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Evolution along the parasitism-mutualism continuum determines the genetic repertoire of prophages

Integrated into their bacterial hosts’ genomes, prophage sequences exhibit a wide diversity of length and gene content, from highly degraded cryptic sequences to intact, functional prophages that retain a full complement of lytic-function genes. We apply three approaches—bioinformatics, analytical m...

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Detalles Bibliográficos
Autores principales: Khan, Amjad, Burmeister, Alita R., Wahl, Lindi M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7744054/
https://www.ncbi.nlm.nih.gov/pubmed/33275597
http://dx.doi.org/10.1371/journal.pcbi.1008482
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author Khan, Amjad
Burmeister, Alita R.
Wahl, Lindi M.
author_facet Khan, Amjad
Burmeister, Alita R.
Wahl, Lindi M.
author_sort Khan, Amjad
collection PubMed
description Integrated into their bacterial hosts’ genomes, prophage sequences exhibit a wide diversity of length and gene content, from highly degraded cryptic sequences to intact, functional prophages that retain a full complement of lytic-function genes. We apply three approaches—bioinformatics, analytical modelling and computational simulation—to understand the diverse gene content of prophages. In the bioinformatics work, we examine the distributions of over 50,000 annotated prophage genes identified in 1384 prophage sequences, comparing the gene repertoires of intact and incomplete prophages. These data indicate that genes involved in the replication, packaging, and release of phage particles have been preferentially lost in incomplete prophages, while tail fiber, transposase and integrase genes are significantly enriched. Consistent with these results, our mathematical and computational approaches predict that genes involved in phage lytic function are preferentially lost, resulting in shorter prophages that often retain genes that benefit the host. Informed by these models, we offer novel hypotheses for the enrichment of integrase and transposase genes in cryptic prophages. Overall, we demonstrate that functional and cryptic prophages represent a diversity of genetic sequences that evolve along a parasitism-mutualism continuum.
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spelling pubmed-77440542020-12-31 Evolution along the parasitism-mutualism continuum determines the genetic repertoire of prophages Khan, Amjad Burmeister, Alita R. Wahl, Lindi M. PLoS Comput Biol Research Article Integrated into their bacterial hosts’ genomes, prophage sequences exhibit a wide diversity of length and gene content, from highly degraded cryptic sequences to intact, functional prophages that retain a full complement of lytic-function genes. We apply three approaches—bioinformatics, analytical modelling and computational simulation—to understand the diverse gene content of prophages. In the bioinformatics work, we examine the distributions of over 50,000 annotated prophage genes identified in 1384 prophage sequences, comparing the gene repertoires of intact and incomplete prophages. These data indicate that genes involved in the replication, packaging, and release of phage particles have been preferentially lost in incomplete prophages, while tail fiber, transposase and integrase genes are significantly enriched. Consistent with these results, our mathematical and computational approaches predict that genes involved in phage lytic function are preferentially lost, resulting in shorter prophages that often retain genes that benefit the host. Informed by these models, we offer novel hypotheses for the enrichment of integrase and transposase genes in cryptic prophages. Overall, we demonstrate that functional and cryptic prophages represent a diversity of genetic sequences that evolve along a parasitism-mutualism continuum. Public Library of Science 2020-12-04 /pmc/articles/PMC7744054/ /pubmed/33275597 http://dx.doi.org/10.1371/journal.pcbi.1008482 Text en © 2020 Khan et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Khan, Amjad
Burmeister, Alita R.
Wahl, Lindi M.
Evolution along the parasitism-mutualism continuum determines the genetic repertoire of prophages
title Evolution along the parasitism-mutualism continuum determines the genetic repertoire of prophages
title_full Evolution along the parasitism-mutualism continuum determines the genetic repertoire of prophages
title_fullStr Evolution along the parasitism-mutualism continuum determines the genetic repertoire of prophages
title_full_unstemmed Evolution along the parasitism-mutualism continuum determines the genetic repertoire of prophages
title_short Evolution along the parasitism-mutualism continuum determines the genetic repertoire of prophages
title_sort evolution along the parasitism-mutualism continuum determines the genetic repertoire of prophages
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7744054/
https://www.ncbi.nlm.nih.gov/pubmed/33275597
http://dx.doi.org/10.1371/journal.pcbi.1008482
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