Skip to main content
Top
Published in: Virology Journal 1/2010

Open Access 01-12-2010 | Review

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

Authors: Vasiliy M Petrov, Swarnamala Ratnayaka, James M Nolan, Eric S Miller, Jim D Karam

Published in: Virology Journal | Issue 1/2010

Login to get access

Abstract

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.
Appendix
Available only for authorised users
Literature
1.
go back to reference Cairns J, Stent GS, Watson JD: Phage and the Origins of Molecular Biology. New York: Cold Spring Harbor Laboratory Press; 1992. Cairns J, Stent GS, Watson JD: Phage and the Origins of Molecular Biology. New York: Cold Spring Harbor Laboratory Press; 1992.
2.
go back to reference Karam JD, et al.: Molecular Biology of Bacteriophage T4. Washington, DC: American Society for Microbiology; 1994. Karam JD, et al.: Molecular Biology of Bacteriophage T4. Washington, DC: American Society for Microbiology; 1994.
4.
6.
go back to reference Epstein RH, Bolle A, Steinberg CM, Kellenberger E, Boy De La Tour E, Chevalley R, Edgar RS, Susman M, Denhardt GH, Lielausis A: Physiological studies of conditional lethal mutants of bacteriophage T4D. In Symposia on Quantitative Biology: 1963; Cold Spring Harbor Laboratory of Quantitative Biology. Cold Spring Harbor Press, New York; 1963:375-394. Epstein RH, Bolle A, Steinberg CM, Kellenberger E, Boy De La Tour E, Chevalley R, Edgar RS, Susman M, Denhardt GH, Lielausis A: Physiological studies of conditional lethal mutants of bacteriophage T4D. In Symposia on Quantitative Biology: 1963; Cold Spring Harbor Laboratory of Quantitative Biology. Cold Spring Harbor Press, New York; 1963:375-394.
7.
go back to reference Miller ES, Kutter E, Mosig G, Arisaka F, Kunisawa T, Ruger W: Bacteriophage T4 genome. Microbiol Mol Biol Rev 2003,67(1):86-156. 10.1128/MMBR.67.1.86-156.2003PubMedPubMedCentralCrossRef Miller ES, Kutter E, Mosig G, Arisaka F, Kunisawa T, Ruger W: Bacteriophage T4 genome. Microbiol Mol Biol Rev 2003,67(1):86-156. 10.1128/MMBR.67.1.86-156.2003PubMedPubMedCentralCrossRef
8.
go back to reference Mosig G, Eiserling F: T4 and related phages: structure and development. In The Bacteriophages. Oxford University Press; 2006:225-267. Mosig G, Eiserling F: T4 and related phages: structure and development. In The Bacteriophages. Oxford University Press; 2006:225-267.
9.
go back to reference Ackermann HW, Krisch HM: A catalogue of T4-type bacteriophages. Arch Virol 1997,142(12):2329-2345. 10.1007/s007050050246PubMedCrossRef Ackermann HW, Krisch HM: A catalogue of T4-type bacteriophages. Arch Virol 1997,142(12):2329-2345. 10.1007/s007050050246PubMedCrossRef
10.
go back to reference Ackermann HW: 5500 Phages examined in the electron microscope. Arch Virol 2006,152(2):227-243. 10.1007/s00705-006-0849-1PubMedCrossRef Ackermann HW: 5500 Phages examined in the electron microscope. Arch Virol 2006,152(2):227-243. 10.1007/s00705-006-0849-1PubMedCrossRef
12.
go back to reference Wang CC, Yeh LS, Karam JD: Modular organization of T4 DNA polymerase. Evidence from phylogenetics. J Biol Chem 1995,270(44):26558-26564. 10.1074/jbc.270.44.26558PubMedCrossRef Wang CC, Yeh LS, Karam JD: Modular organization of T4 DNA polymerase. Evidence from phylogenetics. J Biol Chem 1995,270(44):26558-26564. 10.1074/jbc.270.44.26558PubMedCrossRef
13.
go back to reference Desplats C, Dez C, Tetart F, Eleaume H, Krisch HM: Snapshot of the genome of the pseudo-T-even bacteriophage RB49. J Bacteriol 2002,184(10):2789-2804. 10.1128/JB.184.10.2789-2804.2002PubMedPubMedCentralCrossRef Desplats C, Dez C, Tetart F, Eleaume H, Krisch HM: Snapshot of the genome of the pseudo-T-even bacteriophage RB49. J Bacteriol 2002,184(10):2789-2804. 10.1128/JB.184.10.2789-2804.2002PubMedPubMedCentralCrossRef
14.
