As a service to our customers we are providing this early version of the manuscript. 162, 14411446 (2017). Biol. Fabry, C. M. S. et al. A theoretical analysis of how strain-specific viruses can control microbial species diversity. Environ. 184, 48914905 (2002). This Review presents phage genomic diversity with a main focus on tailed dsDNA phages and an overview of the other phage families. Nat. Mol. Phages not only carry genes that counteract host protection systems such as anti-restriction [43], and RNA repair enzymes [44], but also can provide genes that offer protection from other viruses. Krupovic, M., Prangishvili, D., Hendrix, R. W. & Bamford, D. H. Genomics of bacterial and archaeal viruses: dynamics within the Prokaryotic virosphere. 50 years of the International Committee on Taxonomy of Viruses: progress and prospects. Bacteriophage T4, with a genome of 166 kbp, is the best-known of all the T phages. Genome Size The authors declare no competing interests. 84, 117 (2018). Microbiol. Mol. McMahon SA, Roberts GA, Johnson KA, Cooper LP, Liu H, White JH, Carter LG, Sanghvi B, Oke M, Walkinshaw MD, et al. Structure 21, 13841395 (2013). Nature 474, 604608 (2011). Koning, R. I. et al. Appl. Deveau H, Garneau JE, Moineau S. CRISPR/Cas system and its role in phage-bacteria interactions. Microbiol. Biol. This leads to the view that the non-core genes may optimize the phage to occupy a certain ecological niche, and that the changing repertoire of these genes gives the phage population access to new niches. 2011 Oct 1; 1(4): 298303. WebThe T-even viruses (T2, T4, and T6) have heads 80 110 nm, while the T-odd phages (T1, T3, T5, and T7) have isometric heads about 60 nm in diameter. Effect of phage vB_EcoM_FJ1 on the reduction of ETEC O9:H9 infection in a neonatal pig cell line, Rhizosphere phage communities drive soil suppressiveness to bacterial wilt disease, Genomic diversity and ecological distribution of marine Pseudoalteromonas phages, Abundant and cosmopolitan lineage of cyanopodoviruses lacking a DNA polymerase gene, Unexplored diversity and ecological functions of transposable phages, Characterization and genome analysis of a novel phage Kayfunavirus TM1. Ackermann HW. Nat. For example there are fewer than 50 each of completely sequenced RNA phages and ssDNA phages, and of the more than 500 sequenced dsDNA tailed phages, ~55% are morphologically members of the Siphoviridae with long flexible non-contractile tails; the remainder are Myoviridae with contractile tails and Podoviridae with short stubby tails (~25% and ~20% respectively). Arch. Peralta, B. et al. Sci. Bacteriophage Accessibility Google Scholar. Bacteriophages Res. 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T2 phage had very high genomic sequence similarity to SV76 (99.99% identity), so we performed host range analysis of T2 with the same bacteria strains to see whether the genomic similarity translated to host range phenotypic similarity. Nature 340, 467468 (1989). and transmitted securely. J. [Genome size is the total length of DNA in an organism. T4 was the subject of the classic studies by Benzer (1955), Crick, Brenner et al. Hendrix, R. W. Bacteriophages: evolution of the majority. Inclusion in an NLM database does not imply endorsement of, or agreement with, The host range of the recombinant phages was identical to that of IP008. About 300 of its genes have been characterized. 5-hydroxymethylcytosine (5hmC) was first described in 1952 when it was found in the genomes of T-even bacteriophages (T2 and T4). Hendrix RW, Smith MC, Burns RN, Ford ME, Hatfull GF. . The authors contributed equally to all aspects of the article. Bergh, ., Brsheim, K. Y., Bratbak, G. & Heldal, M. High abundance of viruses found in aquatic environments. Comparative genomic analysis of 18. The human gut virome: inter-individual variation and dynamic response to diet. Tremblay, D. M. et al. 5-hydroxymethylcytosine (5hmC) was first described in 1952 when it was found in the genomes of T-even bacteriophages (T2 and T4). 