Capsids and Genomes of Jumbo-Sized Bacteriophages Reveal the Evolutionary Reach of the HK97 Fold

ABSTRACT Large icosahedral viruses that infect bacteria represent an extreme of the coevolution of capsids and the genomes they accommodate. One subset of these large viruses is the jumbophages, tailed phages with double-stranded DNA genomes of at least 200,000 bp. We explored the mechanism leading...

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Autores principales:	Jianfei Hua, Alexis Huet, Carlos A. Lopez, Katerina Toropova, Welkin H. Pope, Robert L. Duda, Roger W. Hendrix, James F. Conway
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	bacteriophage capsid cryo-EM evolution genome HK97 Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5bc0c24abc934493baae57c06dd4f3f8
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spelling	oai:doaj.org-article:5bc0c24abc934493baae57c06dd4f3f82021-11-15T15:51:51ZCapsids and Genomes of Jumbo-Sized Bacteriophages Reveal the Evolutionary Reach of the HK97 Fold10.1128/mBio.01579-172150-7511https://doaj.org/article/5bc0c24abc934493baae57c06dd4f3f82017-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01579-17https://doaj.org/toc/2150-7511ABSTRACT Large icosahedral viruses that infect bacteria represent an extreme of the coevolution of capsids and the genomes they accommodate. One subset of these large viruses is the jumbophages, tailed phages with double-stranded DNA genomes of at least 200,000 bp. We explored the mechanism leading to increased capsid and genome sizes by characterizing structures of several jumbophage capsids and the DNA packaged within them. Capsid structures determined for six jumbophages were consistent with the canonical phage HK97 fold, and three had capsid geometries with novel triangulation numbers (T=25, T=28, and T=52). Packaged DNA (chromosome) sizes were larger than the genome sizes, indicating that all jumbophages use a head-full DNA packaging mechanism. For two phages (PAU and G), the sizes appeared very much larger than their genome length. We used two-dimensional DNA gel electrophoresis to show that these two DNAs migrated abnormally due to base modifications and to allow us to calculate their actual chromosome sizes. Our results support a ratchet model of capsid and genome coevolution whereby mutations lead to increased capsid volume and allow the acquisition of additional genes. Once the added genes and larger capsid are established, mutations that restore the smaller size are disfavored. IMPORTANCE A large family of viruses share the same fold of the capsid protein as bacteriophage HK97, a virus that infects bacteria. Members of this family use different numbers of the capsid protein to build capsids of different sizes. Here, we examined the structures of extremely large capsids and measured their DNA content relative to the sequenced genome lengths, aiming to understand the process that increases size. We concluded that mutational changes leading to larger capsids become locked in by subsequent changes to the genome organization.Jianfei HuaAlexis HuetCarlos A. LopezKaterina ToropovaWelkin H. PopeRobert L. DudaRoger W. HendrixJames F. ConwayAmerican Society for Microbiologyarticlebacteriophagecapsidcryo-EMevolutiongenomeHK97MicrobiologyQR1-502ENmBio, Vol 8, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	bacteriophage capsid cryo-EM evolution genome HK97 Microbiology QR1-502
spellingShingle	bacteriophage capsid cryo-EM evolution genome HK97 Microbiology QR1-502 Jianfei Hua Alexis Huet Carlos A. Lopez Katerina Toropova Welkin H. Pope Robert L. Duda Roger W. Hendrix James F. Conway Capsids and Genomes of Jumbo-Sized Bacteriophages Reveal the Evolutionary Reach of the HK97 Fold
description	ABSTRACT Large icosahedral viruses that infect bacteria represent an extreme of the coevolution of capsids and the genomes they accommodate. One subset of these large viruses is the jumbophages, tailed phages with double-stranded DNA genomes of at least 200,000 bp. We explored the mechanism leading to increased capsid and genome sizes by characterizing structures of several jumbophage capsids and the DNA packaged within them. Capsid structures determined for six jumbophages were consistent with the canonical phage HK97 fold, and three had capsid geometries with novel triangulation numbers (T=25, T=28, and T=52). Packaged DNA (chromosome) sizes were larger than the genome sizes, indicating that all jumbophages use a head-full DNA packaging mechanism. For two phages (PAU and G), the sizes appeared very much larger than their genome length. We used two-dimensional DNA gel electrophoresis to show that these two DNAs migrated abnormally due to base modifications and to allow us to calculate their actual chromosome sizes. Our results support a ratchet model of capsid and genome coevolution whereby mutations lead to increased capsid volume and allow the acquisition of additional genes. Once the added genes and larger capsid are established, mutations that restore the smaller size are disfavored. IMPORTANCE A large family of viruses share the same fold of the capsid protein as bacteriophage HK97, a virus that infects bacteria. Members of this family use different numbers of the capsid protein to build capsids of different sizes. Here, we examined the structures of extremely large capsids and measured their DNA content relative to the sequenced genome lengths, aiming to understand the process that increases size. We concluded that mutational changes leading to larger capsids become locked in by subsequent changes to the genome organization.
format	article
author	Jianfei Hua Alexis Huet Carlos A. Lopez Katerina Toropova Welkin H. Pope Robert L. Duda Roger W. Hendrix James F. Conway
author_facet	Jianfei Hua Alexis Huet Carlos A. Lopez Katerina Toropova Welkin H. Pope Robert L. Duda Roger W. Hendrix James F. Conway
author_sort	Jianfei Hua
title	Capsids and Genomes of Jumbo-Sized Bacteriophages Reveal the Evolutionary Reach of the HK97 Fold
title_short	Capsids and Genomes of Jumbo-Sized Bacteriophages Reveal the Evolutionary Reach of the HK97 Fold
title_full	Capsids and Genomes of Jumbo-Sized Bacteriophages Reveal the Evolutionary Reach of the HK97 Fold
title_fullStr	Capsids and Genomes of Jumbo-Sized Bacteriophages Reveal the Evolutionary Reach of the HK97 Fold
title_full_unstemmed	Capsids and Genomes of Jumbo-Sized Bacteriophages Reveal the Evolutionary Reach of the HK97 Fold
title_sort	capsids and genomes of jumbo-sized bacteriophages reveal the evolutionary reach of the hk97 fold
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/5bc0c24abc934493baae57c06dd4f3f8
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Capsids and Genomes of Jumbo-Sized Bacteriophages Reveal the Evolutionary Reach of the HK97 Fold

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