Transitory microbial habitat in the hyperarid Atacama Desert

Author:

Schulze-Makuch Dirk,Wagner Dirk,Kounaves Samuel P.ORCID,Mangelsdorf Kai,Devine Kevin G.,de Vera Jean-Pierre,Schmitt-Kopplin PhilippeORCID,Grossart Hans-PeterORCID,Parro Victor,Kaupenjohann Martin,Galy Albert,Schneider Beate,Airo Alessandro,Frösler Jan,Davila Alfonso F.,Arens Felix L.,Cáceres Luis,Cornejo Francisco Solís,Carrizo Daniel,Dartnell Lewis,DiRuggiero Jocelyne,Flury MarkusORCID,Ganzert Lars,Gessner Mark O.,Grathwohl Peter,Guan Lisa,Heinz Jacob,Hess Matthias,Keppler Frank,Maus Deborah,McKay Christopher P.,Meckenstock Rainer U.,Montgomery Wren,Oberlin Elizabeth A.,Probst Alexander J.,Sáenz Johan S.,Sattler Tobias,Schirmack Janosch,Sephton Mark A.,Schloter Michael,Uhl Jenny,Valenzuela Bernardita,Vestergaard Gisle,Wörmer Lars,Zamorano Pedro

Abstract

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.

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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