go back to reference Petrov VM, Nolan JM, Bertrand C, Levy D, Desplats C, Krisch HM, Karam JD: Plasticity of the gene functions for DNA replication in the T4-like phages. J Mol Biol 2006,361(1):46-68. 10.1016/j.jmb.2006.05.071PubMedCrossRef Petrov VM, Nolan JM, Bertrand C, Levy D, Desplats C, Krisch HM, Karam JD: Plasticity of the gene functions for DNA replication in the T4-like phages. J Mol Biol 2006,361(1):46-68. 10.1016/j.jmb.2006.05.071PubMedCrossRef
15.
16.
go back to reference Comeau AM, Bertrand C, Letarov A, Tetart F, Krisch HM: Modular architecture of the T4 phage superfamily: a conserved core genome and a plastic periphery. Virology 2007,362(2):384-396. 10.1016/j.virol.2006.12.031PubMedCrossRef Comeau AM, Bertrand C, Letarov A, Tetart F, Krisch HM: Modular architecture of the T4 phage superfamily: a conserved core genome and a plastic periphery. Virology 2007,362(2):384-396. 10.1016/j.virol.2006.12.031PubMedCrossRef
17.
go back to reference Miller ES, Heidelberg JF, Eisen JA, Nelson WC, Durkin AS, Ciecko A, Feldblyum TV, White O, Paulsen IT, Nierman WC, et al.: Complete genome sequence of the broad-host-range vibriophage KVP40: comparative genomics of a T4-related bacteriophage. J Bacteriol 2003,185(17):5220-5233. 10.1128/JB.185.17.5220-5233.2003PubMedPubMedCentralCrossRef Miller ES, Heidelberg JF, Eisen JA, Nelson WC, Durkin AS, Ciecko A, Feldblyum TV, White O, Paulsen IT, Nierman WC, et al.: Complete genome sequence of the broad-host-range vibriophage KVP40: comparative genomics of a T4-related bacteriophage. J Bacteriol 2003,185(17):5220-5233. 10.1128/JB.185.17.5220-5233.2003PubMedPubMedCentralCrossRef
18.
go back to reference Zuber S, Ngom-Bru C, C B: Genome analysis of phage JS98 defines a fourth major subgroup of T4-like phages in Escherichia coli. J Bacteriol 2007,189(22):8206-8214. 10.1128/JB.00838-07PubMedPubMedCentralCrossRef Zuber S, Ngom-Bru C, C B: Genome analysis of phage JS98 defines a fourth major subgroup of T4-like phages in Escherichia coli. J Bacteriol 2007,189(22):8206-8214. 10.1128/JB.00838-07PubMedPubMedCentralCrossRef
19.
go back to reference Lavigne R, Darius P, Summer EJ, Seto D, Mahadevan P, Nilsson AS, Ackermann HW, Kropinski AM: Classification of Myoviridae bacteriophages using protein sequence similarity. BMC Microbiol 2009, 9: 224. 10.1186/1471-2180-9-224PubMedPubMedCentralCrossRef Lavigne R, Darius P, Summer EJ, Seto D, Mahadevan P, Nilsson AS, Ackermann HW, Kropinski AM: Classification of Myoviridae bacteriophages using protein sequence similarity. BMC Microbiol 2009, 9: 224. 10.1186/1471-2180-9-224PubMedPubMedCentralCrossRef
20.
go back to reference Filee J, Bapteste E, Susko E, Krisch HM: A selective barrier to horizontal gene transfer in the T4-type bacteriophages that has preserved a core genome with the viral replication and structural genes. Mol Biol Evol 2006,23(9):1688-1696. 10.1093/molbev/msl036PubMedCrossRef Filee J, Bapteste E, Susko E, Krisch HM: A selective barrier to horizontal gene transfer in the T4-type bacteriophages that has preserved a core genome with the viral replication and structural genes. Mol Biol Evol 2006,23(9):1688-1696. 10.1093/molbev/msl036PubMedCrossRef
21.
go back to reference Bull A, (ed): Microbial Diversity and Bioprospecting. Washington; ASM Press; 2004. Bull A, (ed): Microbial Diversity and Bioprospecting. Washington; ASM Press; 2004.
