Bacteriophage P2

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Escherichia virus P2
PhageP2.jpg
Virus classification Red Pencil Icon.png
(unranked): Virus
Realm: Duplodnaviria
Kingdom: Heunggongvirae
Phylum: Uroviricota
Class: Caudoviricetes
Order: Caudovirales
Family: Myoviridae
Genus: Peduovirus
Species:
Escherichia virus P2

Bacteriophage P2, scientific name Escherichia virus P2, [1] is a temperate phage that infects E. coli . It is a tailed virus with a contractile sheath and is thus classified in the genus Peduovirus (formerly P2likevirus), subfamily Peduovirinae , family Myoviridae within order Caudovirales . This genus of viruses includes many P2-like phages as well as the satellite phage P4. [2]

Contents

Discovery

Bacteriophage P2 was first isolated by G. Bertani from the Lisbonne and Carrère strain of E. coli in 1951. [3] Since that time, a large number of P2-like prophages (e.g. 186, HP1, HK239, and WΦ) have been isolated that shared characters such as host range, serological relatedness and inability to recombine with phage λ, and they seemed to be quite common in E. coli populations as about 30% of the strains in the E. coli reference collection (SABC) contain P2-like prophages . [4] Of these P2-like prophages is P2 best characterized. The P2 phage was found to be able to multiply in many strains of E. coli, as well as in strains of many other species including Serratia , Klebsiella pneumoniae , and Yersinia sp, [5] which suggested that it played an important role in horizontal gene transfer in bacterial evolution.

Genome and morphology

Phage P2 has a double stranded DNA genome packaged in an icosahedral capsid with a diameter of 60 nanometers that is connected to a 135 nanometer long tail. Presence of phage P4 can cause P2 to form smaller capsids. [6] The tail ends in a baseplate which is the control hub for phage infectivity. The baseplate includes 6 tail fibers which initially bind to receptors on the bacterial cell wall and a tail spike protein that subsequently binds irreversibly to other receptors on the cell wall.[ citation needed ]

The genome of bacteriophage P2 is 33,592 bp of double-stranded, linear DNA with cohesive ends (accession number AF063097). The 42 genes in the genome can be divided in three main categories: (i) genes required for lytic growth, (ii) genes involved in establishing and maintaining lysogeny (such as int and C), and (iii) the nonessential genes (including old, tin, and Z/fun). Furthermore, a number of open reading frames (ORFs) is found in P2 genome, which may encode functional proteins. [5]

Life cycle

Bacteriophage P2 is a temperate phage, which means that it can propagate lytically (i.e. directing the host cell to produce phage progenies and finally lysing the host when the phage progenies exit), as well as establish lysogeny (i.e. injecting and fusing its genetic material into the genome of the host without lysing the cell) and maintain as a prophage in host genome.[ citation needed ]

Infection

Adsorption of the virion to the host cell is the key step in phage infection, which is essential for the following phage binding and injection of phage DNA . During the adsorption process, the tail fiber of phage P2 recognizes and binds to the core region of the lipopolysaccharide of E. coli, and then the phage would inject its DNA into the cytoplasm. [5] [7]

Lytic cycle

Early transcription

The gene expression of P2 is regulated over time during the lytic cycle. Early transcription, which is responsible for the expression of the genes required for the following DNA replication, is initiated immediately after infection. The early operon contains 9 genes and transcribes from the lytic promotor Pe. The first gene in the operon, designated cox, encodes the repressor of the lysogenic promoter Pc and prevent the expression of the genes required for establishing lysogeny. [8] [9] Then the phage enters the lytic lifecycle and early transcription starts. Only host σ70 RNA polymerase is required in the early transcription process. [9]

DNA replication

Besides cox, the early operon contains two other genes which are essential for P2 DNA replication, genes A and B. [10] [11] Replication of P2 genome is initiated by A protein and takes place from a fixed origin (ori) via a modified rolling-circle mechanism that generates double-stranded monomeric circles. [12] [13] The B protein may be required for lagging-strand synthesis, as it can interact with E. coli DnaB and function as a helicase loader. [14]

