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Current Microbiology

, Volume 76, Issue 5, pp 558–565 | Cite as

The Isolation and Characterization of Kronos, a Novel Caulobacter Rhizosphere Phage that is Similar to Lambdoid Phages

  • Louis Berrios
  • Bert ElyEmail author
Article
  • 120 Downloads

Abstract

Despite their ubiquity, relatively few bacteriophages have been characterized. Here, we set out to explore Caulobacter bacteriophages (caulophages) in the rhizosphere and characterized Kronos, the first caulophage isolated from the rhizosphere. Kronos is a member of the Siphoviridae family since it has a long flexible tail. In addition, an analysis of the Kronos genome indicated that many of the predicted proteins were distantly related to those of bacteriophages in the lambdoid family. Consistent with this observation, we were able to demonstrate the presence of cos sites that are similar to those found at the ends of lambdoid phage genomes. Moreover, Kronos displayed a relatively rare head and tail morphology compared to other caulophages but was similar to that of the lambdoid phages. Taken together, these data indicate that Kronos is distantly related to lambdoid phages and may represent a new Siphoviridae genus.

Notes

Funding

This work was funded in part by National Institutes of Health Grant GM076277 to BE.

Supplementary material

284_2019_1656_MOESM1_ESM.pdf (139 kb)
Supplementary material 1 (PDF 139 KB)