22.
go back to reference Hatfull GF, Cresawn SG, Hendrix RW: Comparative genomics of the mycobacteriophages: insights into bacteriophage evolution. Res Microbiol 2008,159(5):332-339. 10.1016/j.resmic.2008.04.008PubMedPubMedCentralCrossRef Hatfull GF, Cresawn SG, Hendrix RW: Comparative genomics of the mycobacteriophages: insights into bacteriophage evolution. Res Microbiol 2008,159(5):332-339. 10.1016/j.resmic.2008.04.008PubMedPubMedCentralCrossRef
23.
24.
go back to reference Lawrence JG, Hatfull GF, Hendrix RW: Imbroglios of viral taxonomy: genetic exchange and failings of phenetic approaches. J Bacteriol 2002,184(17):4891-4905. 10.1128/JB.184.17.4891-4905.2002PubMedPubMedCentralCrossRef Lawrence JG, Hatfull GF, Hendrix RW: Imbroglios of viral taxonomy: genetic exchange and failings of phenetic approaches. J Bacteriol 2002,184(17):4891-4905. 10.1128/JB.184.17.4891-4905.2002PubMedPubMedCentralCrossRef
25.
go back to reference Russell RL: Speciation among the T-even bacteriophages. In Ph.D. Dissertation. Pasadena: California Institute of Technology; 1967. Russell RL: Speciation among the T-even bacteriophages. In Ph.D. Dissertation. Pasadena: California Institute of Technology; 1967.
26.
go back to reference Kim JS, Davidson N: Electron microscope heteroduplex study of sequence relations of T2, T4, and T6 bacteriophage DNAs. Virology 1974,57(1):93-111. 10.1016/0042-6822(74)90111-1PubMedCrossRef Kim JS, Davidson N: Electron microscope heteroduplex study of sequence relations of T2, T4, and T6 bacteriophage DNAs. Virology 1974,57(1):93-111. 10.1016/0042-6822(74)90111-1PubMedCrossRef
27.
go back to reference Mann NH, Clokie MR, Millard A, Cook A, Wilson WH, Wheatley PJ, Letarov A, Krisch HM: The genome of S-PM2, a "photosynthetic" T4-type bacteriophage that infects marine Synechococcus strains. J Bacteriol 2005,187(9):3188-3200. 10.1128/JB.187.9.3188-3200.2005PubMedPubMedCentralCrossRef Mann NH, Clokie MR, Millard A, Cook A, Wilson WH, Wheatley PJ, Letarov A, Krisch HM: The genome of S-PM2, a "photosynthetic" T4-type bacteriophage that infects marine Synechococcus strains. J Bacteriol 2005,187(9):3188-3200. 10.1128/JB.187.9.3188-3200.2005PubMedPubMedCentralCrossRef
28.
go back to reference Klasson L, Andersson SGE: Evolution of minimal-gene-sets in host-dependent bacteria. Trends Microbiol 2004,12(1):37-43. 10.1016/j.tim.2003.11.006PubMedCrossRef Klasson L, Andersson SGE: Evolution of minimal-gene-sets in host-dependent bacteria. Trends Microbiol 2004,12(1):37-43. 10.1016/j.tim.2003.11.006PubMedCrossRef
29.
go back to reference Gil R, Silva FJ, Pereto J, Moya A: Determination of the core of a minimal bacterial gene set. Microbiol Mol Biol Rev 2004,68(3):518-537. 10.1128/MMBR.68.3.518-537.2004PubMedPubMedCentralCrossRef Gil R, Silva FJ, Pereto J, Moya A: Determination of the core of a minimal bacterial gene set. Microbiol Mol Biol Rev 2004,68(3):518-537. 10.1128/MMBR.68.3.518-537.2004PubMedPubMedCentralCrossRef
30.
go back to reference Abby S, Daubin V: Comparative genomics and the evolution of prokaryotes. Trends Microbiol 2007,15(3):135-141. 10.1016/j.tim.2007.01.007PubMedCrossRef Abby S, Daubin V: Comparative genomics and the evolution of prokaryotes. Trends Microbiol 2007,15(3):135-141. 10.1016/j.tim.2007.01.007PubMedCrossRef
31.