Activation of late transcription

Late gene transcription is initiated from four late promoters once DNA replication has started and the transcriptional activator Ogr has been expressed. [15] [16] The late promoters, PP, PO, PV and PF, are activated by Ogr and direct the transcription of the genes responsible for lytic functions as well as encoding building blocks for phage progenies. [5] [17] [18] All the four promoters have a region with a partial dyad symmetry centered around 55 bp downstream from the transcriptional initiation site. Revealed by deletion analysis and base substitutions, this dyad symmetry has been shown to be essential for promoter activity. [9] [19] [20] Moreover, the late genes of P2 can also be activated by the δ proteins of satellite phages P4 and ΦR73 directly. [9] [21]

Lysis

During the lytic cycle, similar to other double-stranded phages, bacteriophage P2 applies a holin-endolysin system to lyse the host cell. P2 have two essential lysis genes (gene K and gene Y) and two ancillary lysis genes (lysA and lysB). [9] [22] The product of K gene has extensive amino acid sequence similarity to that of gene R in λ phage, which exhibits endolysin function and attack the glycosidic bond. Gene Y encodes a polypeptide sharing high similarity to the holin protein family, which forms ‘holes’ in the cell membrane and provide a pathway for endolysin escape to the cell wall. The nonessential genes, lysA and lysB, seem to play a role in controlling the correct timing of lysis. [23]

Lysogenic cycle

Prophage integration

During lysogenic cycle, P2 genome is inserted into the host chromosome and maintained as a prophage. The integration involves site-specific recombination between a bacterial attachment site (attB) and a phage attachment site (attP), which generates host-phage junctions, attL and attR. This reaction is controlled by a phage-encoded integrase, and leads to no gain or loss of nucleotides. [9] Another integration host factor, IHF, is also essential in the integration process and serves as an architectural protein that binds and bends DNA. [16] [24] Thus, the integration mechanism of phage P2 is similar to the well-studied λ site-specific recombination system, but the phage proteins and their DNA binding sites differ. [9] [25]

Maintenance of lysogeny

The lysogenic state of P2 is promoted and maintained by the C repressor. It is a 99-amino acids polypeptide and binds to only one operator region which regulates the expression of the early genes: cox, B and possibly A. Research has shown that C repressor can both positively and negatively regulate its own Pc promoter as Pc is up regulated at low C level and down regulated at high levels. [16] [26] Since the C repressor is not inactivated by the SOS/RecA system of E. coli, the P2 prophage is non-inducible by ultraviolet irradiation. Furthermore, even if C repressor is inactivated, the P2 prophage is unable to excise, due to lack of int expression. [5] [27] Hence, P2 has been regarded as the prototype for the non-inducible class of temperate phages. [9] The mechanism about how P2 solve the induction-excision paradox still remains unknown.[ citation needed ]

Control of lytic versus lysogenic growth

As stated before, upon infection, phage P2 can enter into either lytic or lysogenic cycle. The lytic/lysogenic decision upon infection depends on which promoter takes command, the lysogenic promoter Pc or the promoter Pe that controlled genes responsible for lytic cycle. [16] Pc and Pe are located face-to-face, and they are mutually exclusive. The Pe promotor directs transcription of the Cox protein that represses the Pc promoter and thereby prevents lysogenization, and the Pc promoter directs the C repressor transcription which down regulates Pe. [5] [26] [28] Thus, which promotor takes command is thought to be a consequence of the relative concentrations of the Cox protein and the C repressor. If the balance between the C repressor and Cox proteins is shifted towards C repressor after infection, then the phage will enter the lysogenic lifecycle as the Pe promoter will be turned off and vice versa. [16]

Evolution of bacteriophage P2 and other P2-like phages

Plenty of researches have shown that phage genomes are composed of both genes similar to host genes or other phage genes, and novel genes which show little similarity to any known genes. [9] [29] [30] P2-like phage family are no exception. Their genomes share a lot of similarity but each of them contain unique genes, including some ones which functions remain unknown. Based on the criterion suggested by Ackermann, many phages can be taxonomically classified as P2-like as they share some characters with phage P2, [31] but up to now, only 6 complete genomes are available (P2, 186, ΦCTX, HP1, HP2 and K139). [9]

