The Atacama Desert, northern Chile, is one of the driest deserts on Earth and, as such, a natural laboratory to explore the limits of life and the strategies evolved by microorganisms to adapt to extreme environments. Here we report the exceptional adaptation strategies of chlorophototrophic and eukaryotic algae, and chlorophototrophic and prokaryotic cyanobacteria to the hyperarid and extremely high solar radiation conditions occurring in this desert. Our approach combined several microscopy techniques, spectroscopic analytical methods, and molecular analyses. We found that the major adaptation strategy was to avoid the extreme environmental conditions by colonizing cryptoendolithic, as well as, hypoendolithic habitats within gypsum deposits. The cryptoendolithic colonization occurred a few millimeters beneath the gypsum surface and showed a succession of organized horizons of algae and cyanobacteria, which has never been reported for endolithic microbial communities. The presence of cyanobacteria beneath the algal layer, in close contact with sepiolite inclusions, and their hypoendolithic colonization suggest that occasional liquid water might persist within these sub-microhabitats. We also identified the presence of abundant carotenoids in the upper cryptoendolithic algal habitat and scytonemin in the cyanobacteria hypoendolithic habitat. This study illustrates that successful lithobiontic microbial colonization at the limit for microbial life is the result of a combination of adaptive strategies to avoid excess solar irradiance and extreme evapotranspiration rates, taking advantage of the complex structural and mineralogical characteristics of gypsum deposits—conceptually called “rock's habitable architecture.” Additionally, self-protection by synthesis and accumulation of secondary metabolites likely produces a shielding effect that prevents photoinhibition and lethal photooxidative damage to the chlorophototrophs, representing another level of adaptation.
The hyper-arid core of the Atacama Desert (Chile) is the driest place on Earth and is considered a close analogue to the extremely arid conditions on the surface of Mars. Microbial life is very rare in soils of this hyper-arid region, and autotrophic microorganisms are virtually absent. Instead, photosynthetic micro-organisms have successfully colonized the interior of halite crusts, which are widespread in the Atacama Desert. These endoevaporitic colonies are an example of life that has adapted to the extreme dryness by colonizing the interior of rocks that provide enhanced moisture conditions. As such, these colonies represent a novel example of potential life on Mars. Here, we present non-destructive Raman spectroscopical identification of these colonies and their organic remnants. Spectral signatures revealed the presence of UV-protective biomolecules as well as light-harvesting pigments pointing to photosynthetic activity. Compounds of biogenic origin identified within these rocks differed depending on the origins of specimens from particular areas in the desert, with differing environmental conditions. Our results also demonstrate the capability of Raman spectroscopy to identify biomarkers within rocks that have a strong astrobiological potential.
Raman spectral signatures have been obtained for a series of organic minerals using a compact portable Raman instrument equipped with 785-nm laser excitation. Well-resolved Raman spectra of crystalline salts of carboxylic acids, whewellite and mellite, as well as of the aromatic mineral idrialite were recorded. For comparative purposes, an amorphous fossil resin, baltic amber, was also investigated. The results obtained confirm that portable Raman instruments can be considered as excellent tools for field geological applications, including the detection of organic minerals in the frame of outcrops of sedimentary rocks or coal beds. Organic minerals can be added to the list of established biomarkers, including porphyrins, hydrocarbons and organic acids, which are important for the study with regard to future exobiological missions such as the ESA ExoMars mission to detect the presence of extinct or extant life on Mars.
Scytonemin, a UV-screening molecule produced by certain Cyanobacteria to protect against harmful UV radiation, was studied in endolithic cyanobacterial colonies in the halite crust from one of the driest places on Earth - the hyperarid zone of the Atacama Desert. The distribution of the pigment within the evaporitic crust was studied in detail by various independent analytical methods: Raman spectroscopy (including Raman imaging); advanced microscopic observations (fluorescence microscopy, confocal laser scanning microscopy, low-temperature scanning electron microscopy); and spectrophotometric analyses. The differences in scytonemin biosynthesis were mapped within the colonized interior layers, which can be divided into scytonemin-rich and scytonemin-poor zones. A 532 nm laser for excitation proved to be an ideal excitation source with which to observe the relative content of scytonemin within a particular cell aggregate, as well as between different cell aggregates; based on the scytonemin/carotenoid Raman signal intensity ratio of selected corroborative bands for these two compounds. Significantly, scytonemin was found to accumulate within a decayed biomass in the surface portions of the halite crust. These were found to be highly enriched in both the absolute scytonemin content (as documented by UV/VIS spectrophotometry) and its content relative to other pigments associated with the cyanobacterial cells (e.g. carotenoids and chlorophyll).
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