Skip to main content

Molecular analysis of the low-temperature Escherichia coli phage vB_EcoS_NBD2

Archives of Virology volume 163, pages 105–114 (2018)Cite this article

Abstract

A novel low-temperature Escherichia coli phage vB_EcoS_NBD2 was isolated in Lithuania from agricultural soil. With an optimum temperature for plating around 20 °C, vB_EcoS_NBD2 efficiently produced plaques on Escherichia coli NovaBlue (DE3) at a temperature range of 10–30 °C, yet failed to plate at temperatures above 35 °C. Phage vB_EcoS_NBD2 virions have a siphoviral morphology with an isometric head (65 nm in diameter), and a non-contractile flexible tail (170 nm). The 51,802-bp genome of vB_EcoS_NBD2 has a G + C content of 49.8%, and contains 87 probable protein-encoding genes as well as 1 gene for tRNASer. Comparative sequence analysis revealed that 22 vB_EcoS_NBD2 ORFs encode unique proteins that have no reliable identity to database entries. Based on homology to biologically defined proteins and/or proteomics analysis, 36 vB_EcoS_NBD2 ORFs were given a putative functional annotation, including 20 genes coding for morphogenesis-related proteins and 13 associated with DNA metabolism. Phylogenetic analysis revealed that vB_EcoS_NBD2 belongs to the subfamily Tunavirinae, but cannot be assigned to any genus currently recognized by ICTV.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

References

  1. Salmond GP, Fineran PC (2015) A century of the phage: past, present and future. Nat Rev Microbiol 13:777–786

    CAS  Article  PubMed  Google Scholar 

  2. Clokie MR, Millard AD, Letarov AV, Heaphy S (2011) Phages in nature. Bacteriophage 1:31–45

    Article  PubMed  PubMed Central  Google Scholar 

  3. Keen EC (2015) A century of phage research: Bacteriophages and the shaping of modern biology. Bioessays 37:6–9

    Article  PubMed  PubMed Central  Google Scholar 

  4. Klumpp J, Fouts DE, Sozhamannan S (2013) Bacteriophage functional genomics and its role in bacterial pathogen detection. Brief Funct Genomics 12:354–365

    Article  PubMed  Google Scholar 

  5. Jurczak-Kurek A, Gąsior T, Nejman-Faleńczyk B, Bloch S, Dydecka A et al (2016) Biodiversity of bacteriophages: morphological and biological properties of a large group of phages isolated from urban sewage. Sci Rep 6:34338

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Hatfull GF (2015) Dark matter of the biosphere: the amazing world of bacteriophage diversity. Goodrum F, ed. J Virol 89:8107–8110

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Ackermann HW (2001) Frequency of morphological phage descriptions in the year 2000. Arch Virol 146:843–857

    CAS  Article  PubMed  Google Scholar 

  8. Kutter E, Sulakvelidze A (2004) Bacteriophages: biology and applications. CRC Press, Boca Raton

    Book  Google Scholar 

  9. Seeley ND, Primrose SB (1980) The effect of temperature on the ecology of aquatic bacteriophages. J Gen Virol 46:87–95

    Article  Google Scholar 

  10. Klausa V, Piešinienė L, Staniulis J, Nivinskas R (2003) Abundance of T4-type bacteriophages in municipal wastewater and sewage. Ekologija 1:47–50

    Google Scholar 

  11. Leclerc H, Mossel DAA, Edberg SC, Struijk CB (2001) Advances in the bacteriology of the coliform group: their suitability as markers of microbial water safety. Annu Rev Microbiol 55:201–234

    CAS  Article  PubMed  Google Scholar 

  12. Yanagida M, Suzuki Y, Toda T (1984) Molecular organization of the head of bacteriophage T-even: underlying design principles. Adv Biophys 17:97–146

    CAS  Article  PubMed  Google Scholar 

  13. Wegrzyn G, Wegrzyn A (2005) Genetic switches during bacteriophage lambda development. Prog Nucleic Acid Res Mol Biol 79:1–48

    CAS  Article  PubMed  Google Scholar 

  14. Kaliniene L, Zajančkauskaitė A, Šimoliūnas E, Truncaitė L, Meškys R (2015) Low-temperature bacterial viruses VR—a small but diverse group of E. coli phages. Arch Virol 160:1367–1370