Phylogenetic relationship of 6 sequenced P2-like phages

Revealed by whole genome comparison, only nine late genes (corresponding to genes H, L, M, N, O, P, Q, S, T in phage P2) and an integrase gene were found to be both genetically similar and present in all the 6 full sequenced genomes. Phylogenetic trees based on the amino acid sequences of the 9 late gene products are constructed separately, and they all show identical topology, which suggests that they may have the same evolutionary history. Furthermore, these 9 late genes are likely to be inherited clonally as there is no indication of major recombination events between them for any pair of phages. However, for remaining genes besides these nine, their phylogenetic relationship is often ambiguous and hard to resolve their evolutionary history. [9]

Homologous and non-homologous recombination

Homologous recombination plays a more important role in nucleotide changes of phage P2 than mutation, which is not surprising as P2-like prophages are prevalent in E. coli population and genetic exchange is found to occur between host genomes. [9] [32] Sequencing of five late genes from 18 isolates of P2-like phages demonstrated that homologous recombination is extensive and occurs randomly at multiple breakpoints. The genetic variations in the late genes of the 18 close relatives are small, as the greatest difference in any gene was only 3.7%. For there was much more variation in synonymous rather than nonsynonymous third-codon positions, these late genes are likely to be subject to rather strong stabilizing selection. [9] [33]

Besides homologous recombination between related phages, non-homologous recombination is also a key mechanism for phage evolution. The high level of similarities in the tail fiber genes of phage P2, P1, Mu, λ, K3 and T2, which belong to different families, indicates a previously unappreciated level of non-homologous recombination between unrelated phages. As host range of phage is largely determined by tail fiber, this finding suggests that under selective pressures, phages are likely to change their host range by making use of the gene pool available to them. [7] [9]

Contribution to the evolution of its host

Capable of switching between lytic and lysogenic lifecycle is greatly beneficial for the survival of phage. In a large dense population of isogenic hosts, the lytic strategy is preferred, and phage virulence as well as host defense mechanisms will evolve in an arms race manner. On the contrary, lysogeny is favored when the host cell density is not high enough for maintenance of the phage density by repeated cycles of lytic infections. [34]

It is well known that phage P2 has the potential to mediate horizontal gene transfer upon infection of different bacteria. During this process, phage P2 can serve as a source of new genes to the hosts, which provides materials for evolution and selection. Compared to evolution through mutation and selection, phage-mediated genetic changes can affect drastic alterations to bacterial metabolism and physiology within a short time, and they may confer fitness to their hosts. For example, Edlin et al. found that the lysogenic E. coli having a λ, P1, P2, or Mu prophage could grow more rapidly than a non-lysogenic counterpart under nutrient-limited condition. [35] [36] Furthermore, it was shown that P2 prophage may contribute to the dissemination of cytolethal distending toxins among E. coli O157 strains and facilitate their niche expansion among different animal hosts, which provides new insights into the pathogenesis of E. coli O157. [37]

Related Research Articles

<span class="mw-page-title-main">Bacteriophage</span> Virus that infects and replicates within bacteria

A bacteriophage, also known informally as a phage, is a duplodnaviria virus that infects and replicates within bacteria and archaea. The term was derived from "bacteria" and the Greek φαγεῖν, meaning "to devour". Bacteriophages are composed of proteins that encapsulate a DNA or RNA genome, and may have structures that are either simple or elaborate. Their genomes may encode as few as four genes and as many as hundreds of genes. Phages replicate within the bacterium following the injection of their genome into its cytoplasm.

<span class="mw-page-title-main">Lambda phage</span> Bacteriophage that infects Escherichia coli

Enterobacteria phage λ is a bacterial virus, or bacteriophage, that infects the bacterial species Escherichia coli. It was discovered by Esther Lederberg in 1950. The wild type of this virus has a temperate life cycle that allows it to either reside within the genome of its host through lysogeny or enter into a lytic phase, during which it kills and lyses the cell to produce offspring. Lambda strains, mutated at specific sites, are unable to lysogenize cells; instead, they grow and enter the lytic cycle after superinfecting an already lysogenized cell.

A provirus is a virus genome that is integrated into the DNA of a host cell. In the case of bacterial viruses (bacteriophages), proviruses are often referred to as prophages. However, proviruses are distinctly different from prophages and these terms should not be used interchangeably. Unlike prophages, proviruses do not excise themselves from the host genome when the host cell is stressed.