go back to reference Millard AD, Zwirglmaier K, Downey MJ, Mann NH, Scanlan DJ: Comparative genomics of marine cyanomyoviruses reveals the widespread occurrence of Synechococcus host genes localized to a hyperplastic region: implications for mechanisms of cyanophage evolution. Environ Microbiol 2009,11(9):2370-2387. 10.1111/j.1462-2920.2009.01966.xPubMedCrossRef Millard AD, Zwirglmaier K, Downey MJ, Mann NH, Scanlan DJ: Comparative genomics of marine cyanomyoviruses reveals the widespread occurrence of Synechococcus host genes localized to a hyperplastic region: implications for mechanisms of cyanophage evolution. Environ Microbiol 2009,11(9):2370-2387. 10.1111/j.1462-2920.2009.01966.xPubMedCrossRef
32.
go back to reference Tetart F, Desplats C, Kutateladze M, Monod C, Ackermann HW, Krisch HM: Phylogeny of the major head and tail genes of the wide-ranging T4-type bacteriophages. J Bacteriol 2001,183(1):358-366. 10.1128/JB.183.1.358-366.2001PubMedPubMedCentralCrossRef Tetart F, Desplats C, Kutateladze M, Monod C, Ackermann HW, Krisch HM: Phylogeny of the major head and tail genes of the wide-ranging T4-type bacteriophages. J Bacteriol 2001,183(1):358-366. 10.1128/JB.183.1.358-366.2001PubMedPubMedCentralCrossRef
33.
go back to reference Hendrix RW: Jumbo bacteriophages. In Lesser Known Large dsDNA Viruses. Volume 328. Heidelberg, Germany: Springer-Verlag Berlin; 2009:229-240. full_textCrossRef Hendrix RW: Jumbo bacteriophages. In Lesser Known Large dsDNA Viruses. Volume 328. Heidelberg, Germany: Springer-Verlag Berlin; 2009:229-240. full_textCrossRef
34.
go back to reference Wang CC, Pavlov A, Karam JD: Evolution of RNA-binding specificity in T4 DNA polymerase. J Biol Chem 1997,272(28):17703-17710. 10.1074/jbc.272.28.17703PubMedCrossRef Wang CC, Pavlov A, Karam JD: Evolution of RNA-binding specificity in T4 DNA polymerase. J Biol Chem 1997,272(28):17703-17710. 10.1074/jbc.272.28.17703PubMedCrossRef
35.
go back to reference Yeh LS, Hsu T, Karam JD: Divergence of a DNA replication gene cluster in the T4-related bacteriophage RB69. J Bacteriol 1998,180(8):2005-2013.PubMedPubMedCentral Yeh LS, Hsu T, Karam JD: Divergence of a DNA replication gene cluster in the T4-related bacteriophage RB69. J Bacteriol 1998,180(8):2005-2013.PubMedPubMedCentral
36.
go back to reference Petrov VM, Ratnayaka S, Karam JD: Genetic insertions and diversification of the PolB-type DNA polymerase (gp43) of T4-related phages. J Mol Biol 2010,395(3):457-474. 10.1016/j.jmb.2009.10.054PubMedCrossRef Petrov VM, Ratnayaka S, Karam JD: Genetic insertions and diversification of the PolB-type DNA polymerase (gp43) of T4-related phages. J Mol Biol 2010,395(3):457-474. 10.1016/j.jmb.2009.10.054PubMedCrossRef
37.
go back to reference Filee J, Tetart F, Suttle CA, Krisch HM: Marine T4-type bacteriophages, a ubiquitous component of the dark matter of the biosphere. Proc Natl Acad Sci USA 2005,102(35):12471-12476. 10.1073/pnas.0503404102PubMedPubMedCentralCrossRef Filee J, Tetart F, Suttle CA, Krisch HM: Marine T4-type bacteriophages, a ubiquitous component of the dark matter of the biosphere. Proc Natl Acad Sci USA 2005,102(35):12471-12476. 10.1073/pnas.0503404102PubMedPubMedCentralCrossRef
38.
go back to reference Timms AR, Cambray-Young J, Scott AE, Petty NK, Connerton PL, Clarke L, Seeger K, Quail M, Cummings N, Maskell DJ, et al.: Evidence for a lineage of virulent bacteriophages that target Campylobacter. BMC Genomics 11: 214. 10.1186/1471-2164-11-214 Timms AR, Cambray-Young J, Scott AE, Petty NK, Connerton PL, Clarke L, Seeger K, Quail M, Cummings N, Maskell DJ, et al.: Evidence for a lineage of virulent bacteriophages that target Campylobacter. BMC Genomics 11: 214. 10.1186/1471-2164-11-214
39.
