Advertisement

Virus Genes

pp 1–9 | Cite as

Complete genomic sequence of bacteriophage P23: a novel Vibrio phage isolated from the Yellow Sea, China

  • Yundan Liu
  • Lei Zhao
  • Min WangEmail author
  • Qi Wang
  • Xinran Zhang
  • Yuye Han
  • Meiwen Wang
  • Tong Jiang
  • Hongbing Shao
  • Yong Jiang
  • Andrew McMinn
Original Paper
  • 7 Downloads

Abstract

A novel Vibrio phage, P23, belonging to the family Siphoviridae was isolated from the surface water of the Yellow Sea, China. The complete genome of this phage was determined. A one-step growth curve showed that the latent period was approximately 30 min, the burst size was 24 PFU/cell, and the rise period was 20 min. The phage is host specific and is stable over a range of pH (5–10) and temperatures (4–65 °C). Transmission electron microscopy showed that phage P23 can be categorized into the Siphoviridae family, with an icosahedral head of 60 nm and a long noncontractile tail of 144 nm. The genome consisted of a linear, double-stranded 40.063 kb DNA molecule with 42.5% G+C content and 72 putative open reading frames (ORFs) without tRNA. The predicted ORFs were classified into six functional groups, including DNA replication, regulation and nucleotide metabolism, transcription, phage packaging, phage structure, lysis, and hypothetical proteins. The Vibrio phage P23 genome is a new marine Siphoviridae-family phage genome that provides basic information for further molecular research on interaction mechanisms between bacteriophages and their hosts.

Keywords

Bacteriophage Vibrio Siphoviridae Complete genome 

Notes

Acknowledgements

The research was funded by the Marine Scientific and Technological Innovation Project Financially supported by the Pilot National Laboratory for Marine Science and Technology (Qingdao) (2018SDKJ0104-4, 2018SDKJ0406-6, and 2016ASKJ14), the National Natural Science Foundation of China (41676178, 31500339, and 41076088), the National Key Research and Development Program of China (2017YFA0603200 and 2018YFC1406704), the State Oceanic Administration People’s republic of China (GASI-02-PAC-ST-MSwin, GASI-02-PAC-ST-MSaut), and the Fundamental Research Funds for the Central University of Ocean University of China (201812002, 201762017, and 201562018).

Author contributions

Hongbing Shao, Yong Jiang, Tong Jiang, Meiwen Wang, Yuye Han, and Min Wang conceived and designed the experiments and critically evaluated the manuscript. Xinran Zhang and Qi Wang conducted the sequencing experiments. Lei Zhao isolated and identified the phage and conducted the biological characterization experiments. Andrew McMinn helped to edit the language of manuscript. Yundan Liu was responsible for the data and sequence analyses and wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

