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

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, 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 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

Fingerprint

Streptomyces
Bacteriophages
Growth
Genome
Mycobacteriophages
Prophages
Codon
Proteins
Databases

Keywords

  • adaptation, physiological
  • amino acid sequence
  • bacteriophages
  • base sequence
  • biological evolution
  • gene expression regulation, viral
  • genome, viral
  • molecular sequence data
  • prophages
  • species specificity
  • streptomyces
  • viral proteins

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
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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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

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

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AU - Ko, Ching-Chung

AU - Russell, Daniel

AU - Bell, Emma

AU - Gregory, Matthew

AU - Bibb, Maureen J

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AU - Buttner, Mark J

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AB - The genome sequences of eight Streptomyces phages are presented, four of which were isolated for this study. Phages R4, TG1, 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 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 - amino acid sequence

KW - bacteriophages

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KW - species specificity

KW - streptomyces

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