go back to reference Wuitschick JD, Lindstrom PR, Meyer AE, Karrer KM: Homing endonucleases encoded by germ line-limited genes in Tetrahymena thermophila have APETELA2 DNA binding domains. Eukaryot Cell 2004,3(3):685-694. 10.1128/EC.3.3.685-694.2004PubMedPubMedCentralCrossRef Wuitschick JD, Lindstrom PR, Meyer AE, Karrer KM: Homing endonucleases encoded by germ line-limited genes in Tetrahymena thermophila have APETELA2 DNA binding domains. Eukaryot Cell 2004,3(3):685-694. 10.1128/EC.3.3.685-694.2004PubMedPubMedCentralCrossRef
40.
go back to reference Magnani E, Sjolander K, Hake S: From endonucleases to transcription factors: evolution of the AP2 DNA binding domain in plants. Plant Cell 2004,16(9):2265-2277. 10.1105/tpc.104.023135PubMedPubMedCentralCrossRef Magnani E, Sjolander K, Hake S: From endonucleases to transcription factors: evolution of the AP2 DNA binding domain in plants. Plant Cell 2004,16(9):2265-2277. 10.1105/tpc.104.023135PubMedPubMedCentralCrossRef
41.
go back to reference Wessler SR: Homing into the origin of the AP2 DNA binding domain. Trends Plant Sci 2005,10(2):54-56. 10.1016/j.tplants.2004.12.007PubMedCrossRef Wessler SR: Homing into the origin of the AP2 DNA binding domain. Trends Plant Sci 2005,10(2):54-56. 10.1016/j.tplants.2004.12.007PubMedCrossRef
42.
go back to reference Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW: Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 2005,3(5):e144. 10.1371/journal.pbio.0030144PubMedPubMedCentralCrossRef Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW: Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 2005,3(5):e144. 10.1371/journal.pbio.0030144PubMedPubMedCentralCrossRef
43.
45.
go back to reference Wu LT, Chang SY, Yen MR, Yang TC, Tseng YH: Characterization of extended-host-range pseudo-T-even bacteriophage Kpp95 isolated on Klebsiella pneumoniae. Appl Environ Microbiol 2007,73(8):2532-2540. 10.1128/AEM.02113-06PubMedPubMedCentralCrossRef Wu LT, Chang SY, Yen MR, Yang TC, Tseng YH: Characterization of extended-host-range pseudo-T-even bacteriophage Kpp95 isolated on Klebsiella pneumoniae. Appl Environ Microbiol 2007,73(8):2532-2540. 10.1128/AEM.02113-06PubMedPubMedCentralCrossRef
46.
go back to reference Carlson K, Raleigh EA, Hattman S: Restriction and modification. In Molecular Biology of Bacteriophage T4. Edited by: Karam J. Washington, D. C.: American Society for Microbiology Press; 1994:369-381. Carlson K, Raleigh EA, Hattman S: Restriction and modification. In Molecular Biology of Bacteriophage T4. Edited by: Karam J. Washington, D. C.: American Society for Microbiology Press; 1994:369-381.
47.
go back to reference Snyder L, Kaufman G: T4 phage exclusion mechanism. In Molecular Biology of Bacteriophage T4. Edited by: Karam J. Washington, D. C.: American Society for Microbiology; 1994:391-396. Snyder L, Kaufman G: T4 phage exclusion mechanism. In Molecular Biology of Bacteriophage T4. Edited by: Karam J. Washington, D. C.: American Society for Microbiology; 1994:391-396.
48.
go back to reference Drivdahl RH, Kutter EM: Inhibition of transcription of cytosine-containing DNA in vitro by the alc gene product of bacteriophage T4. J Bacteriol 1990,172(5):2716-2727.PubMedPubMedCentral Drivdahl RH, Kutter EM: Inhibition of transcription of cytosine-containing DNA in vitro by the alc gene product of bacteriophage T4. J Bacteriol 1990,172(5):2716-2727.PubMedPubMedCentral
49.
