Staphylococci phages display vast genomic diversity and evolutionary relationships

BACKGROUND: Bacteriophages are the most abundant and diverse entities in the biosphere, and this diversity is driven by constant predator–prey evolutionary dynamics and horizontal gene transfer. Phage genome sequences are under-sampled and therefore present an untapped and uncharacterized source of...

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Autores principales: Oliveira, Hugo, Sampaio, Marta, Melo, Luís D. R., Dias, Oscar, Pope, Welkin H., Hatfull, Graham F., Azeredo, Joana
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6507118/
https://www.ncbi.nlm.nih.gov/pubmed/31072320
http://dx.doi.org/10.1186/s12864-019-5647-8
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author Oliveira, Hugo
Sampaio, Marta
Melo, Luís D. R.
Dias, Oscar
Pope, Welkin H.
Hatfull, Graham F.
Azeredo, Joana
author_facet Oliveira, Hugo
Sampaio, Marta
Melo, Luís D. R.
Dias, Oscar
Pope, Welkin H.
Hatfull, Graham F.
Azeredo, Joana
author_sort Oliveira, Hugo
collection PubMed
description BACKGROUND: Bacteriophages are the most abundant and diverse entities in the biosphere, and this diversity is driven by constant predator–prey evolutionary dynamics and horizontal gene transfer. Phage genome sequences are under-sampled and therefore present an untapped and uncharacterized source of genetic diversity, typically characterized by highly mosaic genomes and no universal genes. To better understand the diversity and relationships among phages infecting human pathogens, we have analysed the complete genome sequences of 205 phages of Staphylococcus sp. RESULTS: These are predicted to encode 20,579 proteins, which can be sorted into 2139 phamilies (phams) of related sequences; 745 of these are orphams and possess only a single gene. Based on shared gene content, these phages were grouped into four clusters (A, B, C and D), 27 subclusters (A1-A2, B1-B17, C1-C6 and D1-D2) and one singleton. However, the genomes have mosaic architectures and individual genes with common ancestors are positioned in distinct genomic contexts in different clusters. The staphylococcal Cluster B siphoviridae are predicted to be temperate, and the integration cassettes are often closely-linked to genes implicated in bacterial virulence determinants. There are four unusual endolysin organization strategies found in Staphylococcus phage genomes, with endolysins predicted to be encoded as single genes, two genes spliced, two genes adjacent and as a single gene with inter-lytic-domain secondary translational start site. Comparison of the endolysins reveals multi-domain modularity, with conservation of the SH3 cell wall binding domain. CONCLUSIONS: This study provides a high-resolution view of staphylococcal viral genetic diversity, and insights into their gene flux patterns within and across different phage groups (cluster and subclusters) providing insights into their evolution. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5647-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-65071182019-05-13 Staphylococci phages display vast genomic diversity and evolutionary relationships Oliveira, Hugo Sampaio, Marta Melo, Luís D. R. Dias, Oscar Pope, Welkin H. Hatfull, Graham F. Azeredo, Joana BMC Genomics Research Article BACKGROUND: Bacteriophages are the most abundant and diverse entities in the biosphere, and this diversity is driven by constant predator–prey evolutionary dynamics and horizontal gene transfer. Phage genome sequences are under-sampled and therefore present an untapped and uncharacterized source of genetic diversity, typically characterized by highly mosaic genomes and no universal genes. To better understand the diversity and relationships among phages infecting human pathogens, we have analysed the complete genome sequences of 205 phages of Staphylococcus sp. RESULTS: These are predicted to encode 20,579 proteins, which can be sorted into 2139 phamilies (phams) of related sequences; 745 of these are orphams and possess only a single gene. Based on shared gene content, these phages were grouped into four clusters (A, B, C and D), 27 subclusters (A1-A2, B1-B17, C1-C6 and D1-D2) and one singleton. However, the genomes have mosaic architectures and individual genes with common ancestors are positioned in distinct genomic contexts in different clusters. The staphylococcal Cluster B siphoviridae are predicted to be temperate, and the integration cassettes are often closely-linked to genes implicated in bacterial virulence determinants. There are four unusual endolysin organization strategies found in Staphylococcus phage genomes, with endolysins predicted to be encoded as single genes, two genes spliced, two genes adjacent and as a single gene with inter-lytic-domain secondary translational start site. Comparison of the endolysins reveals multi-domain modularity, with conservation of the SH3 cell wall binding domain. CONCLUSIONS: This study provides a high-resolution view of staphylococcal viral genetic diversity, and insights into their gene flux patterns within and across different phage groups (cluster and subclusters) providing insights into their evolution. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5647-8) contains supplementary material, which is available to authorized users. BioMed Central 2019-05-09 /pmc/articles/PMC6507118/ /pubmed/31072320 http://dx.doi.org/10.1186/s12864-019-5647-8 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Oliveira, Hugo
Sampaio, Marta
Melo, Luís D. R.
Dias, Oscar
Pope, Welkin H.
Hatfull, Graham F.
Azeredo, Joana
Staphylococci phages display vast genomic diversity and evolutionary relationships
title Staphylococci phages display vast genomic diversity and evolutionary relationships
title_full Staphylococci phages display vast genomic diversity and evolutionary relationships
title_fullStr Staphylococci phages display vast genomic diversity and evolutionary relationships
title_full_unstemmed Staphylococci phages display vast genomic diversity and evolutionary relationships
title_short Staphylococci phages display vast genomic diversity and evolutionary relationships
title_sort staphylococci phages display vast genomic diversity and evolutionary relationships
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6507118/
https://www.ncbi.nlm.nih.gov/pubmed/31072320
http://dx.doi.org/10.1186/s12864-019-5647-8
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