Complete genome analysis of an active prophage of Vibrio alginolyticus

Abstract

An active prophage, Vibrio phage ValM-yong1, was isolated from pathogenic Vibrio alginolyticus by mitomycin C induction. This phage is a member of the family Myoviridae and contains a head approximately 90 nm in diameter and a retractable tail approximately 250 nm in length. The genome of the phage is 33,851 bp in length with a G+C content of 45.6%. The noteworthy features of Vibrio phage ValM-yong1 are its flower-like head and genomic mosaicism. Here, we focus on presenting the genomic characterization of the virus.

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References

  1. 1.

    Fu S, Hao J, Yang Q, Lan R, Wang Y, Ye S, Liu Y, Li R (2019) Long-distance transmission of pathogenic Vibrio species by migratory waterbirds: a potential threat to the public health. Sci Rep 9:16303

    Article  Google Scholar 

  2. 2.

    Thompson FL, Iida T, Swings J (2004) Biodiversity of Vibrios. Microbiol Mol Biol Rev 68:403–431

    CAS  Article  Google Scholar 

  3. 3.

    Lin Y, Zheng SL (2017) Investigation and analysis of an outbreak of foodborne disease caused by Vibrio alginolyticus. Chin Rural Health Serv Admin 37:59

    Google Scholar 

  4. 4.

    Mustapha S, Mustapha EM, Nozha C (2013) Vibrio alginolyticus: an emerging pathogen of foodborne diseases. Maejo Int J Sci Tech 2:302–309

    Google Scholar 

  5. 5.

    Jacobs Slifka KM, Newton AE, Mahon BE (2017) Vibrio alginolyticus infections in the USA, 1988–2012. Epidemiol Infect 145:1491–1499

    CAS  Article  Google Scholar 

  6. 6.

    Campanelli A, Sanchez-Politta S, Saurat JH (2008) Cutaneous ulceration after an octopus bite: infection due to Vibrio alginolyticus, an emerging pathogen. Ann Dermatol Venereol 135:225–227

    CAS  Article  Google Scholar 

  7. 7.

    Bunpa S, Chaichana N, Teng JLL, Lee HH, Woo PCY, Sermwittayawong D, Sawangjaroen N, Sermwittayawong N (2019) Outer membrane protein A (OmpA) is a potential virulence factor of Vibrio alginolyticus strains isolated from diseased fish. J Fish Dis 43:275–284

    Article  Google Scholar 

  8. 8.

    Hatfull GF, Hendrix RW (2011) Bacteriophages and their genomes. Curr Opin Virol 1:298–303

    CAS  Article  Google Scholar 

  9. 9.

    Filée J, Tétart F, Suttle CA, Krisch HM (2005) Marine t4-type bacteriophages, a ubiquitous component of the dark matter of the biosphere. Proc Natl Acad Sci USA 102:12471–12476

    Article  Google Scholar 

  10. 10.

    Feiner R, Argov T, Rabinovich L, Sigal N, Borovok I, Herskovits AA (2015) A new perspective on lysogeny: prophages as active regulatory switches of bacteria. Nat Rev Microbiol 13:641–650

    CAS  Article  Google Scholar 

  11. 11.

    Wendling CC, Goehlich H, Roth O (2018) The structure of temperate phage bacteria infection networks changes with the phylogenetic distance of the host bacteria. Biol Lett 14:20180320

    CAS  Article  Google Scholar 

  12. 12.

    Wendling CC, Piecyk A, Refardt D, Chibani C, Hertel R, Liesegang H, Bunk B, Overmann J, Roth O (2017) Tripartite species interaction: eukaryotic hosts suffer more from phage susceptible than from phage resistant bacteria. BMC Evol Biol 17:98

    Article  Google Scholar 

  13. 13.

    Harrison E, Brockhurst MA (2017) Ecological and evolutionary benefits of temperate phage: what does or doesn’t kill you makes you stronger. BioEssays 39(10):1002

    Google Scholar 

  14. 14.

    Nanda AM, Thormann K, Frunzke J (2015) Impact of spontaneous prophage induction on the fitness of bacterial populations and host-microbe interactions. J Bacteriol 197:410–419

    Article  Google Scholar 

  15. 15.

    Chen F, Wang K, Stewart J, Belas R (2006) Induction of multiple prophages from a marine bacterium: a genomic approach. Appl Environ Microbiol 72:4995–5001

    CAS  Article  Google Scholar 

  16. 16.