go back to reference Severinov K, Kashlev M, Severinova E, Bass I, McWilliams K, Kutter E, Nikiforov V, Snyder L, Goldfarb A: A non-essential domain of Escherichia coli RNA polymerase required for the action of the termination factor Alc. J Biol Chem 1994,269(19):14254-14259.PubMed Severinov K, Kashlev M, Severinova E, Bass I, McWilliams K, Kutter E, Nikiforov V, Snyder L, Goldfarb A: A non-essential domain of Escherichia coli RNA polymerase required for the action of the termination factor Alc. J Biol Chem 1994,269(19):14254-14259.PubMed
50.
go back to reference Dharmalingam K, Goldberg EB: Phage-coded protein prevents restriction of unmodified progeny T4 DNA. Nature 1976,260(5550):454-456. 10.1038/260454a0PubMedCrossRef Dharmalingam K, Goldberg EB: Phage-coded protein prevents restriction of unmodified progeny T4 DNA. Nature 1976,260(5550):454-456. 10.1038/260454a0PubMedCrossRef
51.
go back to reference Dharmalingam K, Revel HR, Goldberg EB: Physical mapping and cloning of bacteriophage T4 anti-restriction endonuclease gene. J Bacteriol 1982,149(2):694-699.PubMedPubMedCentral Dharmalingam K, Revel HR, Goldberg EB: Physical mapping and cloning of bacteriophage T4 anti-restriction endonuclease gene. J Bacteriol 1982,149(2):694-699.PubMedPubMedCentral
52.
go back to reference Kim BC, Kim K, Park EH, Lim CJ: Nucleotide sequence and revised map location of the arn gene from bacteriophage T4. Mol Cells 1997,7(5):694-696.PubMed Kim BC, Kim K, Park EH, Lim CJ: Nucleotide sequence and revised map location of the arn gene from bacteriophage T4. Mol Cells 1997,7(5):694-696.PubMed
53.
go back to reference Belle A, Landthaler M, Shub DA: Intronless homing: site-specific endonuclease SegF of bacteriophage T4 mediates localized marker exclusion analogous to homing endonucleases of group I introns. Genes Dev 2002,16(3):351-362. 10.1101/gad.960302PubMedPubMedCentralCrossRef Belle A, Landthaler M, Shub DA: Intronless homing: site-specific endonuclease SegF of bacteriophage T4 mediates localized marker exclusion analogous to homing endonucleases of group I introns. Genes Dev 2002,16(3):351-362. 10.1101/gad.960302PubMedPubMedCentralCrossRef
54.
go back to reference Liu Q, Belle A, Shub DA, Belfort M, Edgell DR: SegG endonuclease promotes marker exclusion and mediates co-conversion from a distant cleavage site. J Mol Biol 2003,334(1):13-23. 10.1016/j.jmb.2003.09.027PubMedCrossRef Liu Q, Belle A, Shub DA, Belfort M, Edgell DR: SegG endonuclease promotes marker exclusion and mediates co-conversion from a distant cleavage site. J Mol Biol 2003,334(1):13-23. 10.1016/j.jmb.2003.09.027PubMedCrossRef
55.
go back to reference Wilson GW, Edgell DR: Phage T4 mobE promotes trans homing of the defunct homing endonuclease I-TevIII. Nucleic Acids Res 2009,37(21):7110-7123. 10.1093/nar/gkp769PubMedPubMedCentralCrossRef Wilson GW, Edgell DR: Phage T4 mobE promotes trans homing of the defunct homing endonuclease I-TevIII. Nucleic Acids Res 2009,37(21):7110-7123. 10.1093/nar/gkp769PubMedPubMedCentralCrossRef
56.
go back to reference Monod C, Repoila F, Kutateladze M, Tetart F, Krisch HM: The genome of the pseudo T-even bacteriophages, a diverse group that resembles T4. J Mol Biol 1997,267(2):237-249. 10.1006/jmbi.1996.0867PubMedCrossRef Monod C, Repoila F, Kutateladze M, Tetart F, Krisch HM: The genome of the pseudo T-even bacteriophages, a diverse group that resembles T4. J Mol Biol 1997,267(2):237-249. 10.1006/jmbi.1996.0867PubMedCrossRef
57.
go back to reference Craig NL: Mobile DNA II. Washington, DC: American Society for Microbiology Press; 2002.CrossRef Craig NL: Mobile DNA II. Washington, DC: American Society for Microbiology Press; 2002.CrossRef
58.
