Beate Schneider, Markus Flury, Peter Grathwohl, Rainer U. Meckenstock, Jenny Uhl, Samuel P. Kounaves, Alexander J. Probst, Felix L. Arens, Tobias Sattler, Matthias Hess, Wren Montgomery, Daniel Carrizo, Francisco Solís Cornejo, Mark A. Sephton, Lars Wörmer, Johan S. Saenz, Lisa Guan, Janosch Schirmack, Bernardita Valenzuela, Jacob Heinz, Gisle Vestergaard, Elizabeth Oberlin, Alfonso F. Davila, Philippe Schmitt-Kopplin, Hans-Peter Grossart, Jocelyne DiRuggiero, Martin Kaupenjohann, Christopher P. McKay, Frank Keppler, Kevin G. Devine, Victor Parro, Kai Mangelsdorf, Jan Frösler, Lars Ganzert, Dirk Schulze-Makuch, Mark O. Gessner, Dirk Wagner, Jean-Pierre de Vera, Michael Schloter, Deborah Maus, Luis Cáceres, Alessandro Airo, Pedro Zamorano, Albert Galy, Lewis Dartnell, Science and Technology Facilities Council (STFC), Zentrum für Astronomie und Astrophysik [Berlin] (ZAA), Technische Universität Berlin (TU), Washington State University (WSU), GeoForschungsZentrum - Helmholtz-Zentrum Potsdam (GFZ), Institute of Earth and Environmental Science [Potsdam], University of Potsdam, Tufts University [Medford], Department of Earth Science and Engineering [Imperial College London], Imperial College London, London Metropolitan University, DLR Institut für Planetenforschung, Deutsches Zentrum für Luft- und Raumfahrt [Berlin] (DLR), Technische Universität Munchen - Université Technique de Munich [Munich, Allemagne] (TUM), Helmholtz-Zentrum München (HZM), Leibniz-Institut für Gewässerökologie und Binnenfischerei (IGB), Leibniz Association, Institut fur Biochemie und Biologie, Molekularbiologie (UP), Universität Potsdam, Instituto Nacional de Técnica Aeroespacial (INTA), Centre de Recherches Pétrographiques et Géochimiques (CRPG), Institut national des sciences de l'Univers (INSU - CNRS)-Université de Lorraine (UL)-Centre National de la Recherche Scientifique (CNRS), Universität Duisburg-Essen [Essen], NASA Ames Research Center (ARC), Institute of Geological Sciences [Berlin], Department of Earth Sciences [Berlin], Free University of Berlin (FU)-Free University of Berlin (FU), Universidad de Antofagasta, University of Westminster [London] (UOW), Johns Hopkins University (JHU), Center for Applied Geoscience [Tübingen] (ZAG), Eberhard Karls Universität Tübingen = Eberhard Karls University of Tuebingen, University of California [Davis] (UC Davis), University of California, Universität Heidelberg [Heidelberg], Center for Marine Environmental Sciences [Bremen] (MARUM), Universität Bremen, and Technische Universität München [München] (TUM)
Significance It has remained an unresolved question whether microorganisms recovered from the most arid environments on Earth are thriving under such extreme conditions or are just dead or dying vestiges of viable cells fortuitously deposited by atmospheric processes. Based on multiple lines of evidence, we show that indigenous microbial communities are present and temporally active even in the hyperarid soils of the Atacama Desert (Chile). Following extremely rare precipitation events in the driest parts of this desert, where rainfall often occurs only once per decade, we were able to detect episodic incidences of biological activity. Our findings expand the range of hyperarid environments temporarily habitable for terrestrial life, which by extension also applies to other planetary bodies like Mars., 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.