Bacteriophages of <italic toggle="yes">Gordonia</italic> spp. Display a Spectrum of Diversity and Genetic Relationships

ABSTRACT The global bacteriophage population is large, dynamic, old, and highly diverse genetically. Many phages are tailed and contain double-stranded DNA, but these remain poorly characterized genomically. A collection of over 1,000 phages infecting Mycobacterium smegmatis reveals the diversity of...

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Autores principales: Welkin H. Pope, Travis N. Mavrich, Rebecca A. Garlena, Carlos A. Guerrero-Bustamante, Deborah Jacobs-Sera, Matthew T. Montgomery, Daniel A. Russell, Marcie H. Warner, Graham F. Hatfull
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Publicado: American Society for Microbiology 2017
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spelling oai:doaj.org-article:e76b5255d6aa4fafb2b3fd4034903cdb2021-11-15T15:51:42ZBacteriophages of <italic toggle="yes">Gordonia</italic> spp. Display a Spectrum of Diversity and Genetic Relationships10.1128/mBio.01069-172150-7511https://doaj.org/article/e76b5255d6aa4fafb2b3fd4034903cdb2017-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01069-17https://doaj.org/toc/2150-7511ABSTRACT The global bacteriophage population is large, dynamic, old, and highly diverse genetically. Many phages are tailed and contain double-stranded DNA, but these remain poorly characterized genomically. A collection of over 1,000 phages infecting Mycobacterium smegmatis reveals the diversity of phages of a common bacterial host, but their relationships to phages of phylogenetically proximal hosts are not known. Comparative sequence analysis of 79 phages isolated on Gordonia shows these also to be diverse and that the phages can be grouped into 14 clusters of related genomes, with an additional 14 phages that are “singletons” with no closely related genomes. One group of six phages is closely related to Cluster A mycobacteriophages, but the other Gordonia phages are distant relatives and share only 10% of their genes with the mycobacteriophages. The Gordonia phage genomes vary in genome length (17.1 to 103.4 kb), percentage of GC content (47 to 68.8%), and genome architecture and contain a variety of features not seen in other phage genomes. Like the mycobacteriophages, the highly mosaic Gordonia phages demonstrate a spectrum of genetic relationships. We show this is a general property of bacteriophages and suggest that any barriers to genetic exchange are soft and readily violable. IMPORTANCE Despite the numerical dominance of bacteriophages in the biosphere, there is a dearth of complete genomic sequences. Current genomic information reveals that phages are highly diverse genomically and have mosaic architectures formed by extensive horizontal genetic exchange. Comparative analysis of 79 phages of Gordonia shows them to not only be highly diverse, but to present a spectrum of relatedness. Most are distantly related to phages of the phylogenetically proximal host Mycobacterium smegmatis, although one group of Gordonia phages is more closely related to mycobacteriophages than to the other Gordonia phages. Phage genome sequence space remains largely unexplored, but further isolation and genomic comparison of phages targeted at related groups of hosts promise to reveal pathways of bacteriophage evolution.Welkin H. PopeTravis N. MavrichRebecca A. GarlenaCarlos A. Guerrero-BustamanteDeborah Jacobs-SeraMatthew T. MontgomeryDaniel A. RussellMarcie H. WarnerGraham F. HatfullAmerican Society for MicrobiologyarticleGordoniabacteriophage geneticsbacteriophagesMicrobiologyQR1-502ENmBio, Vol 8, Iss 4 (2017)
institution DOAJ
collection DOAJ
language EN
topic Gordonia
bacteriophage genetics
bacteriophages
Microbiology
QR1-502
spellingShingle Gordonia
bacteriophage genetics
bacteriophages
Microbiology
QR1-502
Welkin H. Pope
Travis N. Mavrich
Rebecca A. Garlena
Carlos A. Guerrero-Bustamante
Deborah Jacobs-Sera
Matthew T. Montgomery
Daniel A. Russell
Marcie H. Warner
Graham F. Hatfull
Bacteriophages of <italic toggle="yes">Gordonia</italic> spp. Display a Spectrum of Diversity and Genetic Relationships
description ABSTRACT The global bacteriophage population is large, dynamic, old, and highly diverse genetically. Many phages are tailed and contain double-stranded DNA, but these remain poorly characterized genomically. A collection of over 1,000 phages infecting Mycobacterium smegmatis reveals the diversity of phages of a common bacterial host, but their relationships to phages of phylogenetically proximal hosts are not known. Comparative sequence analysis of 79 phages isolated on Gordonia shows these also to be diverse and that the phages can be grouped into 14 clusters of related genomes, with an additional 14 phages that are “singletons” with no closely related genomes. One group of six phages is closely related to Cluster A mycobacteriophages, but the other Gordonia phages are distant relatives and share only 10% of their genes with the mycobacteriophages. The Gordonia phage genomes vary in genome length (17.1 to 103.4 kb), percentage of GC content (47 to 68.8%), and genome architecture and contain a variety of features not seen in other phage genomes. Like the mycobacteriophages, the highly mosaic Gordonia phages demonstrate a spectrum of genetic relationships. We show this is a general property of bacteriophages and suggest that any barriers to genetic exchange are soft and readily violable. IMPORTANCE Despite the numerical dominance of bacteriophages in the biosphere, there is a dearth of complete genomic sequences. Current genomic information reveals that phages are highly diverse genomically and have mosaic architectures formed by extensive horizontal genetic exchange. Comparative analysis of 79 phages of Gordonia shows them to not only be highly diverse, but to present a spectrum of relatedness. Most are distantly related to phages of the phylogenetically proximal host Mycobacterium smegmatis, although one group of Gordonia phages is more closely related to mycobacteriophages than to the other Gordonia phages. Phage genome sequence space remains largely unexplored, but further isolation and genomic comparison of phages targeted at related groups of hosts promise to reveal pathways of bacteriophage evolution.
format article
author Welkin H. Pope
Travis N. Mavrich
Rebecca A. Garlena
Carlos A. Guerrero-Bustamante
Deborah Jacobs-Sera
Matthew T. Montgomery
Daniel A. Russell
Marcie H. Warner
Graham F. Hatfull
author_facet Welkin H. Pope
Travis N. Mavrich
Rebecca A. Garlena
Carlos A. Guerrero-Bustamante
Deborah Jacobs-Sera
Matthew T. Montgomery
Daniel A. Russell
Marcie H. Warner
Graham F. Hatfull
author_sort Welkin H. Pope
title Bacteriophages of <italic toggle="yes">Gordonia</italic> spp. Display a Spectrum of Diversity and Genetic Relationships
title_short Bacteriophages of <italic toggle="yes">Gordonia</italic> spp. Display a Spectrum of Diversity and Genetic Relationships
title_full Bacteriophages of <italic toggle="yes">Gordonia</italic> spp. Display a Spectrum of Diversity and Genetic Relationships
title_fullStr Bacteriophages of <italic toggle="yes">Gordonia</italic> spp. Display a Spectrum of Diversity and Genetic Relationships
title_full_unstemmed Bacteriophages of <italic toggle="yes">Gordonia</italic> spp. Display a Spectrum of Diversity and Genetic Relationships
title_sort bacteriophages of <italic toggle="yes">gordonia</italic> spp. display a spectrum of diversity and genetic relationships
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/e76b5255d6aa4fafb2b3fd4034903cdb
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