Evolutionary Relationships among Actinophages and a Putative Adaptation for Growth in Streptomyces spp.

Margaret C. M. Smith*, Roger W. Hendrix, Rebekah Dedrick, Kaitlin Mitchell, Ching-Chung Ko, Daniel Russell, Emma Bell, Matthew Gregory, Maureen J. Bibb, Florence Pethick, Deborah Jacobs-Sera, Paul Herron, Mark J. Buttner, Graham F. Hatfull

*Corresponding author for this work

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

The genome sequences of eight Streptomyces phages are presented, four of which were isolated for this study. Phages R4, TG1, phi Hau3, and SV1 were isolated previously and have been exploited as tools for understanding and genetically manipulating Streptomyces spp. We also extracted five apparently intact prophages from recent Streptomyces spp. genome projects and, together with six phage genomes in the database, we analyzed all 19 Streptomyces phage genomes with a view to understanding their relationships to each other and to other actinophages, particularly the mycobacteriophages. Fifteen of the Streptomyces phages group into four clusters of related genomes. Although the R4-like phages do not share nucleotide sequence similarity with other phages, they clearly have common ancestry with cluster A mycobacteriophages, sharing many protein homologues, common gene syntenies, and similar repressor-stoperator regulatory systems. The R4-like phage phi Hau3 and the prophage StrepC.1 (from Streptomyces sp. strain C) appear to have hijacked a unique adaptation of the streptomycetes, i.e., use of the rare UUA codon, to control translation of the essential phage protein, the terminase. The Streptomyces venezuelae generalized transducing phage SV1 was used to predict the presence of other generalized transducing phages for different Streptomyces species.

Original languageEnglish
Pages (from-to)4924-4935
Number of pages12
JournalJournal of Bacteriology
Volume195
Issue number21
Early online date30 Aug 2013
DOIs
Publication statusPublished - Nov 2013

Keywords

  • temperate phage PHI-C31
  • complete genome sequence
  • plasmid cloning vectors
  • transfer-RNA
  • Coelicolor A3(2)
  • bacteriophage PHI-C31
  • nucleotide-sequence
  • lytic development
  • early region
  • host-range

Cite this

Smith, M. C. M., Hendrix, R. W., Dedrick, R., Mitchell, K., Ko, C-C., Russell, D., ... Hatfull, G. F. (2013). Evolutionary Relationships among Actinophages and a Putative Adaptation for Growth in Streptomyces spp. Journal of Bacteriology, 195(21), 4924-4935. https://doi.org/10.1128/JB.00618-13

Evolutionary Relationships among Actinophages and a Putative Adaptation for Growth in Streptomyces spp. / Smith, Margaret C. M.; Hendrix, Roger W.; Dedrick, Rebekah; Mitchell, Kaitlin; Ko, Ching-Chung; Russell, Daniel; Bell, Emma; Gregory, Matthew; Bibb, Maureen J.; Pethick, Florence; Jacobs-Sera, Deborah; Herron, Paul; Buttner, Mark J.; Hatfull, Graham F.

In: Journal of Bacteriology, Vol. 195, No. 21, 11.2013, p. 4924-4935.