go back to reference Brussow H, Hendrix RW: Phage genomics: small is beautiful. Cell 2002,108(1):13-16. 10.1016/S0092-8674(01)00637-7PubMedCrossRef Brussow H, Hendrix RW: Phage genomics: small is beautiful. Cell 2002,108(1):13-16. 10.1016/S0092-8674(01)00637-7PubMedCrossRef
59.
go back to reference Hendrix RW, Hatfull GF, Smith MC: Bacteriophages with tails: chasing their origins and evolution. Res Microbiol 2003,154(4):253-257. 10.1016/S0923-2508(03)00068-8PubMedCrossRef Hendrix RW, Hatfull GF, Smith MC: Bacteriophages with tails: chasing their origins and evolution. Res Microbiol 2003,154(4):253-257. 10.1016/S0923-2508(03)00068-8PubMedCrossRef
60.
go back to reference Bull A, Stach J: An overview of biodiversity-estimating the scale. In Microbial Diversity and Bioprospecting. Washington, DC: American Society for Microbiology Press; 2004:15-28.CrossRef Bull A, Stach J: An overview of biodiversity-estimating the scale. In Microbial Diversity and Bioprospecting. Washington, DC: American Society for Microbiology Press; 2004:15-28.CrossRef
61.
go back to reference Mosig G: Recombination and recombination-dependent DNA replication in bacteriophage T4. Annu Rev Genet 1998, 32: 379-413. 10.1146/annurev.genet.32.1.379PubMedCrossRef Mosig G: Recombination and recombination-dependent DNA replication in bacteriophage T4. Annu Rev Genet 1998, 32: 379-413. 10.1146/annurev.genet.32.1.379PubMedCrossRef
62.
go back to reference Eddy SR: Introns in the T-even bacteriophages. In Ph.D. Dissertation. Boulder: University of Colorado at Boulder; 1991. Eddy SR: Introns in the T-even bacteriophages. In Ph.D. Dissertation. Boulder: University of Colorado at Boulder; 1991.
63.
go back to reference Sandegren L, Sjoberg BM: Distribution, sequence homology, and homing of group I introns among T-even-like bacteriophages: evidence for recent transfer of old introns. J Biol Chem 2004,279(21):22218-22227. 10.1074/jbc.M400929200PubMedCrossRef Sandegren L, Sjoberg BM: Distribution, sequence homology, and homing of group I introns among T-even-like bacteriophages: evidence for recent transfer of old introns. J Biol Chem 2004,279(21):22218-22227. 10.1074/jbc.M400929200PubMedCrossRef
64.
go back to reference Eddy SR, Gold L: Artificial mobile DNA element constructed from the EcoRI endonuclease gene. Proc Natl Acad Sci USA 1992,89(5):1544-1547. 10.1073/pnas.89.5.1544PubMedPubMedCentralCrossRef Eddy SR, Gold L: Artificial mobile DNA element constructed from the EcoRI endonuclease gene. Proc Natl Acad Sci USA 1992,89(5):1544-1547. 10.1073/pnas.89.5.1544PubMedPubMedCentralCrossRef
65.
go back to reference Zeng Q, Bonocora RP, Shub DA: A free-standing homing endonuclease targets an intron insertion site in the psbA gene of cyanophages. Curr Biol 2009,19(3):218-222. 10.1016/j.cub.2008.11.069PubMedCrossRef Zeng Q, Bonocora RP, Shub DA: A free-standing homing endonuclease targets an intron insertion site in the psbA gene of cyanophages. Curr Biol 2009,19(3):218-222. 10.1016/j.cub.2008.11.069PubMedCrossRef
66.
go back to reference Roman J, Rubin MN, Woodson SA: Sequence specificity of in vivo reverse splicing of the Tetrahymena group I intron. RNA 1999,5(1):1-13. 10.1017/S1355838299981244PubMedPubMedCentralCrossRef Roman J, Rubin MN, Woodson SA: Sequence specificity of in vivo reverse splicing of the Tetrahymena group I intron. RNA 1999,5(1):1-13. 10.1017/S1355838299981244PubMedPubMedCentralCrossRef
67.
go back to reference Roy SW, Irimia M: Mystery of intron gain: new data and new models. Trends Genet 2009,25(2):67-73. 10.1016/j.tig.2008.11.004PubMedCrossRef Roy SW, Irimia M: Mystery of intron gain: new data and new models. Trends Genet 2009,25(2):67-73. 10.1016/j.tig.2008.11.004PubMedCrossRef
68.
