Home LiteratureArticle Details
PMID: 11976309 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Snapshot of the genome of the pseudo-T-even bacteriophage RB49.

Journal of bacteriology ·Vol. 184 ·No. 10 ·2002-05-00 ·Pages 2789-804

Desplats C, Dez C, Tétart F, Eleaume H, Krisch HM

Abstract

RB49 is a virulent bacteriophage that infects Escherichia coli. Its virion morphology is indistinguishable from the well-known T-even phage T4, but DNA hybridization indicated that it was phylogenetically distant from T4 and thus it was classified as a pseudo-T-even phage. To further characterize RB49, we randomly sequenced small fragments corresponding to about 20% of the approximately 170-kb genome. Most of these nucleotide sequences lacked sufficient homology to T4 to be detected in an NCBI BlastN analysis. However, when translated, about 70% of them encoded proteins with homology to T4 proteins. Among these sequences were the numerous components of the virion and the phage DNA replication apparatus. Mapping the RB49 genes revealed that many of them had the same relative order found in the T4 genome. The complete nucleotide sequence was determined for the two regions of RB49 genome that contain most of the genes involved in DNA replication. This sequencing revealed that RB49 has homologues of all the essential T4 replication genes, but, as expected, their sequences diverged considerably from their T4 homologues. Many of the nonessential T4 genes are absent from RB49 and have been replaced by unknown sequences. The intergenic sequences of RB49 are less conserved than the coding sequences, and in at least some cases, RB49 has evolved alternative regulatory strategies. For example, an analysis of transcription in RB49 revealed a simpler pattern of regulation than in T4, with only two, rather than three, classes of temporally controlled promoters. These results indicate that RB49 and T4 have diverged substantially from their last common ancestor. The different T4-type phages appear to contain a set of common genes that can be exploited differently, by means of plasticity in the regulatory sequences and the precise choice of a large group of facultative genes.

MeSH Terms
Amino Acid Sequence Bacteriophage T4/genetics Base Sequence DNA, Viral/chemistry Escherichia coli/virology Genome, Viral Molecular Sequence Data Promoter Regions, Genetic RNA, Messenger/chemistry Transcription, Genetic
Chemicals
DNA, Viral RNA, Messenger
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Desplats Carine
Laboratoire de Microbiologie et Génétique Moléculaire du CNRS, UMR 5100, 118 Route de Norbonne, 31062 Toulouse Cedex, France.
Dez Christophe
Tétart Françoise
Eleaume Heïdy
Krisch H M
References (70)
70 references, click to expand
  1. DNA polymerase of the T4-related bacteriophages.
    Prog Nucleic Acid Res Mol Biol. 2000;64:65-96 PMID: 10697407
  2. Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages.
    J Mol Biol. 2000 May 26;299(1):27-51 PMID: 10860721
  3. Phylogeny of the major head and tail genes of the wide-ranging T4-type bacteriophages.
    J Bacteriol. 2001 Jan;183(1):358-66 PMID: 11114936
  4. Comparative phage genomics and the evolution of Siphoviridae: insights from dairy phages.
    Mol Microbiol. 2001 Jan;39(2):213-22 PMID: 11136444
  5. A conserved genetic module that encodes the major virion components in both the coliphage T4 and the marine cyanophage S-PM2.
    Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11411-6 PMID: 11553768
  6. Crystal structure of a pol alpha family replication DNA polymerase from bacteriophage RB69.
    Cell. 1997 Jun 27;89(7):1087-99 PMID: 9215631
  7. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  8. A retrovirus-like zinc domain is essential for translational repression of bacteriophage T4 gene 32.
    J Biol Chem. 1991 May 5;266(13):7967-70 PMID: 2022625
  9. Gene 32 transcription and mRNA processing in T4-related bacteriophages.
    Mol Microbiol. 1991 Mar;5(3):715-25 PMID: 2046553
  10. Compilation and alignment of DNA polymerase sequences.
    Nucleic Acids Res. 1991 Aug 11;19(15):4045-57 PMID: 1870963
  11. Structural basis for the nucleic acid binding cooperativity of bacteriophage T4 gene 32 protein: the (Lys/Arg)3(Ser/Thr)2 (LAST) motif.
    Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):1050-4 PMID: 1736285
  12. Analysis of five presumptive protein-coding sequences clustered between the primosome genes, 41 and 61, of bacteriophages T4, T2, and T6.
    J Virol. 1993 Apr;67(4):2305-16 PMID: 8383243
  13. Compilation, alignment, and phylogenetic relationships of DNA polymerases.
    Nucleic Acids Res. 1993 Feb 25;21(4):787-802 PMID: 8451181
  14. The bacteriophage T4 AsiA protein: a molecular switch for sigma 70-dependent promoters.
    Mol Microbiol. 1998 Feb;27(4):819-29 PMID: 9515707
  15. Divergence of a DNA replication gene cluster in the T4-related bacteriophage RB69.
    J Bacteriol. 1998 Apr;180(8):2005-13 PMID: 9555879
  16. Non-nearest neighbor effects on the thermodynamics of unfolding of a model mRNA pseudoknot.
    J Mol Biol. 1998 Jun 12;279(3):545-64 PMID: 9641977
  17. A catalogue of T4-type bacteriophages.
    Arch Virol. 1997;142(12):2329-45 PMID: 9672598
  18. Genome plasticity in the distal tail fiber locus of the T-even bacteriophage: recombination between conserved motifs swaps adhesin specificity.
    J Mol Biol. 1998 Sep 25;282(3):543-56 PMID: 9737921
  19. Tailed bacteriophages: the order caudovirales.
    Adv Virus Res. 1998;51:135-201 PMID: 9891587
  20. Evolution of DNA polymerase families: evidences for multiple gene exchange between cellular and viral proteins.
    J Mol Evol. 2002 Jun;54(6):763-73 PMID: 12029358
  21. DNA homology among the T-even bacteriophages.
    Virology. 1971 Jul;45(1):30-7 PMID: 5112413
  22. Translational, autogenous regulation of gene 32 expression during bacteriophage T4 infection.
    J Biol Chem. 1976 Nov 25;251(22):7263-70 PMID: 791948
  23. Stimulation of the synthesis of bacteriophage T4 gene 32 protein by ultraviolet light irradiation.
    J Mol Biol. 1976 Nov;108(1):67-81 PMID: 1003487
  24. Regulation of the expression of bacteriophage T4 genes 32 and 43.
    Virology. 1977 May 1;78(1):87-98 PMID: 324117
  25. Effect of RNase III on efficiency of translation of bacteriophage T7 lysozyme mRNA.
    J Virol. 1978 Jun;26(3):793-804 PMID: 353304
  26. Autogenous translational repression of bacteriophage T4 gene 32 expression in vitro.
    J Mol Biol. 1978 Nov 25;126(1):73-90 PMID: 739544
  27. Isolation and characterization of conditional lethal mutations in the mot gene of bacteriophage T4.
    J Mol Biol. 1978 Dec 15;126(3):551-70 PMID: 745239
  28. DNA binding properties of the T4 DNA helix-destabilizing protein. A calorimetric study.
    J Biol Chem. 1979 Jul 25;254(14):6426-32 PMID: 221498
  29. T4 gene 32 protein trypsin-generated fragments. Fluorescence measurement of DNA-binding parameters.
    J Biol Chem. 1979 Jul 25;254(14):6433-6 PMID: 221499
  30. Proteolytic removal of the COOH terminus of the T4 gene 32 helix-destabilizing protein alters the T4 in vitro replication complex.
    J Biol Chem. 1980 Dec 10;255(23):11484-93 PMID: 6254971
  31. Interactions of bacteriophage T4-coded gene 32 protein with nucleic acids. III. Binding properties of two specific proteolytic digestion products of the protein (G32P*I and G32P*III).
    J Mol Biol. 1981 Jan 5;145(1):123-38 PMID: 6455528
  32. In vitro system for middle T4 RNA. I. Studies with Escherichia coli RNA polymerase.
    J Biol Chem. 1982 Apr 25;257(8):4087-96 PMID: 7040377
  33. In vitro system for middle T4 RNA. II. Studies with T4-modified RNA polymerase.
    J Biol Chem. 1982 Apr 25;257(8):4097-101 PMID: 7040378
  34. Nucleotide sequences involved in bacteriophage T4 gene 32 translational self-regulation.
    Proc Natl Acad Sci U S A. 1982 Aug;79(16):4937-41 PMID: 6289325
  35. Activity of the hybrid trp-lac (tac) promoter of Escherichia coli in Pseudomonas putida. Construction of broad-host-range, controlled-expression vectors.
