Discovery of Cyanophage Genomes Which Contain Mitochondrial DNA Polymerase

Chan, Yi‐Wah; Mohr, Remus; Millard, Andrew; Holmes, Antony B.; Larkum, Anthony W. D.; Whitworth, Anna L.; Mann, Nicholas H.; Scanlan, David J.; Hess, Wolfgang R.; Clokie, Martha R. J.

doi:10.1093/molbev/msr041

Cited by 18 publications

(27 citation statements)

References 19 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Filee et al (34) previously hypothesized that it was of bacteriophage origin on the basis of weak bootstrap support for clustering with T7-like DNA polymerases. Our findings, together with those of Chan et al (35), provide strong evidence for the bacteriophage origin of the mitochondrial DNA polymerase gene. However, our analysis indicates that this is likely to have been a phage ancestral to either or both the TIM5-like myoviruses and the Acaryochloris siphoviruses, rather than to T7-like podoviruses.…”

Section: Discussionsupporting

confidence: 86%

See 1 more Smart Citation

A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans

Sabehi

Shaulov

Silver

et al. 2012

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

104

128

View full text Add to dashboard Cite

Viruses infecting bacteria (phages) are thought to greatly impact microbial population dynamics as well as the genome diversity and evolution of their hosts. Here we report on the discovery of a novel lineage of tailed dsDNA phages belonging to the family Myoviridae and describe its first representative, S-TIM5, that infects the ubiquitous marine cyanobacterium, Synechococcus. The genome of this phage encodes an entirely unique set of structural proteins not found in any currently known phage, indicating that it uses lineage-specific genes for virion morphogenesis and represents a previously unknown lineage of myoviruses. Furthermore, among its distinctive collection of replication and DNA metabolism genes, it carries a mitochondrial-like DNA polymerase gene, providing strong evidence for the bacteriophage origin of the mitochondrial DNA polymerase. S-TIM5 also encodes an array of bacterial-like metabolism genes commonly found in phages infecting cyanobacteria including photosynthesis, carbon metabolism and phosphorus acquisition genes. This suggests a common gene pool and gene swapping of cyanophage-specific genes among different phage lineages despite distinct sets of structural and replication genes. All cytosines following purine nucleotides are methylated in the S-TIM5 genome, constituting a unique methylation pattern that likely protects the genome from nuclease degradation. This phage is abundant in the Red Sea and S-TIM5 gene homologs are widespread in the oceans. This unusual phage type is thus likely to be an important player in the oceans, impacting the population dynamics and evolution of their primary producing cyanobacterial hosts.

show abstract

Section: Discussionsupporting

confidence: 86%

“…Chan et al (35) suggested that environmental sequences clustering phylogenetically with mitochondrial and Acaryochloris siphovirus DNA polymerase sequences may come from a phage or the bacterial ancestor of the mitochondria. These sequences cluster with S-TIM5 and have amino acid identities of 45-98% to that of S-TIM5 (Table S4).…”

Section: Discussionmentioning

confidence: 99%

A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans

Sabehi

Shaulov

Silver

et al. 2012

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

104

128

View full text Add to dashboard Cite

show abstract

“…Eukaryotic mitochondrial polA polymerases, which are thought to have been phage derived (37), are known from crystal structure analysis (38) to have large thumb domain inserts. The phages most similar to mitochondrial polA polymerases, A-HIS1 and -2 and S-TIM5 (39,40), also have insertions in that position. Not all phage clades had thumb inserts.…”

Section: Resultsmentioning

confidence: 99%

“…DNA pol. ), in parentheses, were not included in the tree-making computation but are marked on the figure in the position previously determined (39). Each phage is labeled as to family (p, podovirus; s, siphovirus; m, myovirus) either individually or on a branch leading to a group.…”

Section: Resultsmentioning

confidence: 99%

Morphology, Physiological Characteristics, and Complete Sequence of Marine Bacteriophage ϕRIO-1 Infecting Pseudoalteromonas marina

