Genetic Insertions and Diversification of the PolB-Type DNA Polymerase (gp43) of T4-Related Phages

Petrov, V. M.; Ratnayaka, Swarnamala; Karam, J.D.

doi:10.1016/j.jmb.2009.10.054

Cited by 14 publications

(24 citation statements)

References 62 publications

(95 reference statements)

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“…Interestingly, the phage uEcoM-GJ1 was reported as the first member of a new genus in Myoviridae, which possesses a coliphage T7-like transcriptional system (RNA polymerase) and T1-like DNA-packaging system (large subunit terminase) [9]. In addition, a potential phylogenetic relationship between Aeromonas and enterobacteria phages was suggested by their genomic [5,[18][19][20] and morphological similarity [2]. Therefore, it can be assumed that PAS-1 might be genetically similar to phage uEcoM-GJ1, at least in DNA replication, packaging and transcription systems.…”

Section: Discussionmentioning

confidence: 99%

“…To date, a number of phages infecting Aeromonadaceae have been isolated and characterized [2,14,[19][20][21], and most of them were classified into Myoviridae in the VIIIth ICTV report (http://www.ictvdb.org/ Ictv/index.htm) as P1, P2 and T4-like phages [6]. Recent studies of Aeromonas phages have focused on virulent T4-like ones with extensive genomic investigations [5,14,18,19,23].…”

Section: Introductionmentioning

confidence: 99%

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Isolation and Characterization of a Lytic Myoviridae Bacteriophage PAS-1 with Broad Infectivity in Aeromonas salmonicida

et al. 2012

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To search for candidate control agents against Aeromonas salmonicida subsp. salmonicida infections in aquaculture, one bacteriophage (phage), designated as PAS-1, was isolated from the sediment samples of the rainbow trout (Oncorhynchus mykiss) culture farm in Korea. The PAS-1 was morphologically classified as Myoviridae and possessed approximately 48 kb of double-strand genomic DNA. The phage showed broad host ranges to other subspecies of A. salmonicida as well as A. salmonicida subsp. salmonicida including antibiotic-resistant strains. Its latent period and burst size were estimated to be approximately 40 min and 116.7 PFU/cell, respectively. Furthermore, genomic and structural proteomic analysis of PAS-1 revealed that the phage was closely related to other Myoviridae phages infecting enterobacteria or Aeromonas species. The bacteriolytic activity of phage PAS-1 was evaluated using three subspecies of A. salmonicida strain at different doses of multiplicity of infection, and the results proved to be efficient for the reduction of bacterial growth. Based on these results, PAS-1 could be considered as a novel Aeromonas phage and might have potentiality to reduce the impacts of A. salmonicida infections in aquaculture.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Isolation and Characterization of a Lytic Myoviridae Bacteriophage PAS-1 with Broad Infectivity in Aeromonas salmonicida

et al. 2012

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“…In one case, a GIY-YIG family endonuclease gene disrupts DNA polymerase (28,29); in the other case, a H-N-H family endonuclease gene disrupts the large subunit of ribonucleotide reductase (30). In all three cases, the products of the split genes reunite to form enzymatically active proteins.…”

Section: Origin Of the Bypassmentioning

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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“…In addition, shuffled genes would have to be compatible with new partners. Experimentally, there is some evidence indicating that the products of some Core genes, e.g., the DNA polymerase (gp43) and its accessory proteins (gp45 and gp44/62), can substitute for their diverged homologues in vivo [12,34-36]. Such observations suggest that the shuffling of Core Genome components between diverged T4 relatives can in some cases yield viable combinations.…”

Section: Introductionmentioning

confidence: 99%

“…There are at least three examples of freestanding HEGs in T4-related phages that are suspected to encode the homing enzymes for introns lacking HEGs of their own [36,55,65]. The natural existence of such HEGs raises the possibility that some homing enzymes can mediate the transposition of DNA that is distantly located from their own structural genes without necessarily co-transferring the HEG itself.…”

Section: Introductionmentioning

confidence: 99%

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

Petrov

Ratnayaka

Nolan

et al. 2010

Virol J

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155

185

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The T4-related bacteriophages are a group of bacterial viruses that share morphological similarities and genetic homologies with the well-studied Escherichia coli phage T4, but that diverge from T4 and each other by a number of genetically determined characteristics including the bacterial hosts they infect, the sizes of their linear double-stranded (ds) DNA genomes and the predicted compositions of their proteomes. The genomes of about 40 of these phages have been sequenced and annotated over the last several years and are compared here in the context of the factors that have determined their diversity and the diversity of other microbial genomes in evolution. The genomes of the T4 relatives analyzed so far range in size between ~160,000 and ~250,000 base pairs (bp) and are mosaics of one another, consisting of clusters of homology between them that are interspersed with segments that vary considerably in genetic composition between the different phage lineages. Based on the known biological and biochemical properties of phage T4 and the proteins encoded by the T4 genome, the T4 relatives reviewed here are predicted to share a genetic core, or "Core Genome" that determines the structural design of their dsDNA chromosomes, their distinctive morphology and the process of their assembly into infectious agents (phage morphogenesis). The Core Genome appears to be the most ancient genetic component of this phage group and constitutes a mere 12-15% of the total protein encoding potential of the typical T4-related phage genome. The high degree of genetic heterogeneity that exists outside of this shared core suggests that horizontal DNA transfer involving many genetic sources has played a major role in diversification of the T4-related phages and their spread to a wide spectrum of bacterial species domains in evolution. We discuss some of the factors and pathways that might have shaped the evolution of these phages and point out several parallels between their diversity and the diversity generally observed within all groups of interrelated dsDNA microbial genomes in nature.

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Genetic Insertions and Diversification of the PolB-Type DNA Polymerase (gp43) of T4-Related Phages

Cited by 14 publications

References 62 publications

Isolation and Characterization of a Lytic Myoviridae Bacteriophage PAS-1 with Broad Infectivity in Aeromonas salmonicida

Isolation and Characterization of a Lytic Myoviridae Bacteriophage PAS-1 with Broad Infectivity in Aeromonas salmonicida

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

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

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