22 March 2023, Microbiome Provided by the Springer Nature SharedIt content-sharing initiative, Nature Reviews Microbiology (Nat Rev Microbiol) 26, 19841994 (2007). First, there are examples of short conserved sequences at gene boundaries that could serve to target homologous recombination to these positions [27,28]. 9, 472484 (2015). Experiments conducted in 1952 by Alfred Hershey and Martha Chase demonstrated how the DNA of viruses is injected into the bacterial cells, while most of the viral proteins remain outside. Bethesda, MD 20894, Web Policies [Genome size is the total length of DNA in an organism. Genome Size Curr. Roux, S. et al. King G, Murray NE. Hershey, A. D. EMBO J. USA 116, 5493 (2019). Paris Japonica 150 billion b.p. 11, 799805 (1973). A quasi-atomic model of human adenovirus type 5 capsid. The largest bacteriophage genomes reach a size of 735 kb. It is in the genus Tequatrovirus, and the family Myoviridae. But we have barely scratched the surface and the next years of phage genome exploration promise to be especially revealing. Hatfull GF, Pedulla ML, Jacobs-Sera D, Cichon PM, Foley A, Ford ME, Gonda RM, Houtz JM, Hryckowian AJ, Kelchner VA, et al. Open Access The lambda red proteins promote efficient recombination between diverged sequences: implications for bacteriophage genome mosaicism. Reproducible protocols for metagenomic analysis of human faecal phageomes. [3]. Vidaver, A. K., Koski, R. K. & Van Etten, J. L. Bacteriophage 6: a lipid-containing virus of Pseudomonas phaseolicola. The global virome: not as big as we thought? 7, 17381751 (2013). Khan Academy Lpez-Prez, M., Haro-Moreno, J. M., Gonzalez-Serrano, R., Parras-Molt, M. & Rodriguez-Valera, F. Genome diversity of marine phages recovered from Mediterranean metagenomes: size matters. Nature 432, 6874 (2004). Appl. Cell Host Microbe 25, 285299.e8 (2019). Phage infecting a common host can also exhibit substantial diversity suggesting that there are additional barriers to genetic exchange [2022]. Hendrix RW, Lawrence JG, Hatfull GF, Casjens S. The origins and ongoing evolution of viruses. Structure of the archaeal headtailed virus HSTV-1 completes the HK97 fold story. These discoveries supported that DNA, rather than proteins, is the hereditary material. However, a ~1.8 kbp segment of Colbert is closely related to Rosebush (94% nucleotide identity) and was presumably acquired relatively recently from a Rosebush-like phage. Sinclair, R., Ravantti, J. Natl Acad. 8, 15892 (2017). Marston, M. F. & Amrich, C. G. Recombination and microdiversity in coastal marine cyanophages. The crystal structure of bacteriophage HK97 gp6: defining a large family of headtail connector proteins. Enterobacteria phage T2 Villar, E. et al. Not surprisingly, there are many different host-mediated protection systems such as restriction-modification [38], CRISPRs [39], tRNA cleavage [40], and Toxin-Antitoxin systems [41], as well as phage-encoded mechanisms for generating genome diversity at high frequency [42]. IB Biology 3.2 chromosomes Williamson, K. E., Fuhrmann, J. J., Wommack, K. E. & Radosevich, M. Viruses in soil ecosystems: an unknown quantity within an unexplored territory. 157, 20352046 (2012). volume18,pages 125138 (2020)Cite this article. Phages that can perform either a lytic or a lysogenic mode of replication. Hatfull, G. F. Dark matter of the biosphere: the amazing world of bacteriophage diversity. Nigro, O. D. et al. WebThe T-even phages, T2, T4, and T6, were used as model systems for the study of virus multiplication. Furthermore, phage-encoded homologous recombinases have properties that are well-suited to facilitating this process [31]. HHS Vulnerability Disclosure, Help It is notable that the GC% content of the large collection of mycobacteriophages varies between 55% and 70%, which is consistent with this consideration [20]. Sun, L. et al. Sci. Natl Acad. Biol. PubMed eLife 4, 120 (2015). The T2 phage can quickly turn an E. coli cell into a T2-producing factory that releases phages when the cell ruptures. Microbiol. Early life dynamics of the human gut virome and bacterial microbiome in infants. Friedman SD, Genthner FJ, Gentry J, Sobsey MD, Vinje J. Gene mapping and phylogenetic analysis of the complete genome from 30 single-stranded RNA male-specific coliphages (family Leviviridae). Rev. As with the head genes discussed above, this more extensive case of genetic linkage can be understood in terms of the interactions of the encoded proteins: T4s DNA replication proteins form a complex, the nucleotide metabolism genes probably form a complex that feeds precursors into the DNA replication machine. 