Genomes of the T4-related bacteriophages as windows on microbial genome evolution

Petrov, V. M.; Ratnayaka, Swarnamala; Nolan, Justin M.; Miller, Eric S.; Karam, J.D.

doi:10.1186/1743-422x-7-292

Cited by 156 publications

(199 citation statements)

References 68 publications

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“…† After this work was completed, the phage T4 genomic sequence was redetermined (accession no. HM_137666) with mobA sequence identical to that presented here (11). The inaccuracies in accession NC_000866 were undoubtedly due to the common practice at that time of cloning genes in unregulated plasmids before sequencing.…”

Section: Resultsmentioning

confidence: 99%

A homing endonuclease and the 50-nt ribosomal bypass sequence of phage T4 constitute a mobile DNA cassette

Bonocora

Zeng

Abel

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Since its initial description more than two decades ago, the ribosome bypass (or "hop") sequence of phage T4 stands out as a uniquely extreme example of programmed translational frameshifting. The gene for a DNA topoisomerase subunit of T4 has been split by a 1-kb insertion into two genes that retain topoisomerase function. A second 50-nt insertion, beginning with an inphase stop codon, is inserted near the start of the newly created downstream gene 60. Instead of terminating at this stop codon, approximately half of the ribosomes skip 50 nucleotides and continue translation in a new reading frame. However, no functions, regulatory or otherwise, have been imputed for the truncated peptide that results from termination at codon 46 or for the bypass sequence itself. Moreover, how this unusual mRNA organization arose and why it is maintained have never been explained. We show here that a homing endonuclease (MobA) is encoded in the insertion that created gene 60, and the mobA gene together with the bypass sequence constitute a mobile DNA cassette. The bypass sequence provides protection against self-cleavage by the nuclease, whereas the nuclease promotes horizontal spread of the entire cassette to related bacteriophages. Group I introns frequently provide protection against self-cleavage by associated homing endonucleases. We present a scenario by which the bypass sequence, which is otherwise a unique genetic element, might have been derived from a degenerate group I intron. bacteriophage gene structure | group I intron | horizontal gene transfer | ribosomal frameshifting | mobile genetic element I n most of the phages of the T4 superfamily, the large subunit of DNA topoisomerase is a single polypeptide encoded by gene 39. However, in phage T4 this gene is disrupted by a 1-kb insertion, creating a truncated gene 39 plus a new gene (gene 60) that encodes the remainder of the topoisomerase subunit (1, 2) ( Fig. 1). Furthermore, the C terminus of the truncated gene 39 and the N terminus of the newly created gene 60 each contain additional amino acid residues (43 and 30, respectively) that were not present in the original gene 39 homologs. These two independently translated proteins interact with the small subunit (encoded by gene 52) to create an enzymatically active topoisomerase (4). A second, 50-nt insertion beginning with an inphase stop codon, is inserted into the newly created downstream gene 60 (2). Instead of terminating at this stop codon, approximately half of the ribosomes skip 50 nucleotides and continue translation in a new reading frame (5). Features involved in this remarkable process include: the stop codon, the codon at which translation resumes, a portion of the pre-hop nascent peptide, a stem-loop at the start of the bypassed sequence, a Shine/Dalgarno-like sequence within the bypassed RNA, and the structure of the bypassed mRNA (5-8).The genome sequence of phage T4 (GenBank accession no. NC_000866) indicated that the insertion into gene 39 contains two ORFs: an apparent H-N-H homing endonuclease ps...

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Section: Resultsmentioning

confidence: 99%

A homing endonuclease and the 50-nt ribosomal bypass sequence of phage T4 constitute a mobile DNA cassette

Bonocora

Zeng

Abel

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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“…S2). In fact, class I RNRs are part of the "core genome" among T4-like phages (38) and likely play a vital role in T4-like phage biology, which may explain the constrained RNR diversity observed in these phages ( Fig. 2A).…”

Section: Discussionmentioning

confidence: 99%

Ribonucleotide reductases reveal novel viral diversity and predict biological and ecological features of unknown marine viruses

Sakowski¹,

Munsell²,

Hyatt³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Virioplankton play a crucial role in aquatic ecosystems as topdown regulators of bacterial populations and agents of horizontal gene transfer and nutrient cycling. However, the biology and ecology of virioplankton populations in the environment remain poorly understood. Ribonucleotide reductases (RNRs) are ancient enzymes that reduce ribonucleotides to deoxyribonucleotides and thus prime DNA synthesis. Composed of three classes according to O 2 reactivity, RNRs can be predictive of the physiological conditions surrounding DNA synthesis. RNRs are universal among cellular life, common within viral genomes and virioplankton shotgun metagenomes (viromes), and estimated to occur within >90% of the dsDNA virioplankton sampled in this study. RNRs occur across diverse viral groups, including all three morphological families of tailed phages, making these genes attractive for studies of viral diversity. Differing patterns in virioplankton diversity were clear from RNRs sampled across a broad oceanic transect. The most abundant RNRs belonged to novel lineages of podoviruses infecting α-proteobacteria, a bacterial class critical to oceanic carbon cycling. RNR class was predictive of phage morphology among cyanophages and RNR distribution frequencies among cyanophages were largely consistent with the predictions of the "kill the winner-cost of resistance" model. RNRs were also identified for the first time to our knowledge within ssDNA viromes. These data indicate that RNR polymorphism provides a means of connecting the biological and ecological features of virioplankton populations. viral ecology | viral evolution | phage replication

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“…As a consequence, the genome sequence of only five Campylobacter phages have been reported so far Hammerl et al, 2011;Kropinski et al, 2011;Timms et al, 2010). Interestingly, the phage genomes known are all related and also part of the T4 superfamily of phages (Petrov et al, 2010).…”

Section: Campylobactermentioning

confidence: 99%

Phages as Therapeutic Tools to Control Major Foodborne Pathogens: Campylobacter and Salmonella

Carvalho¹,

Santos²,

Kropinski³

et al. 2012

Bacteriophages

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Genomes of the T4-related bacteriophages as windows on microbial genome evolution

Cited by 156 publications

References 68 publications

A homing endonuclease and the 50-nt ribosomal bypass sequence of phage T4 constitute a mobile DNA cassette

A homing endonuclease and the 50-nt ribosomal bypass sequence of phage T4 constitute a mobile DNA cassette

Ribonucleotide reductases reveal novel viral diversity and predict biological and ecological features of unknown marine viruses

Phages as Therapeutic Tools to Control Major Foodborne Pathogens: Campylobacter and Salmonella

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