Genomic Diversity of Type B3 Bacteriophages of Caulobacter crescentus


The genomes of the type B3 bacteriophages that infect Caulobacter crescentus are among the largest phage genomes thus far deposited into GenBank with sizes over 200 kb. In this study, we introduce six new bacteriophage genomes which were obtained from phage collected from various water systems in the southeastern United States and from tropical locations across the globe. A comparative analysis of the 12 available genomes revealed a “core genome” which accounts for roughly 1/3 of these bacteriophage genomes and is predominately localized to the head, tail, and lysis gene regions. Despite being isolated from geographically distinct locations, the genomes of these bacteriophages are highly conserved in both genome sequence and gene order. We also identified the insertions, deletions, translocations, and horizontal gene transfer events which are responsible for the genomic diversity of this group of bacteriophages and demonstrated that these changes are not consistent with the idea that modular reassortment of genomes occurs in this group of bacteriophages.

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  1. 1.

    Agabian-Keshishian N, Shapiro L (1970) Stalked bacteria: properties of deoxyribonucleic acid bacteriophage phiCbK. J Virol 5(6):795–800

    CAS  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Ash K, Brown T, Watford T, Scott LE, Stephens C, Ely B (2014) A comparison of the Caulobacter NA1000 and K31 genomes reveals extensive genome rearrangements and differences in metabolic potential. Open Biol. doi:10.1098/rsob.140128

    PubMed  PubMed Central  Google Scholar 

  3. 3.

    Auch AF, von Jan M, Klenk HP, Goker M (2010) Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genom Sci 2(1):117–134. doi:10.4056/sigs.531120

    Article  Google Scholar 

  4. 4.

    Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genom 9:75. doi:10.1186/1471-2164-9-75

    Article  Google Scholar 

  5. 5.

    Botstein D (1980) A theory of modular evolution for bacteriophages. Ann N Y Acad Sci 354:484–490

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Comeau AM, Bertrand C, Letarov A, Tetart F, Krisch HM (2007) Modular architecture of the T4 phage superfamily: a conserved core genome and a plastic periphery. Virology 362:384–396

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5(6):e11147. doi:10.1371/journal.pone.0011147

    Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Dillard RS, Storms RE, De Masi L, Hampton C, Panis G, Patrick H, Viollier PH, Wright ER (2016) Analysis of phage-pilus interactions in Caulobacter crescentus. Microsc Microanal 22(Suppl 3):202–203. doi:10.1017/S1431927616001860

    Article  Google Scholar 

  9. 9.

    Ely B (1991) Genetics of Caulobacter crescentus. Methods Enzymol 204:372–384. doi:10.1016/0076-6879(91)04019-k

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Ely B, Gibbs W, Diez S, Ash K (2015) The Caulobacter crescentus transducing phage Cr30 is a unique member of the T4-Like family of myophages. Curr Microbiol 70(6):854–858. doi:10.1007/s00284-015-0799-5

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Ely B, Johnson RC (1977) Generalized transduction in Caulobacter crescentus. Genetics 87:391–399

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151(4):1531–1545

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Gill JJ, Berry JD, Russell WK, Lessor L, Escobar-Garcia DA, Hernandez D, Kane A, Keene J, Maddox M, Martin R, Mohan S, Thorn AM, Russell DH, Young R (2012) The Caulobacter crescentus phage phiCbK: genomics of a canonical phage. BMC Genom 13:542. doi:10.1186/1471-2164-13-542

    CAS  Article  Google Scholar 

  14. 14.

    Guerrero-Ferreira RC, Viollier PH, Ely B, Poindexter JS, Georgieva M, Jensen GJ, Wright ER (2011) Alternative mechanism for bacteriophage adsorption to the motile bacterium Caulobacter crescentus. Proc Natl Acad Sci USA 108(24):9963–9968. doi:10.1073/pnas.1012388108

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Johnson RC, Ely B (1977) Isolation of spontaneously derived mutants of Caulobacter crescentus. Genetics 86(1):25–32

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Johnson RC, Wood NB, Ely B (1977) Isolation and characterization of bacteriophages for Caulobacter crescentus. J Gen Virol 37(2):323–335. doi:10.1099/0022-1317-37-2-323

    Article  Google Scholar 

  17. 17.

    Lagenaur C, Farmer S, Agabian N (1977) Adsorption properties of stage-specific Caulobacter phage phiCbK. Virology 77:401–407

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Milne I, Bayer M, Cardle L, Shaw P, Stephen G, Wright F, Marshall D (2010) Tablet—next generation sequence assembly visualization. Bioinformatics 26(3):401–402. doi:10.1093/bioinformatics/btp666

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R (2013) The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 42(D1):D206–214. doi:10.1093/nar/gkt1226

    Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Paez-Espino D, Sharon I, Morovic W, Stahl B, Thomas BC, Barrangou R, Banfield JF (2015) CRISPR immunity drives rapid phage genome evolution in Streptococcus thermophilus. MBio. doi:10.1128/mBio.00262-15

    PubMed  PubMed Central  Google Scholar 

  21. 21.

    Panis G, Lambert C, Viollier PH (2012) Complete genome sequence of Caulobacter crescentus bacteriophage phiCbK. J Virol 86(18):10234–10235. doi:10.1128/JVI.01579-12

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Poindexter JS (1964) Biological properties and classification of the Caulobacter group. Bacteriol Rev 28:231–295

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualization and annotation. Bioinformatics 16(10):944–945

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Scott D, Ely B (2016) Conservation of the essential genome among Caulobacter and Brevundimonas species. Curr Microbiol 72:503–510

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526

    CAS  PubMed  Google Scholar 

  26. 26.

    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729. doi:10.1093/molbev/mst197

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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This work was funded in part by the National Science Foundation Grant EF-0826792 and NIH Grants R25GM066526 and R25GM076277 to BE.

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Correspondence to Bert Ely.

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The authors declare that there are no competing interests.

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Ash, K.T., Drake, K.M., Gibbs, W.S. et al. Genomic Diversity of Type B3 Bacteriophages of Caulobacter crescentus . Curr Microbiol 74, 779–786 (2017).

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  • Core Gene
  • Phage Genome
  • Major Capsid Protein
  • Phage Gene
  • Swarmer Cell