    Chibani CM, Hertel R, Hoppert M, Liesegang H, Wendling CC (2019) Closely related Vibrio alginolyticus strains encode an identical repertoire of prophages and filamentous phages. bioRxiv 859181

  17. 17.

    Zhang X, Kang H, Li Y, Liu X, Yang Y, Li S, Pei G, Sun Q, Shu P, Mi Z, Huang Y, Zhang Z, Liu Y, An X, Xu X, Tong Y (2015) Conserved termini and adjacent variable region of Twortlikevirus Staphylococcus phages. Virol Sin 30:433–440

    CAS  Article  Google Scholar 

  18. 18.

    Li S, Fan H, An X, Fan H, Jiang H, Chen Y, Tong Y (2014) Scrutinizing virus genome termini by high-throughput sequencing. PLoS ONE 9:e85806

    Article  Google Scholar 

  19. 19.

    Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:686–689

    Article  Google Scholar 

  20. 20.

    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  Article  Google Scholar 

  21. 21.

    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

    Article  Google Scholar 

  22. 22.

    Zimmermann L, Stephens A, Nam SZ, Rau D, Kubler J, Lozajic M, Gabler F, Sing J, Lupas AN, Alva V (2018) A completely reimplemented mpi bioinformatics toolkit with a new HHpred server at its core. J Mol Biol 430:2237–2243

    CAS  Article  Google Scholar 

  23. 23.

    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 (2014) The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res 42:206–214

    Article  Google Scholar 

  24. 24.

    Potter SC, Luciani A, Eddy SR, Park Y, Lopez R, Finn RD (2018) HMMER web server: 2018 update. Nucleic Acids Res 46:200–204

    Article  Google Scholar 

  25. 25.

    Arndt D, Grant JR, Marcu A, Sajed T, Pon A, Liang Y, Wishart DS (2016) PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 44:16–21

    Article  Google Scholar 

  26. 26.

    Xie X, Sun Q, Liao X, Tong Y, Peng S (2018) Complete genomes of two novel active prophages discovered by bioinformatics methods from high-throughput sequencing data. IOP Conf Ser Mater Sci Eng 466:012032

    Article  Google Scholar 

  27. 27.

    Krieg NR (1986) Bergeys manual of systematic bacteriology. Springer, New York

    Google Scholar 

  28. 28.

    Pedersen M, Ligowska M, Hammer K (2010) Characterization of the CI repressor protein encoded by the temperate lactococcal phage TP901-1. J Bacteriol 192:2102–2110

    CAS  Article  Google Scholar 

  29. 29.

    Rasmussen KK, Frandsen KE, Boeri Erba E, Pedersen M, Varming AK, Hammer K, Kilstrup M, Thulstrup PW, Blackledge M, Jensen MR, Lo Leggio L (2016) Structural and dynamics studies of a truncated variant of CI repressor from bacteriophage TP901-1. Sci Rep 6:29574

    CAS  Article  Google Scholar 

  30. 30.

    Rajamanickam K, Hayes S (2018) The bacteriophage lambda CII phenotypes for complementation, cellular toxicity and replication inhibition are suppressed in cII-oop constructs expressing the small RNA OOP. Viruses 10:115

    Article  Google Scholar 

  31. 31.

    Zhang X, Wang Y, Tong Y (2018) Analyzing genome termini of bacteriophage through high-throughput sequencing. Methods Mol Biol 1681:139–163

    CAS  Article  Google Scholar 

  32. 32.

    Carver T, Harris SR, Berriman M, Parkhill J, McQuillan JA (2012) Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics 28:464–469

    CAS  Article  Google Scholar 

  33. 33.

    Sullivan MJ, Petty NK, Beatson SA (2011) Easyfig: a genome comparison visualizer. Bioinformatics 27:10091010

    Article  Google Scholar 

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Acknowledgements

This study was funded by the National Key Research and Development Program (2018YFA0903000). We are also very grateful for the high-quality technical support provided by Pingping Zhan of the Electron Microscopy Laboratory of Ningbo University.

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Correspondence to Dengfeng Li.

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Qin, W., Li, D., Xu, L. et al. Complete genome analysis of an active prophage of Vibrio alginolyticus. Arch Virol 166, 891–896 (2021). https://doi.org/10.1007/s00705-020-04941-8

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