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.

Biology Department The Johns Hopkins University Baltimore MD USA

Carl Sagan Center SETI Institute Mountain View CA USA

Departamento Biología Vegetal Ecología y Ciencias de la Tierra Universidad de Extremadura Plasencia Spain

Department of Botany Charles University Prague Czech Republic

Facultad de Ciencias Experimentales Universidad de Huelva Huelva Spain

Instituto de Ciencias Agrarias CSIC Madrid Spain

Laboratory of Ecological Plant Physiology Global Change Research Centre AS CR Brno Czech Republic ; Institute of Geochemistry Mineralogy and Mineral Resources Charles University Prague Czech Republic

Museo Nacional de Ciencias Naturales CSIC Madrid Spain

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Carotenoids dispersed in gypsum rock as a result of algae adaptation to the extreme conditions of the Atacama Desert

Microbial colonization of gypsum: from the fossil record to the present day

Comparative analysis of cyanobacterial communities in gypsum outcrops: insights from sites in Israel and Poland

Gypsum endolithic phototrophs under moderate climate (Southern Sicily): their diversity and pigment composition

Crystalline water in gypsum is unavailable for cyanobacteria in laboratory experiments and in natural desert endolithic habitats

Discovery of carotenoid red-shift in endolithic cyanobacteria from the Atacama Desert