Transitory microbial habitat in the hyperarid Atacama Desert

Dirk Schulze-Makuch, Dirk Wagner, Samuel P. Kounaves, Kai Mangelsdorf, Kevin G. Devine, Jean-Pierre de Vera, Philippe Schmitt-Kopplin, Hans-Peter Grossart, Victor Parro, Martin Kaupenjohann, Albert Galy, Beate Schneider, Alessandro Airo, Jan Frösler, Alfonso F. Davila, Felix L. Arens, Luis Cáceres, Francisco Solís Cornejo, Daniel Carrizo, Lewis Dartnell, Jocelyne DiRuggiero, Markus Flury, Lars Ganzert, Mark O. Gessner, Peter Grathwohl, Lisa Guan, Jacob Heinz, Matthias Hess, Frank Keppler, Deborah Maus, Christopher P. McKay, Rainer U. Meckenstock, Wren Montgomery, Elizabeth A. Oberlin, Alexander J. Probst, Johan S. Sáenz, Tobias Sattler, Janosch Schirmack, Mark A. Sephton, Michael Schloter, Jenny Uhl, Bernardita Valenzuela, Gisle Vestergaard, Lars Wörmer, and Pedro Zamorano. 2018. Transitory microbial habitat in the hyperarid Atacama Desert. Proceedings of the National Academy of Sciences of the United States of America 115, 11, 2670-2675 DOI: 10.1073/pnas.1714341115

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.

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