Microbial Hotspots in Lithic Microhabitats Inferred from DNA Fractionation and Metagenomics in the Atacama Desert

Schulze-Makuch, Dirk; Lipus, Daniel; Arens, Felix L.; Baqué, Mickael; Bornemann, Till L. V.; de Vera, Jean-Pierre; Flury, Markus; Frösler, Jan; Heinz, Jacob; Hwang, Yunha; Kounaves, Samuel P.; Mangelsdorf, Kai; Meckenstock, Rainer U.; Pannekens, Mark; Probst, Alexander J.; Sáenz, Johan S.; Schirmack, Janosch; Schloter, Michael; Schmitt-Kopplin, Philippe; Schneider, Beate; Uhl, Jenny; Vestergaard, Gisle; Valenzuela, Bernardita; Zamorano, Pedro; Wagner, Dirk

doi:10.3390/microorganisms9051038

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Microbial Hotspots in Lithic Microhabitats Inferred from DNA Fractionation and Metagenomics in the Atacama Desert

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Rainer U. Meckenstock

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Philippe Schmitt-Kopplin

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Beate Schneider

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Jenny Uhl

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Gisle Vestergaard

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Bernardita Valenzuela

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Pedro Zamorano

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Dirk Wagner

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Center for Astronomy and Astrophysics, Technische Universität Berlin, 10623 Berlin, Germany

GFZ German Research Centre for Geosciences, Section Geomicrobiology, Telegrafenberg, 14473 Potsdam, Germany

Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB), Department of Experimental Limnology, 16775 Stechlin, Germany

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School of the Environment, Washington State University, Pullman, WA 99163, USA

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German Aerospace Center (DLR), Institute of Planetary Research, 12489 Berlin, Germany

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Environmental Microbiology and Biotechnology, Department of Chemistry, University of Duisburg-Essen, 45141 Essen, Germany

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German Aerospace Center (DLR), Microgravity User Support Center (MUSC), 51147 Cologne, Germany

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Department of Crop and Soil Science, Washington State University, Pullman, WA 99164, USA

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Department of Crop and Soil Science, Washington State University, Puyallup, WA 98371, USA

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Department of Chemistry, Tufts University, Boston, MA 02155, USA

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Department of Earth Science & Engineering, Imperial College London, London SW7 2AZ, UK

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GFZ German Research Centre for Geosciences, Section Organic Geochemistry, 14473 Potsdam, Germany

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Research Unit for Comparative Microbiome Analysis, Helmholtz Zentrum München, Ingolstädter Landstr. 1, 85764 Neuherberg, Germany

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Research Unit Analytical BioGeoChemistry, Helmholtz Zentrum München, Ingolstädter Landstr. 1, 85764 Neuherberg, Germany

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Federal Institute for Materials Research and Testing (BAM), 12205 Berlin, Germany

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Department of Health Technology, Technical University of Denmark, 2800 Lyngby, Denmark

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Laboratorio de Microorganismos Extremófilos, Instituto Antofagasta, Universidad de Antofagasta, Av. Angamos 601, Antofagasta 1240000, Chile

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Institute of Geosciences, University of Potsdam, Karl-Liebknecht-Str. 24-25, 14476 Potsdam, Germany

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Academic Editors: Annarita Poli and Paola Di Donato

Microorganisms 2021, 9(5), 1038; https://doi.org/10.3390/microorganisms9051038

Received: 30 March 2021 / Revised: 29 April 2021 / Accepted: 5 May 2021 / Published: 12 May 2021

(This article belongs to the Special Issue Astrobiology and Microorganisms: Life to the Extreme, on Earth and Beyond)

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Abstract

The existence of microbial activity hotspots in temperate regions of Earth is driven by soil heterogeneities, especially the temporal and spatial availability of nutrients. Here we investigate whether microbial activity hotspots also exist in lithic microhabitats in one of the most arid regions of the world, the Atacama Desert in Chile. While previous studies evaluated the total DNA fraction to elucidate the microbial communities, we here for the first time use a DNA separation approach on lithic microhabitats, together with metagenomics and other analysis methods (i.e., ATP, PLFA, and metabolite analysis) to specifically gain insights on the living and potentially active microbial community. Our results show that hypolith colonized rocks are microbial hotspots in the desert environment. In contrast, our data do not support such a conclusion for gypsum crust and salt rock environments, because only limited microbial activity could be observed. The hypolith community is dominated by phototrophs, mostly Cyanobacteria and Chloroflexi, at both study sites. The gypsum crusts are dominated by methylotrophs and heterotrophic phototrophs, mostly Chloroflexi, and the salt rocks (halite nodules) by phototrophic and halotolerant endoliths, mostly Cyanobacteria and Archaea. The major environmental constraints in the organic-poor arid and hyperarid Atacama Desert are water availability and UV irradiation, allowing phototrophs and other extremophiles to play a key role in desert ecology. View Full-Text

Keywords: hyperarid; habitat; desert ecology; extremophile; endolith; hypolith

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Schulze-Makuch, D.; Lipus, D.; Arens, F.L.; Baqué, M.; Bornemann, T.L.V.; de Vera, J.-P.; Flury, M.; Frösler, J.; Heinz, J.; Hwang, Y.; Kounaves, S.P.; Mangelsdorf, K.; Meckenstock, R.U.; Pannekens, M.; Probst, A.J.; Sáenz, J.S.; Schirmack, J.; Schloter, M.; Schmitt-Kopplin, P.; Schneider, B.; Uhl, J.; Vestergaard, G.; Valenzuela, B.; Zamorano, P.; Wagner, D. Microbial Hotspots in Lithic Microhabitats Inferred from DNA Fractionation and Metagenomics in the Atacama Desert. Microorganisms 2021, 9, 1038. https://doi.org/10.3390/microorganisms9051038

AMA Style

Schulze-Makuch D, Lipus D, Arens FL, Baqué M, Bornemann TLV, de Vera J-P, Flury M, Frösler J, Heinz J, Hwang Y, Kounaves SP, Mangelsdorf K, Meckenstock RU, Pannekens M, Probst AJ, Sáenz JS, Schirmack J, Schloter M, Schmitt-Kopplin P, Schneider B, Uhl J, Vestergaard G, Valenzuela B, Zamorano P, Wagner D. Microbial Hotspots in Lithic Microhabitats Inferred from DNA Fractionation and Metagenomics in the Atacama Desert. Microorganisms. 2021; 9(5):1038. https://doi.org/10.3390/microorganisms9051038

Chicago/Turabian Style

Schulze-Makuch, Dirk, Daniel Lipus, Felix L. Arens, Mickael Baqué, Till L. V. Bornemann, Jean-Pierre de Vera, Markus Flury, Jan Frösler, Jacob Heinz, Yunha Hwang, Samuel P. Kounaves, Kai Mangelsdorf, Rainer U. Meckenstock, Mark Pannekens, Alexander J. Probst, Johan S. Sáenz, Janosch Schirmack, Michael Schloter, Philippe Schmitt-Kopplin, Beate Schneider, Jenny Uhl, Gisle Vestergaard, Bernardita Valenzuela, Pedro Zamorano, and Dirk Wagner. 2021. "Microbial Hotspots in Lithic Microhabitats Inferred from DNA Fractionation and Metagenomics in the Atacama Desert" Microorganisms 9, no. 5: 1038. https://doi.org/10.3390/microorganisms9051038

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Microbial Hotspots in Lithic Microhabitats Inferred from DNA Fractionation and Metagenomics in the Atacama Desert

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