NOVAC – Novel viruses of terrestrial subsurface archaea impacting global carbon cycling
Final Report Abstract
In the project NOVAC, we investigated infections of uncultured archaea (Candidatus Altiarchaeum spp.) with yet unknown viruses for gaining insight into virus-host interactions in the deep biosphere and for identifying novel viruses. The host was sampled in the reference ecosystem as a biofilm washed up with groundwater. To fulfil these ambitious goals, we used combinations of metagenomics, metatranscriptomics, and correlative microscopy. We identified several viruses that showed infection histories with hosts based on genomic information. To visualize a selected virus in the ecosystem, we adapted virusFISH, a direct-GeneFISH protocol. Fluorescence microscopy images were thoroughly studied with respect to different infection stages, which not only led to the postulation of an infection cycle of natural biofilms in groundwater, but also challenged a long-standing paradigm of the deep biosphere: Visualizations showed a lytic life cycle of the dominant virus, contrasting a previous paradigm predicted the dominance of temperate viruses. Investigations of several biofilms revealed rodshaped bacteria accumulating in regions with high cell lysis rates, indicating heterotrophy and a virus-driven food chain. After thorough literature review, we investigated several approaches to visualize the viruses not only by fluorescence microscopy/virusFISH but also by electron microscopy. The correlation of fluorescence and scanning electron microscopy was the ultimate breakthrough, which not only showed morphological changes of the host during infection, but also visualized the virus particles on the cell surface. Thus, this project not only provided new insights into understanding the complexity of virus-host interactions in the deep biosphere, but also introduces a protocol for visualization of the ultrastructure of virus-host interactions based on sequencing data.
Publications
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Genome-informed microscopy: CLEM for studying viral infection of uncultivated archaea. Microscopy conference 2019, Berlin, Deutschland
Monsees I.; Turzynski V.; Rahlff J.; Klingl A. & Probst A.
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Genome-informed microscopy reveals viral infections of uncultivated archaea in a terrestrial subsurface aquifer. VAAM - Vereinigung für Allgemeine und Angewandte Mikrobiologie, Leipzig, Deutschland
Turzynski, V.; Rahlff, J.; Moraru, C. & Probst, A. J.
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Label-free Raman microspectroscopy for studying infections with bacteriophage. Scix20.
Monsees I. & Probst A.
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Label-free Raman microspectroscopy to study bacteriophage infections. European microscopy conference (virtual presentation)
Monsees, I. & Probst, A.
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Metagenomic prediction of altiarchaeotal virus-host dynamics in a high-CO2 subsurface environment. VAAM - Vereinigung für Allgemeine und Angewandte Mikrobiologie, Leipzig, Deutschland
Esser, S. P.; Bornemann. T. L. V.; Rahlff, J. & Probst, A. J.
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Studying bacteriophage infections using Raman microspectroscopy. VAAM - Vereinigung für Allgemeine und Angewandte Mikrobiologie, Leipzig, Deutschland
Monsees I.; Turzynski V. & Probst A.
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Exploring sample preparation for structure conversation of archaeal cell appendices in a correlative Fluorescence/ Scanning electron Microscopy study. Microscopy conference 2021
Monsees, I.; Turzynski, V.; Hasenberg, M.; Klingl, A. & Probst, A.
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Imaging Techniques for Detecting Prokaryotic Viruses in Environmental Samples. Viruses, 13(11), 2126.
Turzynski, Victoria; Monsees, Indra; Moraru, Cristina & Probst, Alexander J.
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Interactions of archaea and their episymbionts based on CRISPR-Cas interference. VAAM - Vereinigung für Allgemeine und Angewandte Mikrobiologie
Esser, S.P.; Rahlff, J.; Zhao, W. Predl.; M.; Adam, P.S.; Schwank, K.; Krupovic, M.; Bornemann, T.L.V.; Figueroa-Gonzalez, P.A.; Lee, J. Jarett, J.; Rattei, T.; Amano, Y.; Woyke, T.; Zhang, Y. & Probst, A.J.
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Lytic archaeal viruses infect abundant primary producers in Earth’s crust. Nature Communications, 12(1).
Rahlff, Janina; Turzynski, Victoria; Esser, Sarah P.; Monsees, Indra; Bornemann, Till L. V.; Figueroa-Gonzalez, Perla Abigail; Schulz, Frederik; Woyke, Tanja; Klingl, Andreas; Moraru, Cristina & Probst, Alexander J.