<span class="mw-page-title-main">Cloning vector</span>

A cloning vector is a small piece of DNA that can be stably maintained in an organism, and into which a foreign DNA fragment can be inserted for cloning purposes. The cloning vector may be DNA taken from a virus, the cell of a higher organism, or it may be the plasmid of a bacterium. The vector contains features that allow for the convenient insertion of a DNA fragment into the vector or its removal from the vector, for example through the presence of restriction sites. The vector and the foreign DNA may be treated with a restriction enzyme that cuts the DNA, and DNA fragments thus generated contain either blunt ends or overhangs known as sticky ends, and vector DNA and foreign DNA with compatible ends can then be joined together by molecular ligation. After a DNA fragment has been cloned into a cloning vector, it may be further subcloned into another vector designed for more specific use.

<span class="mw-page-title-main">Prophage</span>

A prophage is a bacteriophage genome that is integrated into the circular bacterial chromosome or exists as an extrachromosomal plasmid within the bacterial cell. Integration of prophages into the bacterial host is the characteristic step of the lysogenic cycle of temperate phages. Prophages remain latent in the genome through multiple cell divisions until activation by an external factor, such as UV light, leading to production of new phage particles that will lyse the cell and spread. As ubiquitous mobile genetic elements, prophages play important roles in bacterial genetics and evolution, such as in the acquisition of virulence factors.

<span class="mw-page-title-main">Transduction (genetics)</span> Transfer process in genetics

Transduction is the process by which foreign DNA is introduced into a cell by a virus or viral vector. An example is the viral transfer of DNA from one bacterium to another and hence an example of horizontal gene transfer. Transduction does not require physical contact between the cell donating the DNA and the cell receiving the DNA, and it is DNase resistant. Transduction is a common tool used by molecular biologists to stably introduce a foreign gene into a host cell's genome.

<span class="mw-page-title-main">Lytic cycle</span> Cycle of viral reproduction

The lytic cycle is one of the two cycles of viral reproduction, the other being the lysogenic cycle. The lytic cycle results in the destruction of the infected cell and its membrane. Bacteriophages that only use the lytic cycle are called virulent phages.

<i>Escherichia virus T4</i> Species of bacteriophase

Escherichia virus T4 is a species of bacteriophages that infect Escherichia coli bacteria. It is a double-stranded DNA virus in the subfamily Tevenvirinae from the family Myoviridae. T4 is capable of undergoing only a lytic lifecycle and not the lysogenic lifecycle. The species was formerly named T-even bacteriophage, a name which also encompasses, among other strains, Enterobacteria phage T2, Enterobacteria phage T4 and Enterobacteria phage T6.

In virology, temperate refers to the ability of some bacteriophages to display a lysogenic life cycle. Many temperate phages can integrate their genomes into their host bacterium's chromosome, together becoming a lysogen as the phage genome becomes a prophage. A temperate phage is also able to undergo a productive, typically lytic life cycle, where the prophage is expressed, replicates the phage genome, and produces phage progeny, which then leave the bacterium. With phage the term virulent is often used as an antonym to temperate, but more strictly a virulent phage is one that has lost its ability to display lysogeny through mutation rather than a phage lineage with no genetic potential to ever display lysogeny.

<span class="mw-page-title-main">Lysogenic cycle</span> Process of virus reproduction

Lysogeny, or the lysogenic cycle, is one of two cycles of viral reproduction. Lysogeny is characterized by integration of the bacteriophage nucleic acid into the host bacterium's genome or formation of a circular replicon in the bacterial cytoplasm. In this condition the bacterium continues to live and reproduce normally, while the bacteriophage lies in a dormant state in the host cell. The genetic material of the bacteriophage, called a prophage, can be transmitted to daughter cells at each subsequent cell division, and later events can release it, causing proliferation of new phages via the lytic cycle. Lysogenic cycles can also occur in eukaryotes, although the method of DNA incorporation is not fully understood. For instance the AIDS viruses can either infect humans lytically, or lay dormant (lysogenic) as part of the infected cells' genome, keeping the ability to return to lysis at a later time. The rest of this article is about lysogeny in bacterial hosts.