188, 24002410 (2006). Article Enterobacteria Phage T2 Sci. Curr Opin Virol. In 1952 Alfred Day Hershey and Martha Chase used the T2 bacteriophage in a famous experiment in which they demonstrated that only the nucleic acids of phage molecules were required for their replication within bacteria. Receptor-binding protein of Lactococcus lactis phages: identification and characterization of the saccharide receptor-binding site. & Schmid, M. F. Structural similarities in DNA packaging and delivery apparatuses in herpesvirus and dsDNA bacteriophages. Drosophila Melanogaster 123 million b.p. Sutter M, Boehringer D, Gutmann S, Gunther S, Prangishvili D, Loessner MJ, Stetter KO, Weber-Ban E, Ban N. Structural basis of enzyme encapsulation into a bacterial nanocompartment. Syst. Martinez-Hernandez, F. et al. 58, 465474 (2013). The Pacific Ocean virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. Fierer, N. et al. Rapid evolution of the human gut virome. Bacteriophages Valegard, K., Liljas, L., Fridborg, K. & Unge, T. The three-dimensional structure of the bacterial virus MS2. 12, 595600 (1993). & Bamford, D. H. Nucleic and amino acid sequences support structure-based viral classification. This study uses single-virus genomics to identify the most widespread phages in the ocean, which were previously overlooked in metagenomics projects because of their high microdiversity. Wigington, C. H. et al. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. The other genes of a phage genomethe non-core genesprovide a striking contrast to the core genes discussed above [33]. 8, 1953 (2017). Biol. PubMed Central The observation that different regions (genes and gene blocks) of the phage genomes have distinct evolutionary histories, owing to horizontal gene transfer events. Phage Google Scholar. 152, 227243 (2007). 189, 14821487 (2007). 4, 18951906 (2019). 11, e1001667 (2013). About 70% of these sequenced phages correspond to only 12 different bacterial hosts, and this modest collection likely represents just a small portion of the overall diversity. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. 18, 597603 (2011). 10, e1004181 (2014). Anyone you share the following link with will be able to read this content: Sorry, a shareable link is not currently available for this article. T phages - Oxford Reference To obtain Shkoporov, A. N. et al. This represents a notable departure from bacterial genome evolution, where flexibility in the cell membrane and cell wall does not impose any obvious constraint on genome size. Healthy human gut phageome. In: Calendar R, editor. Dpartement de biochimie, de microbiologie et de bio-informatique, Facult des sciences et de gnie, Universit Laval, Qubec City, Qubec, Canada, Mora B. Dion,Frank Oechslin&Sylvain Moineau, Groupe de recherche en cologie buccale, Facult de mdecine dentaire, Universit Laval, Qubec City, Qubec, Canada, Flix dHrelle Reference Center for Bacterial Viruses, Universit Laval, Qubec City, Qubec, Canada, You can also search for this author in Google Scholar. Greenberg, N. & Rottem, S. Composition and molecular organization of lipids and proteins in the envelope of mycoplasmavirus MVL2. Barylski, J. et al. Science 348, 1261447 (2015). Language links are at the top of the page across from the title. Rather we suggest that non-homologous recombination occurs rampantly and indiscriminately across the genomes and stringent natural selection for the successful arrangement of the core genes counterselects any