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Lytic archaeal viruses of the continental deep biosphere challenge a longstanding paradigm. DOE Joint Genome Institute – Genomics of Energy & Environment Meeting
Turzynski, V.; Rahlff, J.; Esser, S.; Monsees, I.; Bornemann, T.L.V.; Griesdorn, L.; Figueroa-Gonzalez, P. A.; Schulz, F.; Woyke, T.; Klingl, A.; Moraru, C. & Probst, A. J.
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Persistent viral infections of Altiarchaeota in the deep biosphere. 21th German Archaea Meeting, Frankfurt, Deutschland
Turzynski, V.; Rahlff, J.; Esser, S.; Monsees, I.; Bornemann, T.L.V.; Griesdorn, L.; Figueroa-Gonzalez, P. A.; Schulz, F.; Woyke, T.; Klingl, A.; Moraru, C. & Probst, A. J.
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Virocell identification via Raman microspectroscopy. Scix21
Monsees, I.; Turzynski, V.; Esser, S.P.; Soares, A.; Timmermann, L.; Kloster, M.; Beszteri, B. & Probst
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An archaeon with and without its episymbiont: Differences in the expression profile. ISME18 - International Symposium on Microbial Ecology, Lausanne, Switzerland
Esser, S. P.; Moore, C. J.; Plewka, J.; Banas, I.; Lee, J.; Woyke, T. & Probst, A. J.
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Correlative microscopy reveals impact of viral infections on archaeal biofilm composition in groundwater. ISME18 - International Symposium on Microbial Ecology, Lausanne, Switzerland
anas, I.; Turzynski, V.; Hasenberg, M.; Klingl, A. & Probst, A.
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Exploring viral infections of uncultivated archaeal cells using correlative microscopy. VAAM - Vereinigung für Allgemeine und Angewandte Mikrobiologie (virtual presentation)
Monsees, I.; Turzynski, V.; Hasenberg, M.; Klingl, A. & Probst, A.
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Identification/Ultrastructure of novel archaeal viruses with help of multi-omics. EMBO course: Integrated multiomics analysis of microbial communities, Luxembourg, Luxembourg
Esser, S. P.; Monsees, I.; Turzynski, V. & Probst, A. J.
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Label-Free Raman Microspectroscopy for Identifying Prokaryotic Virocells. mSystems, 7(1).
Monsees, Indra; Turzynski, Victoria; Esser, Sarah P.; Soares, André; Timmermann, Lara I.; Weidenbach, Katrin; Banas, Jarno; Kloster, Michael; Beszteri, Bánk; Schmitz, Ruth A. & Probst, Alexander J.
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Microdiversity of archaeal viruses from a terrestrial subsurface aquifer. Viruses of Microbes 2022, Guimarães, Portugal
Esser, S. P.; Beesley, T.; Moore, C. J.; Banas, I.; Turzynski, V. & Probst, A. .J.
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Persistent viral infections of uncultivated subsurface archaea are associated with drastic morphological changes of the host, Annual Conference of the Association for General and Applied Microbiology VAAM
Turzynski, V.; Monsees, I.; Griesdorn, L.; Moraru, C. & Probst, A. J.
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A predicted CRISPR-mediated symbiosis between uncultivated archaea. Nature Microbiology, 8(9), 1619-1633.
Esser, Sarah P.; Rahlff, Janina; Zhao, Weishu; Predl, Michael; Plewka, Julia; Sures, Katharina; Wimmer, Franziska; Lee, Janey; Adam, Panagiotis S.; McGonigle, Julia; Turzynski, Victoria; Banas, Indra; Schwank, Katrin; Krupovic, Mart; Bornemann, Till L. V.; Figueroa-Gonzalez, Perla Abigail; Jarett, Jessica; Rattei, Thomas; Amano, Yuki ... & Probst, Alexander J.
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Identification and characterization of uncultivated archaeal virocells using correlative fluorescence and scanning electron microscopy. Microscopy conference 2023, Darmstadt, Deutschland
Banas, I.; Turzynski, V.; Hasenberg, M.; Klingl, A. & Probst, A.
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Spatio-functional organization in virocells of small uncultivated archaea from the deep biosphere. The ISME Journal, 17(10), 1789-1792.
Banas, Indra; Esser, Sarah P.; Turzynski, Victoria; Soares, André; Novikova, Polina; May, Patrick; Moraru, Cristina; Hasenberg, Mike; Rahlff, Janina; Wilmes, Paul; Klingl, Andreas & Probst, Alexander J.
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Virus-Host Dynamics in Archaeal Groundwater Biofilms and the Associated Bacterial Community Composition. Viruses, 15(4), 910.
Turzynski, Victoria; Griesdorn, Lea; Moraru, Cristina; Soares, André R.; Simon, Sophie A.; Stach, Tom L.; Rahlff, Janina; Esser, Sarah P. & Probst, Alexander J.
