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Diverse viruses carrying genes for microbial extremotolerance in the Atacama Desert hyperarid soil

View ORCID ProfileYunha Hwang, Janina Rahlff, Dirk Schulze-Makuch, Michael Schloter, Alexander J. Probst
doi: https://doi.org/10.1101/2020.09.21.307520
Yunha Hwang
1Department of Organismic and Evolutionary Biology, Harvard University, 02138, MA, USA
2Group for Aquatic Microbial Ecology, Environmental Microbiology and Biotechnology, Department of Chemistry, University of Duisburg-Essen, 45141, Essen, Germany
3Center for Astronomy and Astrophysics, Technische Universität Berlin, 10623, Berlin, Germany
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  • For correspondence: yhwang@g.harvard.edu alexander.probst@uni-due.de
Janina Rahlff
2Group for Aquatic Microbial Ecology, Environmental Microbiology and Biotechnology, Department of Chemistry, University of Duisburg-Essen, 45141, Essen, Germany
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Dirk Schulze-Makuch
3Center for Astronomy and Astrophysics, Technische Universität Berlin, 10623, Berlin, Germany
4German Research Centre for Geosciences (GFZ), Section Geomicrobiology, 14473, Potsdam, Germany
5Department of Experimental Limnology, Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB), 12587, Stechlin, Germany
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Michael Schloter
6Research Unit for Comparative Microbiome Analysis, Helmholtz Zentrum München, German Research Center for Environmental Health, 85758, Oberschleißheim, Germany
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Alexander J. Probst
2Group for Aquatic Microbial Ecology, Environmental Microbiology and Biotechnology, Department of Chemistry, University of Duisburg-Essen, 45141, Essen, Germany
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  • For correspondence: yhwang@g.harvard.edu alexander.probst@uni-due.de
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Abstract

Viruses play an essential role in shaping microbial community structures and serve as reservoirs for genetic diversity in many ecosystems. In hyperarid desert environments, where life itself becomes scarce and loses diversity, the interactions between viruses and host populations have remained elusive. Here, we resolved host-virus interactions in the soil metagenomes of the Atacama Desert hyperarid core, one of the harshest terrestrial environments on Earth. We show evidence of diverse viruses infecting a wide range of hosts found in sites up to 205 km apart. Viral genomes carried putative extremotolerance features (i.e. DNA repair proteins, enzymes against oxidative damage, spore formation proteins) and auxiliary metabolic genes, indicating that viruses could mediate the spread of microbial resilience against environmental stress across the desert. We propose a mutualistic model of host-virus interactions in the hyperarid core where viruses seek protection in microbial cells as lysogens or pseudolysogens, while viral extremotolerance genes aid survival of their hosts. Our results suggest that the host-virus interactions in the Atacama Desert soils are dynamic and complex, shaping uniquely adapted microbiomes in this highly selective and hostile environment.

Importance Deserts are one of the largest and rapidly expanding terrestrial ecosystems characterized by low biodiversity and biomass. The hyperarid core of the Atacama Desert, previously thought to be devoid of life, is one of the harshest environments supporting only scant biomass of highly adapted microbes. While there is growing evidence that viruses play essential roles in shaping the diversity and structure of nearly every ecosystem, very little is known about the role of viruses in desert soils, especially where viral contact with viable hosts is significantly reduced. Our results indicate that diverse viruses are widely dispersed across the desert, potentially spreading key stress resilience and metabolic genes to ensure host survival. The desertification accelerated by climate change expands both the ecosystem cover and the ecological significance of the desert virome. This study sheds light on the complex virus-host interplay that shapes the unique microbiome in desert soils.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted March 31, 2021.
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Diverse viruses carrying genes for microbial extremotolerance in the Atacama Desert hyperarid soil
Yunha Hwang, Janina Rahlff, Dirk Schulze-Makuch, Michael Schloter, Alexander J. Probst
bioRxiv 2020.09.21.307520; doi: https://doi.org/10.1101/2020.09.21.307520
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Diverse viruses carrying genes for microbial extremotolerance in the Atacama Desert hyperarid soil
Yunha Hwang, Janina Rahlff, Dirk Schulze-Makuch, Michael Schloter, Alexander J. Probst
bioRxiv 2020.09.21.307520; doi: https://doi.org/10.1101/2020.09.21.307520

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