Comparative analysis of bacterial viruses Bam35, infecting a gram-positive host, and PRD1, infecting gram-negative hosts, demonstrates a viral lineage

Ravantti, Janne J.; Gaidelyte, Ausra; Bamford, Dennis H.; Bamford, Jaana K. H.

doi:10.1016/s0042-6822(03)00295-2

Cited by 72 publications

(103 citation statements)

References 61 publications

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“…Although representatives of the two groups are extremely similar to each other structurally (1,157), their genomes share virtually no sequence conservation; only four proteins of Bam35 could be linked to those of PRD1 by use of bioinformatic methods (227). Within the groups, however, the genomes are highly similar.…”

Section: Tectiviridaementioning

confidence: 99%

Genomics of Bacterial and Archaeal Viruses: Dynamics within the Prokaryotic Virosphere

Krupovìč

Prangishvili

Hendrix

et al. 2011

Microbiol Mol Biol Rev

218

176

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SUMMARY Prokaryotes, bacteria and archaea, are the most abundant cellular organisms among those sharing the planet Earth with human beings (among others). However, numerous ecological studies have revealed that it is actually prokaryotic viruses that predominate on our planet and outnumber their hosts by at least an order of magnitude. An understanding of how this viral domain is organized and what are the mechanisms governing its evolution is therefore of great interest and importance. The vast majority of characterized prokaryotic viruses belong to the order Caudovirales, double-stranded DNA (dsDNA) bacteriophages with tails. Consequently, these viruses have been studied (and reviewed) extensively from both genomic and functional perspectives. However, albeit numerous, tailed phages represent only a minor fraction of the prokaryotic virus diversity. Therefore, the knowledge which has been generated for this viral system does not offer a comprehensive view of the prokaryotic virosphere. In this review, we discuss all families of bacterial and archaeal viruses that contain more than one characterized member and for which evolutionary conclusions can be attempted by use of comparative genomic analysis. We focus on the molecular mechanisms of their genome evolution as well as on the relationships between different viral groups and plasmids. It becomes clear that evolutionary mechanisms shaping the genomes of prokaryotic viruses vary between different families and depend on the type of the nucleic acid, characteristics of the virion structure, as well as the mode of the life cycle. We also point out that horizontal gene transfer is not equally prevalent in different virus families and is not uniformly unrestricted for diverse viral functions.

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Section: Tectiviridaementioning

confidence: 99%

Genomics of Bacterial and Archaeal Viruses: Dynamics within the Prokaryotic Virosphere

Krupovìč

Prangishvili

Hendrix

et al. 2011

Microbiol Mol Biol Rev

218

176

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“…Φ29, along with other protein-primed genome replication phages, such as PRD1 or Cp-1 (28, 29), can undergo a lytic cycle only after infection of the host cell occurs. In contrast, phage Bam35, which infects Bacillus thuringiensis and related tectiviruses infecting Bacillus cereus sensu lato group (30,31), are temperate viruses that can self-replicate as linear episomes within lysogenic cells.In this work, we describe the biochemical properties of Bam35 DNA polymerase (B35DNAP) as a faithful, processive DNAP endowed with intrinsic strand displacement activity. Surprisingly, we also found that, despite its high fidelity, it can elude to some Significance Functional classification of DNA polymerases (DNAPs) usually divides them into replicative faithful replicases and error-prone enzymes devoted to DNA repair and DNA damage tolerance through translesion synthesis (TLS).…”

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confidence: 99%

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confidence: 99%

DNA polymerase from temperate phage Bam35 is endowed with processive polymerization and abasic sites translesion synthesis capacity

Berjón-Otero

Villar

Vega

et al. 2015

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

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DNA polymerases (DNAPs) responsible for genome replication are highly faithful enzymes that nonetheless cannot deal with damaged DNA. In contrast, translesion synthesis (TLS) DNAPs are suitable for replicating modified template bases, although resulting in very lowfidelity products. Here we report the biochemical characterization of the temperate bacteriophage Bam35 DNA polymerase (B35DNAP), which belongs to the protein-primed subgroup of family B DNAPs, along with phage Φ29 and other viral and mobile element polymerases. B35DNAP is a highly faithful DNAP that can couple strand displacement to processive DNA synthesis. These properties allow it to perform multiple displacement amplification of plasmid DNA with a very low error rate. Despite its fidelity and proofreading activity, B35DNAP was able to successfully perform abasic site TLS without template realignment and inserting preferably an A opposite the abasic site (A rule). Moreover, deletion of the TPR2 subdomain, required for processivity, impaired primer extension beyond the abasic site. Taken together, these findings suggest that B35DNAP may perform faithful and processive genome replication in vivo and, when required, TLS of abasic sites.protein-primed DNA polymerase | Bam35 | abasic sites | translesion synthesis | isothermal DNA amplification R eplicative DNA polymerases (DNAPs) from A and B families, collectively termed replicases, exhibit a "tight fit" for their DNA and dNTP substrates and are wondrously adapted to form correct Watson-Crick base pairs, resulting in very pronounced fidelity (1, 2). This strict preference to produce A:T and G:C base pairs is also the Achilles heel of faithful DNA polymerases, however, because they are strongly inhibited by modified nucleotides present at sites of DNA damage, leading to the stalling of replication fork and eventually to replicative stress and cell death (3). At the stalled replication fork, the DNA polymerase may be exchanged by a translesion synthesis (TLS) polymerase, generally belonging to the Y family. These enzymes possess looser solventexposed active sites, which allows them to deal with aberrant DNA features much better, although with a very low polymerization accuracy with the risk of the accumulation of mutations and genetic instability (4, 5). Alternatively, nonbulky modified bases, such as uracil and 8-oxo-deoxyguanosine (8oxoG), can be bypassed by replicases, with faithful or mutagenic outcomes that can be modified by the sequence context and dNTP availability (6, 7).Abasic or apurinic/apyrimidinic (AP) sites are the most common DNA lesions arising in cells when the N-glycosydic bond between the sugar moiety and the nucleobase is broken, either spontaneously or by a DNA glycosylase reaction product in the base excision repair pathway (8, 9). Unrepaired abasic sites are highly blocking lesions for replicative DNA polymerases (10), although mutant polymerases with impaired proofreading activity or with mutations in the polymerization active site residues that affect the incoming nucleotide sel...