Research output: Contribution to journalArticle

Smith, MCM, Hendrix, RW, Dedrick, R, Mitchell, K, Ko, C-C, Russell, D, Bell, E, Gregory, M, Bibb, MJ, Pethick, F, Jacobs-Sera, D, Herron, P, Buttner, MJ & Hatfull, GF 2013, 'Evolutionary Relationships among Actinophages and a Putative Adaptation for Growth in Streptomyces spp.', Journal of Bacteriology, vol. 195, no. 21, pp. 4924-4935. https://doi.org/10.1128/JB.00618-13
Smith, Margaret C. M. ; Hendrix, Roger W. ; Dedrick, Rebekah ; Mitchell, Kaitlin ; Ko, Ching-Chung ; Russell, Daniel ; Bell, Emma ; Gregory, Matthew ; Bibb, Maureen J. ; Pethick, Florence ; Jacobs-Sera, Deborah ; Herron, Paul ; Buttner, Mark J. ; Hatfull, Graham F. / Evolutionary Relationships among Actinophages and a Putative Adaptation for Growth in Streptomyces spp. In: Journal of Bacteriology. 2013 ; Vol. 195, No. 21. pp. 4924-4935.
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abstract = "The genome sequences of eight Streptomyces phages are presented, four of which were isolated for this study. Phages R4, TG1, phi Hau3, and SV1 were isolated previously and have been exploited as tools for understanding and genetically manipulating Streptomyces spp. We also extracted five apparently intact prophages from recent Streptomyces spp. genome projects and, together with six phage genomes in the database, we analyzed all 19 Streptomyces phage genomes with a view to understanding their relationships to each other and to other actinophages, particularly the mycobacteriophages. Fifteen of the Streptomyces phages group into four clusters of related genomes. Although the R4-like phages do not share nucleotide sequence similarity with other phages, they clearly have common ancestry with cluster A mycobacteriophages, sharing many protein homologues, common gene syntenies, and similar repressor-stoperator regulatory systems. The R4-like phage phi Hau3 and the prophage StrepC.1 (from Streptomyces sp. strain C) appear to have hijacked a unique adaptation of the streptomycetes, i.e., use of the rare UUA codon, to control translation of the essential phage protein, the terminase. The Streptomyces venezuelae generalized transducing phage SV1 was used to predict the presence of other generalized transducing phages for different Streptomyces species.",
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note = "M.C.M.S. acknowledges funding from the Biotechnology and Biological Sciences Research Council (BBSRC) of the United Kingdom via project grants BB/H001212/1 and BB/H05447/1. Work in Pittsburgh was supported by NIH grants GM47795 to R.W.H. and GM093901 to G.F.H. Work in Norwich was funded by a MET Institute Strategic Programme grant to the John Innes Centre from the BBSRC. We are grateful to Charles A. Bowman for the construction of the Phamerator database and to John Atkins and Keith Chater for stimulating discussions on ribosome bypassing and UUA codons.",
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AU - Ko, Ching-Chung

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N2 - The genome sequences of eight Streptomyces phages are presented, four of which were isolated for this study. Phages R4, TG1, phi Hau3, and SV1 were isolated previously and have been exploited as tools for understanding and genetically manipulating Streptomyces spp. We also extracted five apparently intact prophages from recent Streptomyces spp. genome projects and, together with six phage genomes in the database, we analyzed all 19 Streptomyces phage genomes with a view to understanding their relationships to each other and to other actinophages, particularly the mycobacteriophages. Fifteen of the Streptomyces phages group into four clusters of related genomes. Although the R4-like phages do not share nucleotide sequence similarity with other phages, they clearly have common ancestry with cluster A mycobacteriophages, sharing many protein homologues, common gene syntenies, and similar repressor-stoperator regulatory systems. The R4-like phage phi Hau3 and the prophage StrepC.1 (from Streptomyces sp. strain C) appear to have hijacked a unique adaptation of the streptomycetes, i.e., use of the rare UUA codon, to control translation of the essential phage protein, the terminase. The Streptomyces venezuelae generalized transducing phage SV1 was used to predict the presence of other generalized transducing phages for different Streptomyces species.

AB - The genome sequences of eight Streptomyces phages are presented, four of which were isolated for this study. Phages R4, TG1, phi Hau3, and SV1 were isolated previously and have been exploited as tools for understanding and genetically manipulating Streptomyces spp. We also extracted five apparently intact prophages from recent Streptomyces spp. genome projects and, together with six phage genomes in the database, we analyzed all 19 Streptomyces phage genomes with a view to understanding their relationships to each other and to other actinophages, particularly the mycobacteriophages. Fifteen of the Streptomyces phages group into four clusters of related genomes. Although the R4-like phages do not share nucleotide sequence similarity with other phages, they clearly have common ancestry with cluster A mycobacteriophages, sharing many protein homologues, common gene syntenies, and similar repressor-stoperator regulatory systems. The R4-like phage phi Hau3 and the prophage StrepC.1 (from Streptomyces sp. strain C) appear to have hijacked a unique adaptation of the streptomycetes, i.e., use of the rare UUA codon, to control translation of the essential phage protein, the terminase. The Streptomyces venezuelae generalized transducing phage SV1 was used to predict the presence of other generalized transducing phages for different Streptomyces species.

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KW - bacteriophage PHI-C31

KW - nucleotide-sequence

KW - lytic development

KW - early region

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JO - Journal of Bacteriology

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