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Temporal epigenome modulation enables efficient bacteriophage engineering and functional analysis of phage DNA modifications

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Pozhydaieva,  Nadiia
Max Planck Research Group Bacterial Epitranscriptomics, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

Billau,  Franziska Anna
Max Planck Research Group Bacterial Epitranscriptomics, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Wolfram-Schauerte,  Maik
Max Planck Research Group Bacterial Epitranscriptomics, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Ramírez Rojas,  Adán Andrés
Core Facility MPG MAXGenesys DNAfoundry, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Paczia,  Nicole       
Core Facility Metabolomics and small Molecules Mass Spectrometry, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Schindler,  Daniel       
Core Facility MPG MAXGenesys DNAfoundry, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Höfer,  Katharina       
Max Planck Research Group Bacterial Epitranscriptomics, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Citation

Pozhydaieva, N., Billau, F. A., Wolfram-Schauerte, M., Ramírez Rojas, A. A., Paczia, N., Schindler, D., et al. (2024). Temporal epigenome modulation enables efficient bacteriophage engineering and functional analysis of phage DNA modifications. PLOS Genetics, 20(9): e1011384. doi:10.1371/journal.pgen.1011384.


Cite as: https://hdl.handle.net/21.11116/0000-000F-D0CD-F
Abstract
Author summary Bacteriophages, viruses that target bacteria, hold substantial promise for applications in biotechnological and medical settings. A comprehensive understanding of their infection mechanisms is essential for harnessing their full potential in these fields. To study the mechanisms underlying efficient phage infection, mutagenesis of the bacteriophage genome is the key. While CRISPR-Cas offers a powerful tool for performing mutagenesis in various organisms in a site-specific manner, its application is limited to bacteriophages due to the extensive modification of bacteriophage DNA, collectively termed the epigenome. For bacteriophages with highly modified genomes, e. g. bacteriophage T4, the DNA modifications impede Cas nuclease targeting–a crucial step in CRISPR-Cas mutagenesis. In our study, we introduce a temporal modulation of the bacteriophage epigenome, allowing us to decrease the abundance of bacteriophage DNA modifications. This approach enables the investigation of the biological role of the bacteriophage epigenome and allows for its efficient targeting by Cas nucleases, permitting successful phage mutagenesis. Our approach to modulating the bacteriophage epigenome not only deepens the understanding of bacteriophage infection mechanisms through mutagenesis but also holds significant potential for synthetic biology. This advancement paves the way for the efficient engineering of phages, enhancing their application in biotechnological and medical fields.