go back to reference Gibb EA, Edgell DR: An RNA hairpin sequesters the ribosome binding site of the homing endonuclease mobE gene. J Bacteriol 2009,191(7):2409-2413. 10.1128/JB.01751-08PubMedPubMedCentralCrossRef Gibb EA, Edgell DR: An RNA hairpin sequesters the ribosome binding site of the homing endonuclease mobE gene. J Bacteriol 2009,191(7):2409-2413. 10.1128/JB.01751-08PubMedPubMedCentralCrossRef
69.
go back to reference Denou E, Bruttin A, Barretto C, Ngom-Bru C, Brussow H, Zuber S: T4 phages against Escherichia coli diarrhea: potential and problems. Virology 2009,388(1):21-30. 10.1016/j.virol.2009.03.009PubMedCrossRef Denou E, Bruttin A, Barretto C, Ngom-Bru C, Brussow H, Zuber S: T4 phages against Escherichia coli diarrhea: potential and problems. Virology 2009,388(1):21-30. 10.1016/j.virol.2009.03.009PubMedCrossRef
70.
go back to reference Eddy SR, Gold L: The phage T4 nrdB intron: a deletion mutant of a version found in the wild. Genes Dev 1991,5(6):1032-1041. 10.1101/gad.5.6.1032PubMedCrossRef Eddy SR, Gold L: The phage T4 nrdB intron: a deletion mutant of a version found in the wild. Genes Dev 1991,5(6):1032-1041. 10.1101/gad.5.6.1032PubMedCrossRef
71.
go back to reference Waldor M, Friedman D, Adhya S: Phages: Their Role in Bacterial Pathogenesis and Biotechnology. Washington, D.C: American Society for Microbiology Press; 2005.CrossRef Waldor M, Friedman D, Adhya S: Phages: Their Role in Bacterial Pathogenesis and Biotechnology. Washington, D.C: American Society for Microbiology Press; 2005.CrossRef
72.
go back to reference Fischetti VA, Nelson D, Schuch R: Reinventing phage therapy: are the parts greater than the sum? Nat Biotechnol 2006,24(12):1508-1511. 10.1038/nbt1206-1508PubMedCrossRef Fischetti VA, Nelson D, Schuch R: Reinventing phage therapy: are the parts greater than the sum? Nat Biotechnol 2006,24(12):1508-1511. 10.1038/nbt1206-1508PubMedCrossRef
74.
go back to reference Chibani-Chennoufi S, Sidoti J, Bruttin A, Dillmann ML, Kutter E, Qadri F, Sarker SA, Brussow H: Isolation of Escherichia coli bacteriophages from the stool of pediatric diarrhea patients in Bangladesh. J Bacteriol 2004,186(24):8287-8294. 10.1128/JB.186.24.8287-8294.2004PubMedPubMedCentralCrossRef Chibani-Chennoufi S, Sidoti J, Bruttin A, Dillmann ML, Kutter E, Qadri F, Sarker SA, Brussow H: Isolation of Escherichia coli bacteriophages from the stool of pediatric diarrhea patients in Bangladesh. J Bacteriol 2004,186(24):8287-8294. 10.1128/JB.186.24.8287-8294.2004PubMedPubMedCentralCrossRef
75.
go back to reference Weigele PR, Pope WH, Pedulla ML, Houtz JM, Smith AL, Conway JF, King J, Hatfull GF, Lawrence JG, Hendrix RW: Genomic and structural analysis of Syn9, a cyanophage infecting marine Prochlorococcus and Synechococcus. Environ Microbiol 2007,9(7):1675-1695. 10.1111/j.1462-2920.2007.01285.xPubMedCrossRef Weigele PR, Pope WH, Pedulla ML, Houtz JM, Smith AL, Conway JF, King J, Hatfull GF, Lawrence JG, Hendrix RW: Genomic and structural analysis of Syn9, a cyanophage infecting marine Prochlorococcus and Synechococcus. Environ Microbiol 2007,9(7):1675-1695. 10.1111/j.1462-2920.2007.01285.xPubMedCrossRef
Metadata
Title
Genomes of the T4-related bacteriophages as windows on microbial genome evolution
Authors
Vasiliy M Petrov
Swarnamala Ratnayaka
James M Nolan
Eric S Miller
Jim D Karam
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2010
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-7-292

Other articles of this Issue 1/2010

Virology Journal 1/2010 Go to the issue