1887

Abstract

The phage P106B (vB_RglS_P106B) is a phage with a narrow spectrum of infectivity, which has been isolated from soils with a history of pea cultivation. The trapping host of P106B is an indigenous strain of (SO14B-4) isolated from soils associated with . Phenotypic characterization of the phage revealed that P106B has an approximate burst size of 21 p.f.u. per infected cell with 60 min and 100 min eclipse and latent periods, respectively. Phage P106B was unable to transduce under the conditions tested. The genome of P106B is 56 024 bp in length with a mean DNA G+C content of 47.9 %. The complete genome sequence contains 95 putative ORFs and a single tRNA gene coding for leucine with the anticodon TTA. Putative functions could only be assigned to 22 of the predicted ORFs while a significant number of ORFs (47) shared no sequence similarities to previously characterized proteins. The remaining 26 putative protein-coding genes exhibited a sequence resemblance to other hypothetical proteins. No lysogeny-related genes were found in the P106B genome.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000022
2015-03-01
2019-10-13
Loading full text...

Full text loading...

/deliver/fulltext/micro/161/3/611.html?itemId=/content/journal/micro/10.1099/mic.0.000022&mimeType=html&fmt=ahah

References

  1. Adams M. H. . ( 1959; ). Bacteriophages. New York:: Interscience;.
    [Google Scholar]
  2. Ahmad M. H. , Morgan V. . ( 1994; ). Characterization of a cowpea (Vigna unguiculata) rhizobiophage and its effect on cowpea nodulation and growth. . Biol Fertil Soils 18:, 297–301. [CrossRef]
    [Google Scholar]
  3. Altschul S. F. , Madden T. L. , Schäffer A. A. , Zhang J. H. , Zhang Z. , Miller W. , Lipman D. J. . ( 1997; ). Gapped blast and psi-blast: a new generation of protein database search programs. . Nucleic Acids Res 25:, 3389–3402. [CrossRef] [PubMed]
    [Google Scholar]
  4. Amarger N. , Macheret V. , Laguerre G. . ( 1997; ). Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. . Int J Syst Bacteriol 47:, 996–1006. [CrossRef] [PubMed]
    [Google Scholar]
  5. Appunu C. , Dhar B. . ( 2006; ). Phage typing of indigenous soybean-rhizobia and relationship of a phage group strains for their asymbiotic and symbiotic nitrogen fixation. . Indian J Exp Biol 44:, 1006–1011.[PubMed]
    [Google Scholar]
  6. Aziz R. K. , Bartels D. , Best A. A. , DeJongh M. , Disz T. , Edwards R. A. , Formsma K. , Gerdes S. , Glass E. M. . & other authors ( 2008; ). The rast server: rapid annotations using subsystems technology. . BMC Genomics 9:, 75. [CrossRef] [PubMed]
    [Google Scholar]
  7. Bailly-Bechet M. , Vergassola M. , Rocha E. . ( 2007; ). Causes for the intriguing presence of tRNAs in phages. . Genome Res 17:, 1486–1495. [CrossRef] [PubMed]
    [Google Scholar]
  8. Becker A. , Kleickmann A. , Küster H. , Keller M. , Arnold W. , Pühler A. . ( 1993; ). Analysis of the Rhizobium meliloti genes exoU, exoV, exoW, exoT, and exoI involved in exopolysaccharide biosynthesis and nodule invasion: exoU and exoW probably encode glucosyltransferases. . Mol Plant Microbe Interact 6:, 735–744. [CrossRef] [PubMed]
    [Google Scholar]
  9. Beringer J. E. . ( 1974; ). R factor transfer in Rhizobium leguminosarum . . J Gen Microbiol 84:, 188–198. [CrossRef] [PubMed]