<span class="mw-page-title-main">T7 phage</span> Species of virus

Bacteriophage T7 is a bacteriophage, a virus that infects bacteria. It infects most strains of Escherichia coli and relies on these hosts to propagate. Bacteriophage T7 has a lytic life cycle, meaning that it destroys the cell it infects. It also possesses several properties that make it an ideal phage for experimentation: its purification and concentration have produced consistent values in chemical analyses; it can be rendered noninfectious by exposure to UV light; and it can be used in phage display to clone RNA binding proteins.

Salmonella virus P22 is a bacteriophage in the Podoviridae family that infects Salmonella typhimurium. Like many phages, it has been used in molecular biology to induce mutations in cultured bacteria and to introduce foreign genetic material. P22 has been used in generalized transduction and is an important tool for investigating Salmonella genetics.

P1 is a temperate bacteriophage that infects Escherichia coli and some other bacteria. When undergoing a lysogenic cycle the phage genome exists as a plasmid in the bacterium unlike other phages that integrate into the host DNA. P1 has an icosahedral head containing the DNA attached to a contractile tail with six tail fibers. The P1 phage has gained research interest because it can be used to transfer DNA from one bacterial cell to another in a process known as transduction. As it replicates during its lytic cycle it captures fragments of the host chromosome. If the resulting viral particles are used to infect a different host the captured DNA fragments can be integrated into the new host's genome. This method of in vivo genetic engineering was widely used for many years and is still used today, though to a lesser extent. P1 can also be used to create the P1-derived artificial chromosome cloning vector which can carry relatively large fragments of DNA. P1 encodes a site-specific recombinase, Cre, that is widely used to carry out cell-specific or time-specific DNA recombination by flanking the target DNA with loxP sites.

fis

fis is an E. coli gene encoding the Fis protein. The regulation of this gene is more complex than most other genes in the E. coli genome, as Fis is an important protein which regulates expression of other genes. It is supposed that fis is regulated by H-NS, IHF and CRP. It also regulates its own expression (autoregulation). Fis is one of the most abundant DNA binding proteins in Escherichia coli under nutrient-rich growth conditions.

A P1-derived artificial chromosome, or PAC, is a DNA construct derived from the DNA of P1 bacteriophages and Bacterial artificial chromosome. It can carry large amounts of other sequences for a variety of bioengineering purposes in bacteria. It is one type of the efficient cloning vector used to clone DNA fragments in Escherichia coli cells.

Zygotic induction occurs when a bacterial cell carrying the silenced DNA of a bacterial virus in its chromosome transfers the viral DNA along with its own DNA to another bacterial cell lacking the virus, causing the recipient of the DNA to break open. In the donor cell, a repressor protein encoded by the prophage keeps the viral genes turned off so that virus is not produced. When DNA is transferred to the recipient cell by conjugation, the viral genes in the transferred DNA are immediately turned on because the recipient cell lacks the repressor. As a result, many virus are made in the recipient cell, and lysis eventually occurs to release the new virus.

Escherichia virus 186 is a virus of the family Myoviridae, genus Eganvirus.

<span class="mw-page-title-main">CII protein</span> InterPro Family

cII or transcriptional activator II is a DNA-binding protein and important transcription factor in the life cycle of lambda phage. It is encoded in the lambda phage genome by the 291 base pair cII gene. cII plays a key role in determining whether the bacteriophage will incorporate its genome into its host and lie dormant (lysogeny), or replicate and kill the host (lysis).

Escherichia virus CC31, formerly known as Enterobacter virus CC31, is a dsDNA bacteriophage of the subfamily Tevenvirinae responsible for infecting the bacteria family of Enterobacteriaceae. It is one of two discovered viruses of the genus Karamvirus, diverging away from the previously discovered T4virus, as a clonal complex (CC). CC31 was first isolated from Escherichia coli B strain S/6/4 and is primarily associated with Escherichia, even though is named after Enterobacter.

The T7 expression system is used in the field of microbiology to clone recombinant DNA using strains of E. coli. It is the most popular system for expressing recombinant proteins in E. coli.