Hardies

Hwang

et al. 2013

J Virol

View full text Add to dashboard Cite

c Bacteria of the genus Pseudoalteromonas are ubiquitous in the world's oceans. Marine bacteria have been posited to be associated with a major ancient branch of podoviruses related to T7. Yet, although Pseudoalteromonas phages belonging to the Corticoviridae and the Siphoviridae and prophages belonging to the Myoviridae have been reported, no Pseudoalteromonas podovirus was previously known. Here, a new lytic Pseudoalteromonas marina phage, RIO-1, belonging to the Podoviridae was isolated and characterized with respect to morphology, genomic sequence, and biological properties. Its major encoded proteins were distantly similar to those of T7. The most similar previously sequenced viruses were Pseudomonas phage PA11 and Salinivibrio phage CW02. Whereas many elements of the morphology and gene organization of RIO-1 are similar to those of podoviruses broadly related to T7, RIO-1 conspicuously lacked an RNA polymerase gene. Since definitions of a T7 supergroup have included similarity in the DNA polymerase gene, a detailed phylogenetic analysis was conducted, and two major DNA polymerase clades in Autographivirinae and several structural variants of the polA family represented in podoviruses were found. RIO-1 carries an operon similar to that in a few other podoviruses predicted to specify activities related to ␥-glutamyl amide linkages and/or unusual peptide bonds. Most growth properties of RIO-1 were typical of T7-like phages, except for a long latent period.V iral particles outnumber bacteria in the world's oceans by a factor of about 10:1 and are thought to enforce diversity at the base of the microbiological community by restraining overgrowth of any particularly successful microbial species and returning their biomolecules as nutrients into the water through lysis (1, 2). This role rests critically on a network of specific host-virus interactions. Estimates of viral diversity by metagenomics tend to indicate extraordinarily high numbers of viral species (3-5), yet the total number of sequenced marine bacteriophages as of the last published count (6) was only 17. Current marine phage sequencing initiatives are expected to raise this to only a few hundred.Two of the earliest marine phages genomically characterized were the podoviruses roseophage SIO1 (7) and vibriophage VpV262 (8). These exemplify a group of podoviruses that are vaguely similar to enterobacterial phage T7 but lack the singlechain RNA polymerase and have two converging transcription units rather than one unidirectional transcription unit. It was postulated that this description represented an ancestral phage type present in ancient oceans and widespread descendants would be found in oceanic bacterial species.Pseudoalteromonas is a genus of gammaproteobacteria with many species, all found in marine environments. The genus contains specialists for various marine habitats ranging from sea ice (9) to deep-sea sediments (10). Its species are divided into pigmented and nonpigmented species; the former are known for habitation of marine biofilms and p...

show abstract

“…Relationship with DNA polymerase g Recent studies have reported that genes with homology to mitochondrial DNA polymerase g are abundant within the virioplankton have been found in cyanophage genomes and the Global Ocean Survey data set (Chan et al, 2011;. To determine the prevalence of these polymerases in our metagenomic libraries the VIROME databank was queried with the set of S15 DNA pol g sequences from the mitochondria, cyanophage and the Global Ocean Survey Yooseph et al, 2007) and BroadPhage (John et al, 2011) data sets (BLASTP E-score p10 À 10 ).…”

Section: Discussionmentioning

confidence: 99%

Shotgun metagenomics indicates novel family A DNA polymerases predominate within marine virioplankton

et al. 2013

View full text Add to dashboard Cite

Virioplankton have a significant role in marine ecosystems, yet we know little of the predominant biological characteristics of aquatic viruses that influence the flow of nutrients and energy through microbial communities. Family A DNA polymerases, critical to DNA replication and repair in prokaryotes, are found in many tailed bacteriophages. The essential role of DNA polymerase in viral replication makes it a useful target for connecting viral diversity with an important biological feature of viruses. Capturing the full diversity of this polymorphic gene by targeted approaches has been difficult; thus, full-length DNA polymerase genes were assembled out of virioplankton shotgun metagenomic sequence libraries (viromes). Within the viromes novel DNA polymerases were common and found in both double-stranded (ds) DNA and single-stranded (ss) DNA libraries. Finding DNA polymerase genes in ssDNA viral libraries was unexpected, as no such genes have been previously reported from ssDNA phage. Surprisingly, the most common virioplankton DNA polymerases were related to a siphovirus infecting an a-proteobacterial symbiont of a marine sponge and not the podoviral T7-like polymerases seen in many other studies. Amino acids predictive of catalytic efficiency and fidelity linked perfectly to the environmental clades, indicating that most DNA polymerase-carrying virioplankton utilize a lower efficiency, higher fidelity enzyme. Comparisons with previously reported, PCR-amplified DNA polymerase sequences indicated that the most common virioplankton metagenomic DNA polymerases formed a new group that included siphoviruses. These data indicate that slower-replicating, lytic or lysogenic phage populations rather than fast-replicating, highly lytic phages may predominate within the virioplankton.

show abstract

Discovery of Cyanophage Genomes Which Contain Mitochondrial DNA Polymerase

Cited by 18 publications

References 19 publications

A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans

A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans

Morphology, Physiological Characteristics, and Complete Sequence of Marine Bacteriophage ϕRIO-1 Infecting Pseudoalteromonas marina

Shotgun metagenomics indicates novel family A DNA polymerases predominate within marine virioplankton

Contact Info

Product

Resources

About