    [Google Scholar]
  10. Brewer T. E. , Stroupe M. E. , Jones K. M. . ( 2014; ). The genome, proteome and phylogenetic analysis of Sinorhizobium meliloti phage ΦM12, the founder of a new group of T4-superfamily phages. . Virology 450-451:, 84–97. [CrossRef] [PubMed]
    [Google Scholar]
  11. Brewin N. J. , Wood E. A. , Johnston A. W. B. , Dibb N. J. , Hombrecher G. . ( 1982; ). Recombinant nodulation plasmids in Rhizobium leguminosarum . . J Gen Microbiol 128:, 1817–1827.
    [Google Scholar]
  12. Bromfield E. S. P. , Sinha I. B. , Wolynetz M. S. . ( 1986; ). Influence of location, host cultivar, and inoculation on the composition of naturalized populations of Rhizobium meliloti in Medicago sativa nodules. . Appl Environ Microbiol 51:, 1077–1084.[PubMed]
    [Google Scholar]
  13. Buchanan-Wollaston V. . ( 1979; ). Generalized transduction in Rhizobium leguminosarum . . J Gen Microbiol 112:, 135–142. [CrossRef]
    [Google Scholar]
  14. Casjens S. R. . ( 2011; ). The DNA-packaging nanomotor of tailed bacteriophages. . Nat Rev Microbiol 9:, 647–657. [CrossRef] [PubMed]
    [Google Scholar]
  15. Christie G. E. , Temple L. M. , Bartlett B. A. , Goodwin T. S. . ( 2002; ). Programmed translational frameshift in the bacteriophage P2 FETUD tail gene operon. . J Bacteriol 184:, 6522–6531. [CrossRef] [PubMed]
    [Google Scholar]
  16. Davis R. W. , Botstein D. , Roth J. R. . ( 1980; ). Advanced Bacterial Genetics: A Manual for Genetic Engineering. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  17. Deák V. , Lukács R. , Buzás Z. , Pálvölgyi A. , Papp P. P. , Orosz L. , Putnoky P. . ( 2010; ). Identification of tail genes in the temperate phage 16-3 of Sinorhizobium meliloti 41. . J Bacteriol 192:, 1617–1623. [CrossRef] [PubMed]
    [Google Scholar]
  18. Finan T. M. , Hartweig E. , LeMieux K. , Bergman K. , Walker G. C. , Signer E. R. . ( 1984; ). General transduction in Rhizobium meliloti . . J Bacteriol 159:, 120–124.[PubMed]
    [Google Scholar]
  19. Ganyu A. , Csiszovszki Z. , Ponyi T. , Kern A. , Buzás Z. , Orosz L. , Papp P. P. . ( 2005; ). Identification of cohesive ends and genes encoding the terminase of phage 16-3. . J Bacteriol 187:, 2526–2531. [CrossRef] [PubMed]
    [Google Scholar]
  20. Geniaux E. , Laguerre G. , Amarger N. . ( 1993; ). Comparison of geographically distant populations of Rhizobium isolated from root nodules of Phaseolus vulgaris . . Mol Ecol 2:, 295–302. [CrossRef]
    [Google Scholar]
  21. Guo P. X. , Erickson S. , Anderson D. . ( 1987; ). A small viral RNA is required for in vitro packaging of bacteriophage phi 29 DNA. . Science 236:, 690–694. [CrossRef] [PubMed]
    [Google Scholar]
  22. Hashem F. M. , Angle J. S. . ( 1988; ). Rhizobiophage effects on Bradyrhizobium japonicum nodulation and soybean growth. . Soil Biol Biochem 20:, 69–73. [CrossRef]
    [Google Scholar]
  23. Hashem F. M. , Angle J. S. . ( 1990; ). Rhizobiophage effects on nodulation, nitrogen-fixation, and yield of field-grown soybeans (Glycine max L. Merr.). . Biol Fertil Soils 9:, 330–334. [CrossRef]
    [Google Scholar]
  24. Herridge D. F. , Peoples M. B. , Boddey R. M. . ( 2008; ). Global inputs of biological nitrogen fixation in agricultural systems. . Plant Soil 311:, 1–18. [CrossRef]