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“…These plasmids encode the phage receptor but are not otherwise involved in the virus life cycle (22). Five other PRD1-like viruses have been isolated from different parts of the world (PR3 [5], PR4 [26], PR5 [30], PR772 [8], and L17 [4]), and it has been shown that their genomic sequences share approximately 98% identity (21).…”

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confidence: 99%

“…The bacteriophages AP50 and NS11, isolated from Bacillus anthracis (19) and Bacillus acidocaldarius (23,24), respectively, have only been morphologically characterized. Bam35 was isolated from B. thuringiensis serovar Alesti in 1978 (1) and was recently sequenced (21), revealing that it differs from GIL01 by 11 bp. A previous distribution analysis of similar prophages among the B. cereus group had unveiled the presence of a GIL01-related molecule in B. thuringiensis strain B16.…”

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confidence: 99%

GIL16, a New Gram-Positive Tectiviral Phage Related to theBacillus thuringiensisGIL01 and theBacillus cereuspBClin15 Elements

2005

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One of the most notable characteristics of Tectiviridae resides in their double-layer coats: the doublestranded DNA is located within a flexible lipoprotein vesicle covered by a rigid protein capsid. Despite their apparent rarity, tectiviruses have an extremely wide distribution compared to other phage groups. Members of this family have been found to infect gram-negative (PRD1 and relatives) as well as gram-positive (Bam35, GIL01, AP50, and NS11) hosts. Several reports have shown that tectiviruses infecting gram-negative bacteria are closely related, whereas no information is currently available on the genetic relationship among those infecting gram-positive bacteria. The present study reports the sequence of GIL16, a new isolate originating from Bacillus thuringiensis, and a genetic comparison of this isolate with the tectiviral bacteriophages Bam35 and GIL01, which originated from B. thuringiensis serovars Alesti and Israelensis, respectively. In contrast to PRD1 and its relatives, these are temperate bacteriophages existing as autonomous linear prophages within the host cell. Mutations in a particular motif in both the GIL01 and GIL16 phages are also shown to correlate with a switch to the lytic cycle. Interestingly, both bacterial viruses displayed narrow, yet slightly different, host spectrums. We also explore the hypothesis that pBClin15, a linear plasmid hosted by the Bacillus cereus reference strain ATCC 14579, is also a prophage. Sequencing of its inverted repeats at both extremities and a comparison with GIL01 and GIL16 emphasize its relationship to the Tectiviridae.The bacteriophage GIL01 has a linear double-stranded DNA genome of 14,931 bp delineated by imperfect 73-bp inverted repeats and protected by proteins at its 5Ј ends. GIL01 is a temperate bacteriophage that was isolated from Bacillus thuringiensis serovar Israelensis whose prophage form, designated pGIL01, resides in the host cell as an autonomous linear plasmid without any apparent integration into the host chromosome. It has been suggested that GIL01 belongs to the family Tectiviridae (28), whose members are characterized by the presence of an internal lipid membrane. While tectiviruses infecting gram-negative bacteria have been extensively studied at the genetic level, those infecting gram-positive bacteria remain less well characterized. PRD1, for instance, is the family model and infects bacteria harboring conjugative plasmids of the P, N, or W incompatibility groups, such as Escherichia coli and Salmonella enterica. These plasmids encode the phage receptor but are not otherwise involved in the virus life cycle In addition to GIL01, three other tectiviruses that infect gram-positive bacteria have been identified so far. The bacteriophages AP50 and NS11, isolated from Bacillus anthracis (19) and Bacillus acidocaldarius (23, 24), respectively, have only been morphologically characterized. Bam35 was isolated from B. thuringiensis serovar Alesti in 1978 (1) and was recently sequenced (21), revealing that it differs from GIL01 by 11 bp. A p...

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Comparative analysis of bacterial viruses Bam35, infecting a gram-positive host, and PRD1, infecting gram-negative hosts, demonstrates a viral lineage

Cited by 72 publications

References 61 publications

Genomics of Bacterial and Archaeal Viruses: Dynamics within the Prokaryotic Virosphere

Genomics of Bacterial and Archaeal Viruses: Dynamics within the Prokaryotic Virosphere

DNA polymerase from temperate phage Bam35 is endowed with processive polymerization and abasic sites translesion synthesis capacity

GIL16, a New Gram-Positive Tectiviral Phage Related to theBacillus thuringiensisGIL01 and theBacillus cereuspBClin15 Elements

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