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The Promise and Pitfalls of Prophages

View ORCID ProfileJody C. McKerral, View ORCID ProfileBhavya Papudeshi, View ORCID ProfileLaura K. Inglis, View ORCID ProfileMichael J. Roach, View ORCID ProfilePrzemyslaw Decewicz, View ORCID ProfileKatelyn McNair, View ORCID ProfileAntoni Luque, View ORCID ProfileElizabeth A. Dinsdale, View ORCID ProfileRobert A. Edwards
doi: https://doi.org/10.1101/2023.04.20.537752
Jody C. McKerral
1College of Science and Engineering, Flinders University, Bedford Park, SA, 5042, Australia
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Bhavya Papudeshi
2Flinders Accelerator for Microbiome Exploration, College of Science and Engineering, Flinders University, Bedford Park, SA, 5042, Australia
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Laura K. Inglis
2Flinders Accelerator for Microbiome Exploration, College of Science and Engineering, Flinders University, Bedford Park, SA, 5042, Australia
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Michael J. Roach
2Flinders Accelerator for Microbiome Exploration, College of Science and Engineering, Flinders University, Bedford Park, SA, 5042, Australia
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Przemyslaw Decewicz
3Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Miecznikowa 1, Warsaw, 02-096, Poland
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Katelyn McNair
4Computational Sciences Research Center, San Diego State University, 5500 Campanile Dr., San Diego, CA, 92182, USA
5The Viral Information Institute, San Diego State University, 5500 Campanile Dr., San Diego, CA, 92182, USA
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Antoni Luque
5The Viral Information Institute, San Diego State University, 5500 Campanile Dr., San Diego, CA, 92182, USA
6Department of Mathematics and Statistics, San Diego State University, 5500 Campanile Dr., San Diego, CA, 92182, USA
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Elizabeth A. Dinsdale
2Flinders Accelerator for Microbiome Exploration, College of Science and Engineering, Flinders University, Bedford Park, SA, 5042, Australia
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Robert A. Edwards
2Flinders Accelerator for Microbiome Exploration, College of Science and Engineering, Flinders University, Bedford Park, SA, 5042, Australia
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  • For correspondence: robert.edwards@flinders.edu.au
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Abstract

Phages dominate every ecosystem on the planet. While virulent phages sculpt the microbiome by killing their bacterial hosts, temperate phages provide unique growth advantages to their hosts through lysogenic conversion. Many prophages benefit their host, and prophages are responsible for genotypic and phenotypic differences that separate individual microbial strains. However, the microbes also endure a cost to maintain those phages: additional DNA to replicate and proteins to transcribe and translate. We have never quantified those benefits and costs. Here, we analysed over two and a half million prophages from over half a million bacterial genome assemblies. Analysis of the whole dataset and a representative subset of taxonomically diverse bacterial genomes demonstrated that the normalised prophage density was uniform across all bacterial genomes above 2 Mbp. We identified a constant carrying capacity of phage DNA per bacterial DNA. We estimated that each prophage provides cellular services equivalent to approximately 2.4 % of the cell’s energy or 0.9 ATP per bp per hour. We demonstrate analytical, taxonomic, geographic, and temporal disparities in identifying prophages in bacterial genomes that provide novel targets for identifying new phages. We anticipate that the benefits bacteria accrue from the presence of prophages balance the energetics involved in supporting prophages. Furthermore, our data will provide a new framework for identifying phages in environmental datasets, diverse bacterial phyla, and from different locations.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://open.flinders.edu.au/projects/Prophage_predictions/162127

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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The Promise and Pitfalls of Prophages
Jody C. McKerral, Bhavya Papudeshi, Laura K. Inglis, Michael J. Roach, Przemyslaw Decewicz, Katelyn McNair, Antoni Luque, Elizabeth A. Dinsdale, Robert A. Edwards
bioRxiv 2023.04.20.537752; doi: https://doi.org/10.1101/2023.04.20.537752
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The Promise and Pitfalls of Prophages
Jody C. McKerral, Bhavya Papudeshi, Laura K. Inglis, Michael J. Roach, Przemyslaw Decewicz, Katelyn McNair, Antoni Luque, Elizabeth A. Dinsdale, Robert A. Edwards
bioRxiv 2023.04.20.537752; doi: https://doi.org/10.1101/2023.04.20.537752

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