    [Google Scholar]
  25. Hirsch P. R. . ( 1979; ). Plasmid-determined bacteriocin production by Rhizobium leguminosarum . . J Gen Microbiol 113:, 219–228. [CrossRef]
    [Google Scholar]
  26. Hyatt D. , Chen G. L. , LoCascio P. F. , Land M. L. , Larimer F. W. , Hauser L. J. . ( 2010; ). Prodigal: prokaryotic gene recognition and translation initiation site identification. . BMC Bioinformatics 11:, 119. [CrossRef] [PubMed]
    [Google Scholar]
  27. Hynes M. F. , Quandt J. , O’Connell M. P. , Pühler A. . ( 1989; ). Direct selection for curing and deletion of Rhizobium plasmids using transposons carrying the Bacillus subtilis sacB gene. . Gene 78:, 111–120. [CrossRef] [PubMed]
    [Google Scholar]
  28. Josey D. P. , Beynon J. L. , Johnston A. W. B. , Beringer J. E. . ( 1979; ). Strain identification in Rhizobium using intrinsic antibiotic resistance. . J Appl Bacteriol 46:, 343–350. [CrossRef]
    [Google Scholar]
  29. Kearse M. , Moir R. , Wilson A. , Stones-Havas S. , Cheung M. , Sturrock S. , Buxton S. , Cooper A. . & other authors ( 2012; ). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. . Bioinformatics 28:, 1647–1649.[CrossRef]
    [Google Scholar]
  30. Kondorosi E. , Gyuris J. , Schmidt J. , John M. , Duda E. , Hoffmann B. , Schell J. , Kondorosi A. . ( 1989; ). Positive and negative control of nod gene expression in Rhizobium meliloti is required for optimal nodulation. . EMBO J 8:, 1331–1340.[PubMed]
    [Google Scholar]
  31. Kutter E. , Raya R. , Carlson K. . ( 2005; ). Molecular mechanisms of phage infection. . In Bacteriophages: Biology and Applications, pp. 165–222. Edited by Kutter B. , Sulakvelidze A. . . Boca Raton, FL:: CRC press;.
    [Google Scholar]
  32. Laemmli U. K. . ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. . Nature 227:, 680–685. [CrossRef] [PubMed]
    [Google Scholar]
  33. Laslett D. , Canback B. . ( 2004; ). aragorn, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. . Nucleic Acids Res 32:, 11–16. [CrossRef] [PubMed]
    [Google Scholar]
  34. Lawson K. A. , Barnet Y. M. , McGilchrist C. A. . ( 1987; ). Environmental factors influencing numbers of Rhizobium leguminosarum biovar trifolii and its bacteriophages in two field soils. . Appl Environ Microbiol 53:, 1125–1131.[PubMed]
    [Google Scholar]
  35. Lech K. , Reddy K. J. , Sherman L. A. . ( 2001; ). Preparing lambda DNA from phage lysates. . In Current Protocols in Molecular Biology, 1.13.1–1.13.10. Edited by Ausubel F. M. , Brent R. , Kingston R. E. , Moore D. D. , Seidman J. G. , Smith J. A. , Struhl K. . . New York:: Wiley;. [CrossRef]
    [Google Scholar]
  36. Lehman S. M. , Kropinski A. M. , Castle A. J. , Svircev A. M. . ( 2009; ). Complete genome of the broad-host-range Erwinia amylovora phage phiEa21-4 and its relationship to Salmonella phage felix O1. . Appl Environ Microbiol 75:, 2139–2147. [CrossRef] [PubMed]
    [Google Scholar]
  37. Levin M. E. , Hendrix R. W. , Casjens S. R. . ( 1993; ). A programmed translational frameshift is required for the synthesis of a bacteriophage lambda tail assembly protein. . J Mol Biol 234:, 124–139. [CrossRef] [PubMed]
    [Google Scholar]
  38. Lowe T. M. , Eddy S. R. . ( 1997; ). tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. . Nucleic Acids Res 25:, 955–964. [CrossRef] [PubMed]