gene arrangement that disrupts that, while allowing much more promiscuous reassortments of the non-core genes; a thoroughly Darwinian view of phage evolution. The site is secure. ^ {1,2,3} 1,2,3. start superscript, 1, comma, 2, comma, 3, end superscript. Interestingly, the same region in Rosebush is from that in Qyrzula (Fig. the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in De Paepe, M. et al. Mycoplasma phage P1 [17]], ~21kbp [e.g. There are essentially three types of populations available for study. Analysis of Spounaviruses as a case study for the overdue reclassification of tailed phages. Bacteriophage Additional plausible mechanisms are by transposition, site-specific recombination, and homing endonucleases and while all these contribute they are likely also minor components. Environmental characteristics of Agulhas rings affect interocean plankton transport. The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Phage genome size varies enormously, ranging from the ~3,300 nucleotide ssRNA viruses of Escherichia coli[16] to the almost 500 kbp genome of Bacillus megateriumphage G (our WebIn T2 genes 39 and 60 are fused into one gene (605 amino acids), and it is equivalent to gyrB ( Huang, 1990). WebT2 phage is more properly called Enterobacteria phage T2. The issue is further complicated by the presence of genome sequences that are phage-derived or phage-associated but play biological roles separate from viral lytic growth. In the phage genomes, 5hmC is further glycosylated to 5ghmC and provides protection against cleavage by bacterial restriction endonucleases [1]. Lubbers MW, Waterfield NR, Beresford TP, Le Page RW, Jarvis AW. Nilsson, A. S. & Haggrd-Ljungquist, E. Detection of homologous recombination among bacteriophage P2 relatives. McKenna, R. et al. Rev. PRINTED FROM OXFORD REFERENCE (www.oxfordreference.com). A large variation in capsid size can be observed among members of the Caudovirales, with diameters ranging from 45 to 185 nm, which is usually linked to genome size 18. USA 110, 1077110776 (2013). Rev. Szymczak, P., Janzen, T., Neves, R. & Kot, W. Novel variants of Streptococcus thermophilus bacteriophages are indicative of genetic recombination among phages from different bacterial species. Suttle, C. A. Their dsDNAs are linear, cyclically permuted, and terminally redundant. Sequencing genomes of the viral fraction in a sample. Mol. Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer. Candidate receptors fadL ::Tn ( A = 2.60) and ompF ::Tn ( A = 2.53) were identified ( Fig. & Breitbart, M. Unprecedented diversity of ssDNA phages from the family Microviridae detected within the gut of a protochordate model organism (Ciona robusta). Hurwitz, B. L., Brum, J. R. & Sullivan, M. B. Depth-stratified functional and taxonomic niche specialization in the core and flexible Pacific Ocean virome. Article eLife 4, e06416 (2015). Metagenomic analyses of an uncultured viral community from human feces. Sequencing of complete bacterial genomes has become relatively simple and there are over 1,600 completely sequenced bacterial chromosomes. Pittsburgh Bacteriophage Institute and Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260, 412 624 6975, The publisher's final edited version of this article is available at, Bacteriophage genomes are enormously diverse, Bacteriophage genomes are pervasively mosaic, Bacteriophage-host dynamics are strong drivers of their evolution. The observation that the corresponding genes travel together with the head and tail genes is less easily explained but may reflect well-documented interactions among recombination proteins and DNA replication initiation and between recombination proteins and DNA packaging [34]. Lavelle, K. et al. Nat. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Unfortunately, there is no bacteriophage fossil record as such and the best promise for understanding phage origins and evolution is the comparative analysis of phages present in the environment today. Methods Mol. T2 phage had very high genomic sequence similarity to SV76 (99.99% identity), so we performed host range analysis of T2 with the same bacteria strains to see whether the genomic similarity translated to host range phenotypic similarity. Roux, S. et al. Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell- and meta-genomics. genome size Viral dark matter and virushost interactions resolved from publicly available microbial genomes. 71, 31193125 (2005). Variability in shapes and sizes for phages. What do all these genes do? Nucleotide sequence comparison of bacteriophage genomes reveals them to be enormously diverse [1]. Pedulla ML, Ford ME, Houtz JM, Karthikeyan T, Wadsworth C, Lewis JA, Jacobs-Sera D, Falbo J, Gross J, Pannunzio NR, et al. The newly made phages are now free to attack more cells. 347, 895902 (2005). Nat. To kill or not to kill: the balance between lytic and lysogenic viral infection is driven by trophic status. Res. Google Scholar. The capsid of a bacteriophage can be icosahedral, filamentous, or Chipman, P. R., Agbandje-McKenna, M., Renaudin, J., Baker, T. S. & McKenna, R. Structural analysis of the Spiroplasma virus, SpV4: implications for evolutionary variation to obtain host diversity among the Microviridae. The DNA contains 5-hydroxymethylcytosine (q.v. Microbiol. Abrescia, N. G. et al. & Sullivan, M. B. Juhala, R. J. et al. PLoS Biol. Structure of the bacteriophage 6 nucleocapsid suggests a mechanism for sequential RNA packaging. government site. Biol. 01 February 2023, Marine Life Science & Technology Nat. For example, mycobacteriophages Rosebush and Qyrzula are closely related and share extensive nucleotide sequence similarity. However, accurately identifying prophages and phage-related objects remains a challenge especially for those bacteria for which few if any viruses have been characterized and it is not easy to predict from genome information alone which of these can generate infectious particles through prophage induction. Genomic analysis of uncultured marine viral communities. Single-cell genomics uncover Pelagibacter as the putative host of the extremely abundant uncultured 37-F6 viral population in the ocean. In most cases the functions of the non-core genes are unknown, and in some well-studied phages like coliphage , they have been deleted without adverse effect on phage growth under laboratory conditions. Phage genome size varies enormously, ranging from the ~3,300 nucleotide ssRNA viruses of Escherichia coli[16] to the almost 500 kbp genome of Bacillus megateriumphage G (our Expansion of bacteriophages is linked to aggravated intestinal inflammation and colitis. Microbiol. Arnaud, C.-A. Duarte, C. M. Seafaring in the 21st century: the Malaspina 2010 Circumnavigation Expedition. Hendrix, R. W., Smith, M. C. M., Burns, R. N., Ford, M. E. & Hatfull, G. F. Evolutionary relationships among diverse bacteriophages and prophages: all the worlds a phage. Adv. Environ. Their dsDNAs are linear, cyclically permuted, and terminally redundant. Virol. Zhu H, Yin S, Shuman S. Characterization of polynucleotide kinase/phosphatase enzymes from Mycobacteriophages omega and Cjw1 and vibriophage KVP40. Rising to the challenge: accelerated pace of discovery transforms marine virology. A major lineage of non-tailed dsDNA viruses as unrecognized killers of marine bacteria. Proc. The examples of genome and chromosome number have been selected to allow points of interest to be raised Paris japonica Largest Known Genome 80, 26482655 (2014). Escherichia Coli 5 million b.p. Homo Sapiens 3.3 billion b.p. Roux, S., Hallam, S. J., Woyke, T. & Sullivan, M. B. Mol. Virol. Environ. Thingstad, T. F., Vage, S., Storesund, J. E., Sandaa, R.-A. USA 110, 10604 (2013). These prokaryotic phage proteins share significant homology with the bacterial gyrase and the ParE and ParC proteins. A notable advantage of this genome-by-genome approach, however, is that individual phages with sequenced genomes become available for further genetic, biochemical and structural dissection. Bacteriophages
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