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Genome-informed microscopy reveals infections of uncultivated carbon-fixing archaea by lytic viruses in Earth’s crust

View ORCID ProfileJanina Rahlff, Victoria Turzynski, Sarah P. Esser, Indra Monsees, Till L.V. Bornemann, Perla Abigail Figueroa-Gonzalez, View ORCID ProfileFrederik Schulz, View ORCID ProfileTanja Woyke, View ORCID ProfileAndreas Klingl, View ORCID ProfileCristina Moraru, View ORCID ProfileAlexander J. Probst
doi: https://doi.org/10.1101/2020.07.22.215848
Janina Rahlff
1University of Duisburg-Essen, Department of Chemistry, Environmental Microbiology and Biotechnology (EMB), Group for Aquatic Microbial Ecology, Universitätsstraße 5, 45141 Essen, Germany
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Victoria Turzynski
1University of Duisburg-Essen, Department of Chemistry, Environmental Microbiology and Biotechnology (EMB), Group for Aquatic Microbial Ecology, Universitätsstraße 5, 45141 Essen, Germany
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Sarah P. Esser
1University of Duisburg-Essen, Department of Chemistry, Environmental Microbiology and Biotechnology (EMB), Group for Aquatic Microbial Ecology, Universitätsstraße 5, 45141 Essen, Germany
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Indra Monsees
1University of Duisburg-Essen, Department of Chemistry, Environmental Microbiology and Biotechnology (EMB), Group for Aquatic Microbial Ecology, Universitätsstraße 5, 45141 Essen, Germany
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Till L.V. Bornemann
1University of Duisburg-Essen, Department of Chemistry, Environmental Microbiology and Biotechnology (EMB), Group for Aquatic Microbial Ecology, Universitätsstraße 5, 45141 Essen, Germany
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Perla Abigail Figueroa-Gonzalez
1University of Duisburg-Essen, Department of Chemistry, Environmental Microbiology and Biotechnology (EMB), Group for Aquatic Microbial Ecology, Universitätsstraße 5, 45141 Essen, Germany
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Frederik Schulz
2DOE Joint Genome Institute, 1 Cyclotron Rd, Berkeley, CA, 94720, USA
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Tanja Woyke
2DOE Joint Genome Institute, 1 Cyclotron Rd, Berkeley, CA, 94720, USA
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Andreas Klingl
3Plant Development & Electron Microscopy, Biocenter LMU Munich, Großhaderner Str. 2-4, 82152 Planegg-Martinsried, Germany
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Cristina Moraru
4Institute for Chemistry and Biology of the Marine Environment (ICBM), Carl-von-Ossietzky-University Oldenburg, PO Box 2503, Carl-von-Ossietzky-Straße 9-11, 26111, Oldenburg, Germany
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Alexander J. Probst
1University of Duisburg-Essen, Department of Chemistry, Environmental Microbiology and Biotechnology (EMB), Group for Aquatic Microbial Ecology, Universitätsstraße 5, 45141 Essen, Germany
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  • For correspondence: alexander.probst@uni-due.de
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ABSTRACT

The continental subsurface houses a major portion of life’s abundance and diversity, yet little is known about viruses infecting microbes that reside there. Here, we used a combination of metagenomics and genome-informed microscopy to show that highly abundant carbon-fixing organisms of the uncultivated genus Candidatus Altiarchaeum are frequent targets of previously unrecognized viruses in the deep subsurface. Analysis of CRISPR spacer matches displayed resistances of Ca. Altiarchaea against eight predicted viral clades, which showed genomic relatedness across continents but little similarity to previously identified viruses. Based on metagenomic information, we tagged and imaged a putatively viral genome rich in protospacers using fluorescence microscopy. Virus-targeted genomeFISH revealed a lytic lifestyle of the respective virus and challenges previous predictions that lysogeny prevails as the dominant viral lifestyle in the subsurface. CRISPR development over time and imaging of 18 samples from one subsurface ecosystem suggest a sophisticated interplay of viral diversification and adapting CRISPR-mediated resistances of Ca. Altiarchaeum. We conclude that infections of primary producers with lytic viruses followed by cell lysis potentially jump-start heterotrophic carbon cycling in these subsurface ecosystems.

Competing Interest Statement

The authors have declared no competing interest.

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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 July 22, 2020.
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Genome-informed microscopy reveals infections of uncultivated carbon-fixing archaea by lytic viruses in Earth’s crust
Janina Rahlff, Victoria Turzynski, Sarah P. Esser, Indra Monsees, Till L.V. Bornemann, Perla Abigail Figueroa-Gonzalez, Frederik Schulz, Tanja Woyke, Andreas Klingl, Cristina Moraru, Alexander J. Probst
bioRxiv 2020.07.22.215848; doi: https://doi.org/10.1101/2020.07.22.215848
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Genome-informed microscopy reveals infections of uncultivated carbon-fixing archaea by lytic viruses in Earth’s crust
Janina Rahlff, Victoria Turzynski, Sarah P. Esser, Indra Monsees, Till L.V. Bornemann, Perla Abigail Figueroa-Gonzalez, Frederik Schulz, Tanja Woyke, Andreas Klingl, Cristina Moraru, Alexander J. Probst
bioRxiv 2020.07.22.215848; doi: https://doi.org/10.1101/2020.07.22.215848

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