    [Google Scholar]
  39. Lu L. D. , Sun Q. , Fan X. Y. , Zhong Y. , Yao Y. F. , Zhao G. P. . ( 2010; ). Mycobacterial MazG is a novel NTP pyrophosphohydrolase involved in oxidative stress response. . J Biol Chem 285:, 28076–28085. [CrossRef] [PubMed]
    [Google Scholar]
  40. Martin M. O. , Long S. R. . ( 1984; ). Generalized transduction in Rhizobium meliloti . . J Bacteriol 159:, 125–129.[PubMed]
    [Google Scholar]
  41. Martín A. C. , López R. , García P. . ( 1996; ). Analysis of the complete nucleotide sequence and functional organization of the genome of Streptococcus pneumoniae bacteriophage Cp-1. . J Virol 70:, 3678–3687.[PubMed]
    [Google Scholar]
  42. Martínez-Romero E. , Segovia L. , Mercante F. M. , Franco A. A. , Graham P. , Pardo M. A. . ( 1991; ). Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. . Int J Syst Bacteriol 41:, 417–426. [CrossRef] [PubMed]
    [Google Scholar]
  43. Mendum T. A. , Clark I. M. , Hirsch P. R. . ( 2001; ). Characterization of two novel Rhizobium leguminosarum bacteriophages from a field release site of genetically-modified rhizobia. . Antonie van Leeuwenhoek 79:, 189–197. [CrossRef] [PubMed]
    [Google Scholar]
  44. Mink M. , Orosz L. , Sik T. . ( 1982; ). Specialized and generalized transducing rhizobiophage 16–3 and 11 are closely related. . FEMS Microbiol Lett 13:, 383–387. [CrossRef]
    [Google Scholar]
  45. Moroz O. V. , Murzin A. G. , Makarova K. S. , Koonin E. V. , Wilson K. S. , Galperin M. Y. . ( 2005; ). Dimeric dUTPases, HisE, and MazG belong to a new superfamily of all-alpha NTP pyrophosphohydrolases with potential “house-cleaning” functions. . J Mol Biol 347:, 243–255. [CrossRef] [PubMed]
    [Google Scholar]
  46. Noel K. D. , Sánchez A. , Fernández L. , Leemans J. , Cevallos M. A. . ( 1984; ). Rhizobium phaseoli symbiotic mutants with transposon Tn5 insertions. . J Bacteriol 158:, 148–155.[PubMed]
    [Google Scholar]
  47. Petty N. K. , Foulds I. J. , Pradel E. , Ewbank J. J. , Salmond G. P. C. . ( 2006; ). A generalized transducing phage (phiIF3) for the genomically sequenced Serratia marcescens strain Db11: a tool for functional genomics of an opportunistic human pathogen. . Microbiology 152:, 1701–1708. [CrossRef] [PubMed]
    [Google Scholar]
  48. Poole P. S. , Blyth A. , Reid C. J. , Walters K. . ( 1994; ). Myoinositol catabolism and catabolite regulation in Rhizobium leguminosarum bv. viciae . . Microbiology 140:, 2787–2795. [CrossRef]
    [Google Scholar]
  49. Priefer U. B. . ( 1989; ). Genes involved in lipopolysaccharide production and symbiosis are clustered on the chromosome of Rhizobium leguminosarum biovar viciae VF39. . J Bacteriol 171:, 6161–6168.[PubMed]
    [Google Scholar]
  50. Quandt J. , Clark R. G. , Venter A. P. , Clark S. R. D. , Twelker S. , Hynes M. F. . ( 2004; ). Modified RP4 and Tn5-Mob derivatives for facilitated manipulation of large plasmids in Gram-negative bacteria. . Plasmid 52:, 1–12. [CrossRef] [PubMed]
    [Google Scholar]
  51. Ribeiro R. A. , Rogel M. A. , López-López A. , Ormeño-Orrillo E. , Barcellos F. G. , Martínez J. , Thompson F. L. , Martínez-Romero E. , Hungria M. . ( 2012; ). Reclassification of Rhizobium tropici type A strains as Rhizobium leucaenae sp. nov.. Int J Syst Evol Microbiol 62:, 1179–1184. [CrossRef] [PubMed]