    Gene. 1983 Dec;26(2-3):273-82 PMID: 6323265
  36. Escherichia coli and Pseudomonas putida RNA polymerases display identical contacts with promoters.
    Mol Gen Genet. 1984;195(3):511-5 PMID: 6236350
  37. The T4 mot protein functions as part of a pre-replicative DNA-protein complex.
    J Biol Chem. 1985 Jan 10;260(1):633-9 PMID: 3880747
  38. Purification and properties of the bacteriophage T4 gene 61 RNA priming protein.
    J Biol Chem. 1985 Feb 10;260(3):1711-22 PMID: 3871437
  39. The stability of bacteriophage T4 gene 32 mRNA: a 5' leader sequence that can stabilize mRNA transcripts.
    Cell. 1985 Dec;43(2 Pt 1):461-9 PMID: 3000608
  40. Efficient utilization of Escherichia coli transcriptional signals in Bacillus subtilis.
    J Mol Biol. 1985 Dec 5;186(3):547-55 PMID: 2419570
  41. Vector for regulated expression of cloned genes in a wide range of gram-negative bacteria.
    J Bacteriol. 1986 Aug;167(2):447-54 PMID: 3525513
  42. Single-stranded DNA binding proteins required for DNA replication.
    Annu Rev Biochem. 1986;55:103-36 PMID: 3527040
  43. Gene 32 protein, the single-stranded DNA binding protein from bacteriophage T4, is a zinc metalloprotein.
    Proc Natl Acad Sci U S A. 1986 Nov;83(22):8452-6 PMID: 3490667
  44. Sense and antisense transcription of bacteriophage T4 gene 32. Processing and stability of the mRNAs.
    J Mol Biol. 1987 Mar 20;194(2):231-43 PMID: 3612804
  45. Zinc (II) and the single-stranded DNA binding protein of bacteriophage T4.
    Proc Natl Acad Sci U S A. 1987 Dec;84(23):8515-9 PMID: 3120192
  46. A bacteriophage T4 expression cassette that functions efficiently in a wide range of gram-negative bacteria.
    Gene. 1988;62(2):237-47 PMID: 3259198
  47. Nucleotide sequences of the bacteriophage T2 and T6 gene 32 mRNAs.
    Nucleic Acids Res. 1988 Oct 11;16(19):9341 PMID: 3262868
  48. Processing of unstable bacteriophage T4 gene 32 mRNAs into a stable species requires Escherichia coli ribonuclease E.
    EMBO J. 1988 Nov;7(11):3601-7 PMID: 3061803
  49. Human DNA polymerase alpha: predicted functional domains and relationships with viral DNA polymerases.
    FASEB J. 1989 Jan;3(1):14-21 PMID: 2642867
  50. Transcription and messenger RNA processing upstream of bacteriophage T4 gene 32.
    Mol Gen Genet. 1989 Oct;219(1-2):39-48 PMID: 2615764
  51. Transcriptional mapping of a DNA replication gene cluster in bacteriophage T4. Sites for initiation, termination, and mRNA processing.
    J Biol Chem. 1990 Mar 25;265(9):5303-16 PMID: 2180963
  52. An RNA polymerase-binding protein that is required for communication between an enhancer and a promoter.
    Science. 1990 May 4;248(4955):573-8 PMID: 2185541
  53. Overexpression, purification, and characterization of recombinant T4 gene 32 protein22-301 (g32P-B).
    J Biol Chem. 1990 Jul 15;265(20):11444-55 PMID: 2195020
  54. Sequence analysis of conserved regA and variable orf43.1 genes in T4-like bacteriophages.
    J Bacteriol. 1990 Sep;172(9):5180-6 PMID: 2168375
  55. Identification of protein coding regions by database similarity search.
    Nat Genet. 1993 Mar;3(3):266-72 PMID: 8485583
  56. Translational repression by the bacteriophage T4 gene 32 protein involves specific recognition of an RNA pseudoknot structure.