    CAS  Article  PubMed  Google Scholar 

  15. Šimoliūnas E, Kaliniene L, Stasilo M, Truncaitė L, Zajančkauskaitė A et al (2014) Isolation and characterization of vB_ArS-ArV2—first Arthrobacter sp. infecting bacteriophage with completely sequenced genome. PLoS One 9:e111230

    Article  PubMed  PubMed Central  Google Scholar 

  16. Carlson K, Miller E (1994) Experiments in T4 genetics. In: Karam JD (ed) Bacteriophage T4. ASM Press, Washington DC, pp 419–483

    Google Scholar 

  17. Alva V, Nam SZ, Söding J, Lupas AN (2016) The MPI bioinformatics toolkit as an integrative platform for advanced protein sequence and structure analysis. Nucleic Acids Res. doi:10.1093/nar/gkw348

    PubMed  PubMed Central  Google Scholar 

  18. Söding J, Biegert A, Lupas AN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33(suppl 2):W244–W248

    Article  PubMed  PubMed Central  Google Scholar 

  19. Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32(suppl 2):W273–W279

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Lopes A, Tavares P, Petit MA, Guérois R, Zinn-Justin S (2014) Automated identification of tailed bacteriophages and classification according to their neck organization. BMC Genomics 15:1027

    Article  PubMed  PubMed Central  Google Scholar 

  22. Selick HE, Kreuzer KN, Alberts BM (1988) The bacteriophage T4 insertion/substitution vector system. A method for introducing site-specific mutations into the virus chromosome. J Biol Chem 263:11336–11347

    CAS  PubMed  Google Scholar 

  23. Grenier F, Matteau D, Baby V, Rodrigue S (2014) Complete genome sequence of Escherichia coli BW25113. Genome Announc 2:e01038-14

    Article  PubMed  PubMed Central  Google Scholar 

  24. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2(2006):0008

    PubMed  Google Scholar 

  25. Yoon SH, Han MJ, Jeong H, Lee CH, Xia XX, Lee DH, Shim JH, Lee SY, Oh TK, Kim JF (2012) Comparative multi-omics systems analysis of Escherichia coli strains B and K-12. Genome Biol 13:R37

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. Han MJ, Lee SY, Hong SH (2012) Comparative analysis of envelope proteomes in Escherichia coli B and K-12 strains. J Microbiol Biotechnol 22:470–478

    CAS  Article  PubMed  Google Scholar 

  27. Silhavy TJ, Kahne D, Walker S (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2:a000414

    Article  PubMed  PubMed Central  Google Scholar 

  28. Müller-Loennies S, Lindner B, Brade H (2003) Structural analysis of oligosaccharides from lipopolysaccharide (LPS) of Escherichia coli K12 strain W3100 reveals a link between inner and outer core LPS biosynthesis. J Biol Chem 278:34090–34101

    Article  PubMed  Google Scholar 

  29. Jansson PE, Lindberg AA, Lindberg B, Wollin R (1981) Structural studies on the hexose region of the core in lipopolysaccharides from Enterobacteriaceae. Eur J Biochem 115:571–577

    CAS  Article  PubMed  Google Scholar 

  30. Bertozzi Silva J, Storms Z, Sauvageau D (2016) Host receptors for bacteriophage adsorption. FEMS Microbiol Lett 363(4):fnw002

    Article  PubMed  Google Scholar 

  31. Iyer LM, Koonin EV, Aravind L (2002) Classification and evolutionary history of the single-strand annealing proteins, RecT, Redbeta, ERF and RAD52. BMC Genomics 3:8

    Article  PubMed  PubMed Central  Google Scholar 

  32. Warren RA (1980) Modified bases in bacteriophage DNAs. Annu Rev Microbiol 34:137–158

    CAS  Article  PubMed  Google Scholar 

  33. Young R (2014) Phage lysis: three steps, three choices, one outcome. J Microbiol 52:243–258

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Rajaure M, Berry J, Kongari R, Cahill J, Young R (2015) Membrane fusion during phage lysis. Proc Natl Acad Sci USA 112:5497–5502