References

  1. ↑ "ICTV Taxonomy history: Escherichia virus P2". International Committee on Taxonomy of Viruses. Retrieved 2019-01-14.
  2. ↑ Bowden, DW; Modrich, P (Jun 10, 1985). "In vitro maturation of circular bacteriophage P2 DNA. Purification of ter components and characterization of the reaction". The Journal of Biological Chemistry. 260 (11): 6999–7007. doi: 10.1016/S0021-9258(18)88879-2 . PMID   2987239.
  3. ↑ Bertani, G., STUDIES ON LYSOGENESIS I.: The Mode of Phage Liberation by Lysogenic Escherichia coli1. Journal of Bacteriology, 1951. 62(3): p. 293.
  4. ↑ Nilsson, A.S., J.L. Karlsson, and E. Haggård-Ljungquist, Site-specific recombination links the evolution of P2-like coliphages and pathogenic enterobacteria. Molecular Biology and Evolution, 2004. 21(1): p. 1-13.
  5. 1 2 3 4 5 6 Haggård-Ljungquist, E., C. Halling, and R. Calendar, DNA sequences of the tail fiber genes of bacteriophage P2: evidence for horizontal transfer of tail fiber genes among unrelated bacteriophages. Journal of Bacteriology, 1992. 174(5): p. 1462-1477.
  6. ↑ Dearborn, AD; Laurinmaki, P; Chandramouli, P; Rodenburg, CM; Wang, S; Butcher, SJ; Dokland, T (Apr 9, 2012). "Structure and size determination of bacteriophage P2 and P4 procapsids: Function of size responsiveness mutations". Journal of Structural Biology. 178 (3): 215–24. doi:10.1016/j.jsb.2012.04.002. PMC   3361666 . PMID   22508104.
  7. 1 2 Haggård-Ljungquist, E., C. Halling, and R. Calendar, DNA sequences of the tail fiber genes of bacteriophage P2: evidence for horizontal transfer of tail fiber genes among unrelated bacteriophages. Journal of Bacteriology, 1992. 174(5): p. 1462-1477.
  8. ↑ Saha, S., E. Haggård-Ljungquist, and K. Nordström, The cox protein of bacteriophage P2 inhibits the formation of the repressor protein and autoregulates the early operon. The EMBO Journal, 1987. 6(10): p. 3191.
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  16. 1 2 3 4 5 Mandali, S., Site-specific recombination of P2-like phages; possible tools for safe gene therapy: A focus on phage ΦD145. 2010.
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  20. ↑ Van Bokkelen, G., et al., Mutational analysis of a bacteriophage P4 late promoter. Journal of Bacteriology, 1991. 173(1): p. 37-45.
  21. ↑ Clerch, B., E. Rivera, and M. Llagostera, Bacteriophage PSP3 and phi R73 activator proteins: analysis of promoter specificities. Journal of Bacteriology, 1996. 178(19): p. 5568-5572.
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  25. ↑ Landy, A., Dynamic, structural, and regulatory aspects of lambda site-specific recombination. Annual Review of Biochemistry, 1989. 58(1): p. 913-941.
  26. 1 2 Saha, S., B. Lundqvist, and E. Haggård-Ljungquist, Autoregulation of bacteriophage P2 repressor. The EMBO Journal, 1987. 6(3): p. 809.
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  32. ↑ Feil, E.J., et al., Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proceedings of the National Academy of Sciences, 2001. 98(1): p. 182-187.
  33. ↑ Nilsson, A.S. and E. Haggård-Ljungquist, Detection of homologous recombination among bacteriophage P2 relatives. Molecular Phylogenetics and Evolution, 2001. 21(2): p. 259-269.
  34. ↑ Nilsson, A.S. and E. Haggård-Ljungquist, Evolution of P2-like phages and their impact on bacterial evolution. Research in Microbiology, 2007. 158(4): p. 311-317.
  35. ↑ Edlin, G., L. Lin, and R. Kudrna, λ Lysogens of E. coli reproduce more rapidly than non-lysogens. 1975.
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  37. ↑ Svab, D., et al., Sequence variability of P2-like prophage genomes carrying the cytolethal distending toxin V operon in Escherichia coli O157. Appl Environ Microbiol, 2013. 79(16): p. 4958-64.

2. Bertani, G., STUDIES ON LYSOGENESIS I.: The Mode of Phage Liberation by Lysogenic Escherichia coli1. Journal of Bacteriology, 1951. 62(3): p. 293.

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