    J Mol Biol. 1993 Jul 5;232(1):89-104 PMID: 8331672
  57. A single mutation in bacteriophage T4 DNA polymerase (A737V, tsL141) decreases its processivity as a polymerase and increases its processivity as a 3'-->5' exonuclease.
    J Biol Chem. 1994 Jan 7;269(1):438-46 PMID: 8276833
  58. Interaction of DNA polymerase and DNA helicase within the bacteriophage T4 DNA replication complex. Leading strand synthesis by the T4 DNA polymerase mutant A737V (tsL141) requires the T4 gene 59 helicase assembly protein.
    J Biol Chem. 1994 Jan 7;269(1):447-55 PMID: 8276834
  59. Copurification of E. coli RNAase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation.
    Cell. 1994 Mar 11;76(5):889-900 PMID: 7510217
  60. Direct PCR sequencing of the ndd gene of bacteriophage T4: identification of a product involved in bacterial nucleoid disruption.
    Gene. 1994 Apr 8;141(1):9-16 PMID: 8163181
  61. The asiA gene product of bacteriophage T4 is required for middle mode RNA synthesis.
    J Bacteriol. 1994 Jul;176(13):3956-65 PMID: 8021178
  62. Isolation, characterization, and kinetic properties of truncated forms of T4 DNA polymerase that exhibit 3'-5' exonuclease activity.
    J Biol Chem. 1994 Jul 29;269(30):19286-94 PMID: 8034691
  63. Genomic polymorphism in the T-even bacteriophages.
    EMBO J. 1994 Sep 1;13(17):4181-92 PMID: 8076614
  64. Function and structure relationships in DNA polymerases.
    Annu Rev Biochem. 1994;63:777-822 PMID: 7526780
  65. Comparative molecular biology of lambdoid phages.
    Annu Rev Microbiol. 1994;48:193-222 PMID: 7826005
  66. Characterization of the osmotically inducible gene osmE of Escherichia coli K-12.
    Mol Microbiol. 1995 May;16(3):553-63 PMID: 7565114
  67. Modular organization of T4 DNA polymerase. Evidence from phylogenetics.
    J Biol Chem. 1995 Nov 3;270(44):26558-64 PMID: 7592876
  68. Bacteriophage T4 host range is expanded by duplications of a small domain of the tail fiber adhesin.
    J Mol Biol. 1996 May 24;258(5):726-31 PMID: 8637004
  69. The genome of the pseudo T-even bacteriophages, a diverse group that resembles T4.
    J Mol Biol. 1997 Mar 28;267(2):237-49 PMID: 9096222
  70. Evolutionary relationships among diverse bacteriophages and prophages: all the world's a phage.
    Proc Natl Acad Sci U S A. 1999 Mar 2;96(5):2192-7 PMID: 10051617
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
DOI
10.1128/JB.184.10.2789-2804.2002
Published
2002-05-00
Pages
2789-804
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC135041
Subset
IM
Databases
GENBANK
AY051145, AY051146, AY051147, AY051148, AY051149, AY051150, AY051151, AY051152, AY051153, AY051154, AY051155, AY051156, AY051157, AY051158, AY051159, AY051160, AY051161, AY051162, AY051163, AY051164, AY051165, AY051166, AY051167, AY051168, AY051169, AY051170, AY051171, AY051172, AY051173, AY051174, AY051175, AY051176, AY051177, AY051178, AY051179, AY051180, AY051181, AY051182, AY051183, AY051184, AY051185, AY051186, AY051187, AY051188, AY051189, AY051190, AY051191, AY051192, AY051193, AY051194, AY051195, AY051196, AY051197, BH153088, BH153089, BH153090, BH153091, BH153092, BH153093, BH153094, BH153095, BH153096, BH153097, BH153098, BH153099, BH153100, BH153101, BH153102, BH153103, BH153104, BH153105, BH153106, BH153107, BH153108, BH153109, BH153110, BH153111, BH153112, BH153113, BH153114, BH153115, BH153116, BH153117, BH153118, BH153119, BH153120, BH153121, BH153122, BH153123, BH153124, BH153125, BH153126, BH153127, BH153128, BH153129, BH153130, BH153131
External Links
PubMed source DOI: 10.1128/JB.184.10.2789-2804.2002 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2