosynthetic microorganisms within dry evaporite rocks could be an important and previously unrecognized target for the search for life within our Solar System.

Mars-like soils in the Atacama Desert, Chile, and the dry limit of microbial life.

The Viking missions showed the martian soil to be lifeless and depleted in organic material and indicated the presence of one or more reactive oxidants. Here we report the presence of Mars-like soils in the extreme arid region of the Atacama Desert. Samples from this region had organic species only at trace levels and extremely low levels of culturable bacteria. Two samples from the extreme arid region were tested for DNA and none was recovered. Incubation experiments, patterned after the Viking labeled-release experiment but with separate biological and nonbiological isomers, show active decomposition of organic species in these soils by nonbiological processes.

Temperature and moisture conditions for life in the extreme arid region of the Atacama desert: four years of observations including the El Niño of 1997-1998.

The Atacama along the Pacific Coast of Chile and Peru is one of the driest and possibly oldest deserts in the world. It represents an extreme habitat for life on Earth and is an analog for life in dry conditions on Mars. We report on four years (September 1994-October 1998) of climate and moisture data from the extreme arid region of the Atacama. Our data are focused on understanding moisture sources and their role in creating suitable environments for photosynthetic microorganisms in the desert surface. The average air temperature was 16.5 degrees C and 16.6 degrees C in 1995 and 1996, respectively. The maximum air temperature recorded was 37.9 degrees C, and the minimum was -5.7 degrees C. Annual average sunlight was 336 and 335 W m(-2) in 1995 and 1996, respectively. Winds averaged a few meters per second, with strong föhn winds coming from the west exceeding 12 m s(-1). During our 4 years of observation there was only one significant rain event of 2.3 mm, which occurred near midnight local time. We suggest that this event was a rainout of a heavy fog. It is of interest that the strong El Niño of 1997-1998 brought heavy rainfall to the deserts of Peru, but did not bring significant rain to the central Atacama in Chile. Dew occurred at our station frequently following high nighttime relative humidity, but is not a significant source of moisture in the soil or under stones. Groundwater also does not contribute to surface moisture. Only the one rain event of 2.3 mm resulted in liquid water in the soil and beneath stones for a total of only 65-85 h over 4 years. The paucity of liquid water under stones is consistent with the apparent absence of hypolithic (under-stone) cyanobacteria, the only known primary producers in such extreme deserts.