References

  1. 1.
    Aalto AP, Bitto D, Ravantti JJ et al (2012) Snapshot of virus evolution in hypersaline environments from the characterization of a membrane-containing salisaeta icosahedral phage 1. Proc Natl Acad Sci USA 109:7079–7084CrossRefGoogle Scholar
  2. 2.
    Abedon ST, Yin J (2009) Bacteriophage plaques: theory and analysis. In: Clokie MR, Kropinski AM (eds) Methods in molecular biology™, vol 501. Humana Press, Clifton, pp 161–174Google Scholar
  3. 3.
    Ash KT, Drake KM, Gibbs WS et al (2017) Genomic diversity of Type B3 bacteriophages of Caulobacter crescentus. Curr Microbiol 74:779–786CrossRefGoogle Scholar
  4. 4.
    Aziz RK, Bartels D, Best AA et al (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75CrossRefGoogle Scholar
  5. 5.
    Black LW (1989) DNA packaging in dsDNA bacteriophages. Annu Rev Microbiol 43:267–292CrossRefGoogle Scholar
  6. 6.
    Casjens SR, Hendrix RW (2015) Bacteriophage lambda: early pioneer and still relevant. Virology 479:310–330CrossRefGoogle Scholar
  7. 7.
    Catalano CE (2000) The terminase enzyme from bacteriophage lambda: a DNA-packaging machine. Cell Mol Life Sci 57:128–148CrossRefGoogle Scholar
  8. 8.
    Chen J, Novick RP (2009) Phage-mediated intergeneric transfer of toxin genes. Science 323:139–141CrossRefGoogle Scholar
  9. 9.
    Dingwall A, Shapiro L, Ely B (1990) Analysis of bacterial genome organization and replication using pulsed-field gel electrophoresis. Methods 1:160–168CrossRefGoogle Scholar
  10. 10.
    Ely B, Gibbs W, Diez S et al (2015) The Caulobacter crescentus transducing phage Cr30 is a unique member of the T4-like family of myophages. Curr Microbiol 70:854–858CrossRefGoogle Scholar
  11. 11.
    Ely B, Johnson RC (1977) Generalized transduction in Caulobacter crescentus. Genetics 87:391–399Google Scholar
  12. 12.
    Etesami H, Maheshwari DK (2018) Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: Action mechanisms and future prospects. Ecotoxicol Environ Saf 156:225–246CrossRefGoogle Scholar
  13. 13.
    Fuhrman JA, Noble RT (1995) Viruses and protists cause similar bacterial mortality in coastal seawater. Limnol Oceanogr 40:1236–1242CrossRefGoogle Scholar
  14. 14.
    Gill JJ, Berry JD, Russell WK et al (2012) The Caulobacter crescentus phage phiCbK: genomics of a canonical phage. BMC Genom 13:542CrossRefGoogle Scholar
  15. 15.
    Johnson RC, Wood NB, Ely B (1977) Isolation and characterization of bacteriophages for Caulobacter crescentus. J Gen Virol 37:323–335CrossRefGoogle Scholar
  16. 16.
    Juhala RJ, Ford ME, Duda RL et al (2000) Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol 299:27–51CrossRefGoogle Scholar
  17. 17.
    Lee JH, Shin H, Choi Y, Ryu S (2013) Complete genome sequence analysis of bacterial-flagellum-targeting bacteriophage chi. Arch Virol 158:2179–2183CrossRefGoogle Scholar
  18. 18.
    Naveed M, Mitter B, Yousaf S et al (2014) The endophyte Enterobacter sp. FD17: a maize growth enhancer selected based on rigorous testing of plant beneficial traits and colonization characteristics. Biol Fertil Soils 50:249–262CrossRefGoogle Scholar
  19. 19.
    Nedialkova LP, Sidstedt M, Koeppel MB et al (2016) Temperate phages promote colicin-dependent fitness of Salmonella enteric serovar Typhimurium. Enviro Microbiol 18:1591–1603CrossRefGoogle Scholar
  20. 20.
    Nguyen D, Ely B (2018) A genome comparison of T7-like Podoviruses that infect Caulobacter crescentus. Curr Microbiol 75:760–765CrossRefGoogle Scholar
  21. 21.
    Oliveira L, Tavares P, Alonso JC (2013) Headful DNA packaging: bacteriophage SPP1 as a model system. Virus Res 173:247–259CrossRefGoogle Scholar
  22. 22.
    Poindexter JS (1964) Biological properties and classification of the Caulobacter group. Bacteriol Rev 28:231–295Google Scholar
  23. 23.
    Prischl M, Hackl E, Pastar M et al (2012) Genetically modified Bt maize lines containing cry3Bb1, cry1A105 or cry1Ab2 do not affect the structure and functioning of root-associated endophyte communities. Appl Soil Ecol 54:39–48CrossRefGoogle Scholar
  24. 24.
    Rao VB, Feiss M (2008) The bacteriophage DNA packaging motor. Annu Rev Genet 42:647–681CrossRefGoogle Scholar
  25. 25.
    Richardson CC (1983) Bacteriophage T7: minimal requirements for the replication of a duplex DNA molecule. Cell 33:315–317CrossRefGoogle Scholar
  26. 26.
    Roberts MD, Martin NL, Kropinski AM (2004) The genome and proteome of coliphage T1. Virology 318:245–266CrossRefGoogle Scholar
  27. 27.
    Rosenvold EC, Honigman A (1977) Mapping of AvaI and XmaI cleavage sites in bacteriophage DNA including a new technique of DNA digestion in agarose gels. Gene 2:273–288CrossRefGoogle Scholar
  28. 28.
    Rutherford K, Parkhill J, Crook J et al (2000) Artemis: sequence visualization and annotation. Bioinformatics 10:944–945CrossRefGoogle Scholar
  29. 29.
    Saraf M, Jha CK, Patel D (2010) The role of ACC deaminase producing PGPR in sustainable agriculture. In: Maheshwari DK (ed) Plant growth and health promoting bacteria, vol 1. Springer, Berlin, pp 365–385CrossRefGoogle Scholar
  30. 30.
    Schaefer AL, Lappala CR, Morlen RP et al (2013) LuxR-and LuxI-type quorum sensing circuits are prevalent in members of the Populus deltoides microbiome. J Appl Environ Microbiol 79:5745–5752CrossRefGoogle Scholar
  31. 31.
    Sharaf A, Mercati F, Elmaghraby I et al (2017) Functional and comparative genome analysis of novel virulent actinophages belonging to Streptomyces flavovirens. BMC Microbiol 17:51CrossRefGoogle Scholar
  32. 32.
    Takeshi M, Kenichi M (1983) Lambda phage DNA sequences affecting the packaging process. Gene 24:199–206CrossRefGoogle Scholar
  33. 33.
    Vahanian N, Oh CS, Sippy J et al (2017) Natural history of a viral cohesive end site: cosN of the λ-like phages. Virology 509:140–145CrossRefGoogle Scholar
  34. 34.
    Vance CP (2011) Phosphorus as a critical macronutrient. In: Barraclough P, Hawkesford MJ (eds) The molecular and physiological basis of nutrient use efficiency in crops, vol 1. Wiley, New York, pp 227–264CrossRefGoogle Scholar
  35. 35.
    Wang N (2006) Lysis timing and bacteriophage fitness. Genetics 172:17–26CrossRefGoogle Scholar
  36. 36.
    Waterbury PG, Lane MJ (1987) Generation of lambda phage concatemers for use as pulsed field electrophoresis size markers. Nucleic Acids Res 15:3930CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of South CarolinaColumbiaUSA

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