    [Google Scholar]
  52. Robertsen B. K. , Aman P. , Darvill A. G. , McNeil M. , Albersheim P. . ( 1981; ). Host-symbiont interactions: V. The structure of acidic extracellular polysaccharides secreted by Rhizobium leguminosarum and Rhizobium trifolii . . Plant Physiol 67:, 389–400. [CrossRef] [PubMed]
    [Google Scholar]
  53. Rocha E. P. C. , Danchin A. . ( 2002; ). Base composition bias might result from competition for metabolic resources. . Trends Genet 18:, 291–294. [CrossRef] [PubMed]
    [Google Scholar]
  54. Sambrook J. , Fritsch E. F. , Maniatis T. . ( 1989; ). Molecular Cloning: A Laboratory Manual, , 2nd edn.. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory Press;.
    [Google Scholar]
  55. Santamaría R. I. , Bustos P. , Sepúlveda-Robles O. , Lozano L. , Rodríguez C. , Fernández J. L. , Juárez S. , Kameyama L. , Guarneros G. . & other authors ( 2014; ). Narrow-host-range bacteriophages that infect Rhizobium etli associate with distinct genomic types. . Appl Environ Microbiol 80:, 446–454. [CrossRef] [PubMed]
    [Google Scholar]
  56. Semsey S. , Papp I. , Buzas Z. , Patthy A. , Orosz L. , Papp P. P. . ( 1999; ). Identification of site-specific recombination genes int and xis of the Rhizobium temperate phage 16-3. . J Bacteriol 181:, 4185–4192.[PubMed]
    [Google Scholar]
  57. Semsey S. , Blaha B. , Köles K. , Orosz L. , Papp P. P. . ( 2002; ). Site-specific integrative elements of rhizobiophage 16-3 can integrate into proline tRNA (CGG) genes in different bacterial genera. . J Bacteriol 184:, 177–182. [CrossRef] [PubMed]
    [Google Scholar]
  58. Shah K. , Desousa S. , Modi V. V. . ( 1981; ). Studies on transducing phage M-1 for Rhizobium japonicum D211. . Arch Microbiol 130:, 262–266. [CrossRef]
    [Google Scholar]
  59. Shu D. , Guo P. X. . ( 2003; ). Only one pRNA hexamer but multiple copies of the DNA-packaging protein gp16 are needed for the motor to package bacterial virus phi29 genomic DNA. . Virology 309:, 108–113. [CrossRef] [PubMed]
    [Google Scholar]
  60. Staniewski R. . ( 1980; ). Typing of Rhizobium with two different phage dilutions. . Acta Microbiol Pol 29:, 331–341.[PubMed]
    [Google Scholar]
  61. Steward G. F. . ( 2001; ). Fingerprinting viral assemblage by pulsed field gel electrophoresis (PFGE). . Methods Microbiol 30:, 85–103. [CrossRef]
    [Google Scholar]
  62. Swinton D. , Hattman S. , Benzinger R. , Buchanan-Wollaston V. , Beringer J. . ( 1985; ). Replacement of the deoxycytidine residues in Rhizobium bacteriophage RL38JI DNA. . FEBS Lett 184:, 294–298. [CrossRef] [PubMed]
    [Google Scholar]
  63. Udvardi M. , Poole P. S. . ( 2013; ). Transport and metabolism in legume-rhizobia symbioses. . Annu Rev Plant Biol 64:, 781–805. [CrossRef] [PubMed]
    [Google Scholar]
  64. Werquin M. , Ackermann H. W. , Lévesque R. C. . ( 1988; ). A Study of 33 Bacteriophages of Rhizobium meliloti . . Appl Environ Microbiol 54:, 188–196.[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000022
Loading
/content/journal/micro/10.1099/mic.0.000022
Loading

Data & Media loading...

Supplementary Data



PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error