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Rao VB, Feiss M (2008) The bacteriophage DNA packaging motor. Annu Rev Genet 42:647–681

    CAS  Article  PubMed  Google Scholar 

  36. Rao VB, Feiss M (2015) Mechanisms of DNA packaging by large double-stranded DNA viruses. Annu Rev Virol 2:351–378

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. Wietzorrek A, Schwarz H, Herrmann C, Braun V (2006) The genome of the novel phage Rtp, with a rosette-like tail tip, is homologous to the genome of phage T1. J Bacteriol 188:1419–1436

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Casjens SR, Gilcrease EB (2009) Determining DNA packaging strategy by analysis of the termini of the chromosomes in tailed-bacteriophage virions. Methods Mol Biol 502:91–111

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Stirm S, Bessler W, Fehmel F, Freund-Mölbert E (1971) Bacteriophage particles with endo-glycosidase activity. J Virol 8:343–346

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Stummeyer K, Dickmanns A, Mühlenhoff M, Gerardy-Schahn R, Ficner R (2005) Crystal structure of the polysialic acid-degrading endosialidase of bacteriophage K1F. Nat Struct Mol Biol 12:90–96

    CAS  Article  PubMed  Google Scholar 

  41. Niu YD, McAllister TA, Nash JH, Kropinski AM, Stanford K (2014) Four Escherichia coli O157:H7 phages: a new bacteriophage genus and taxonomic classification of T1-like phages. PLoS One 9(6):e100426

    Article  PubMed  PubMed Central  Google Scholar 

  42. Sharma M (2013) Lytic bacteriophages: potential interventions against enteric bacterial pathogens on produce. Bacteriophage 3:e25518

    Article  PubMed  PubMed Central  Google Scholar 

  43. Painter JA, Hoekstra RM, Ayers T, Tauxe RV, Braden CR et al (2013) Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998–2008. Emerg Infect Dis 19:407–415

    Article  PubMed  PubMed Central  Google Scholar 

  44. Ongeng D, Geeraerd AH, Springael D, Ryckeboer J, Muyanja C et al (2015) Fate of Escherichia coli O157:H7 and Salmonella enterica in the manure-amended soil-plant ecosystem of fresh vegetable crops: a review. Crit Rev Microbiol 41:273–294

    Article  PubMed  Google Scholar 

  45. Pérez Pulido R, Grande Burgos MJ, Gálvez A, Lucas López R (2016) Application of bacteriophages in post-harvest control of human pathogenic and food spoiling bacteria. Crit Rev Biotechnol 36:851–861

    PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Research Council of Lithuania (Project No. SIT-7/2015).

Author information

Author notes

  1. Laura Kaliniene, Lidija Truncaitė and Eugenijus Šimoliūnas contributed equally to this work.

Authors and Affiliations

  1. Department of Molecular Microbiology and Biotechnology, Institute of Biochemistry, Life Sciences Center, Vilnius University, Sauletekio al. 7, 10257, Vilnius, Lithuania

    Laura Kaliniene, Lidija Truncaitė, Eugenijus Šimoliūnas, Aurelija Zajančkauskaitė, Monika Vilkaitytė & Rolandas Meškys

  2. Proteomics Center, Institute of Biochemistry, Life Sciences Center, Vilnius University, Sauletekio al. 7, 10257, Vilnius, Lithuania

    Algirdas Kaupinis

  3. Centre for Physical Sciences and Technology, Sauletekio al. 3, 10257, Vilnius, Lithuania

    Martynas Skapas

Authors
  1. Laura Kaliniene
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lidija Truncaitė
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eugenijus Šimoliūnas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aurelija Zajančkauskaitė
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Monika Vilkaitytė
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Algirdas Kaupinis
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Martynas Skapas
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rolandas Meškys
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laura Kaliniene.

Ethics declarations

Conflict of interest

The authors declare no conflict of interests.

Human and animal rights statement

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Handling Editor: Horst Neve.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 3910 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kaliniene, L., Truncaitė, L., Šimoliūnas, E. et al. Molecular analysis of the low-temperature Escherichia coli phage vB_EcoS_NBD2. Arch Virol 163, 105–114 (2018). https://doi.org/10.1007/s00705-017-3589-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-017-3589-5