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

References

  1. 1.
    Grimes DJ, Johnson CN, Dillon KS, Flowers AR, Iii NFN, Berutti T (2009) What genomic sequence information has revealed about Vibrio ecology in the ocean—a review. Microb Ecol 58:447–460.  https://doi.org/10.1007/s00248-009-9578-9 CrossRefGoogle Scholar
  2. 2.
    Almasi A (2005) An investigation on pathogenic Vibrios distribution in domestic wastewater. Iran J Environ Health Sci Eng 2(3):153–157Google Scholar
  3. 3.
    Almeida A, Cunha A, Gomes NCM, Alves E, Costa L, Faustino MAF (2009) Phage therapy and photodynamic therapy: low environmental impact approaches to inactivate microorganisms in fish farming plants. Marine Drugs 7:268–313.  https://doi.org/10.3390/md7030268 CrossRefGoogle Scholar
  4. 4.
    Yaashikaa PR, Saravanan A, Kumar PS (2016) Isolation and identification of Vibrio cholerae and Vibrio parahaemolyticus from prawn (Penaeus monodon) seafood: preservation strategies. Microb Pathog 99:5–13.  https://doi.org/10.1016/j.micpath.2016.07.014 CrossRefGoogle Scholar
  5. 5.
    Fuhrman JA, Suttle CA (1993) Viruses in marine planktonic systems. Oceanography 6(2):51–63.  https://doi.org/10.5670/oceanog.1993.14 CrossRefGoogle Scholar
  6. 6.
    Suttle CA (1994) The significance of viruses to mortality in aquatic microbial communities. Microb Ecol 28(2):237–243.  https://doi.org/10.1007/bf00166813 CrossRefGoogle Scholar
  7. 7.
    Malki K, Kula A, Bruder K, Sible E, Hatzopoulos T, Steidel S, Watkins SC, Putonti C (2015) Bacteriophages isolated from Lake Michigan demonstrate broad host-range across several bacterial phyla. Virol J 12:164.  https://doi.org/10.1186/s12985-015-0395-0 CrossRefGoogle Scholar
  8. 8.
    Ghai R, Martin-Cuadrado AB, Motto AG, Heredia IG, Cabrera R, Martin J, Verdú M, Deschamps P, Moreira D, López-García P, Mira A, Rodriguez-Valera F (2010) Metagenome of the Mediterranean deep chlorophyll maximum studied by direct and fosmid library 454 pyrosequencing. ISME J 4:1154–1166.  https://doi.org/10.1038/ismej.2010.44 CrossRefGoogle Scholar
  9. 9.
    Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, Wu D, Eisen JA, Hoffman JM, Remington K, Beeson K, Tran B, Smith H, Baden-Tillson H, Stewart C, Thorpe J, Freeman J, Andrews-Pfannkoch C, Venter JE, Li K, Kravitz S, Heidelberg JF, Utterback T, Rogers YH, Falcon LI, Souza V, Bonilla-Rosso G, Eguiarte LE, Karl DM, Sathyendranath S, Platt T, Bermingham E, Gallardo V, Tamayo-Castillo G, Ferrari MR, Strausberg RL, Nealson K, Friedman R, Frazier M, Venter JC (2007) The sorcerer II Global Ocean sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5:e77.  https://doi.org/10.1371/journal.pbio.0050077 CrossRefGoogle Scholar
  10. 10.
    Duhaime MB, Wichels A, Waldmann J, Teeling H, Glöckner FO (2011) Ecogenomics and genome landscapes of marine Pseudoalteromonas phage H105/1. ISME J Multidiscip J Microb Ecol 5:107–121.  https://doi.org/10.1038/ismej.2010.94 Google Scholar
  11. 11.
    Li Y, Wang M, Liu Q, Song X, Wang D, Ma Y, Jiang Y (2016) Complete genomic sequence of bacteriophage H188: a novel Vibrio kanaloae phage isolated from Yellow Sea. Curr Microbiol 72:628–633.  https://doi.org/10.1007/s00284-015-0984-6 CrossRefGoogle Scholar
  12. 12.
    Marmur J (1961) A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol 3:208–218.  https://doi.org/10.1016/0076-6879(63)06240-6 CrossRefGoogle Scholar
  13. 13.
    Hyman P, Abedon ST (2010) Bacteriophage host range and bacterial resistance. Adv Appl Microbiol 70:217–248.  https://doi.org/10.1016/s0065-2164(10)70007-1 CrossRefGoogle Scholar
  14. 14.
    Liu ZY, Li HF, Wang M, Jiang Y, Yang QW, Zhou XH, Gong Z, Liu Q, Shao HB (2018) Isolation, characterization and genome sequencing of the novel phage SL25 from the Yellow Sea, China. Marine Genom 37:31–34.  https://doi.org/10.1016/j.margen.2017.09.008 CrossRefGoogle Scholar
  15. 15.
    Ghosh K, Senevirathne A, Kang HS, Hyun WB, Kim JE, Kim KP (2018) Complete nucleotide sequence analysis of a novel Bacillus subtilis-infecting bacteriophage BSP10 and its effect on poly- gamma-glutamic acid degradation. Viruses 10:240.  https://doi.org/10.3390/v10050240 CrossRefGoogle Scholar
  16. 16.
    Pajunen M, Kiljunen S, Skurnik M (2000) Bacteriophage φYeO3-12, Specific for Yersinia enterocolitica Serotype O:3, is related to coliphages T3 and T7. J Bacteriol 182:5114–5120.  https://doi.org/10.1128/JB.182.18.5114-5120.2000 CrossRefGoogle Scholar
  17. 17.
    Gong Z, Wang M, Yang QW, Li ZS, Xia J, Gao Y et al (2017) Isolation and complete genome sequence of a novel Pseudoalteromonas phage PH357 from the Yangtze River estuary. Curr Microbiol 74:1–8.  https://doi.org/10.1007/s00284-017-1244-8 CrossRefGoogle Scholar
  18. 18.
    Capra ML, Quiberoni A, Reinheimer JA (2004) Thermal and chemical resistance of Lactobacillus casei and Lactobacillus paracasei bacteriophages. Lett Appl Microbiol 38:499–504.  https://doi.org/10.1111/j.1472-765X.2004.01525.x CrossRefGoogle Scholar
  19. 19.
    Alonso MDC, Rodríguez J, Borrego JJ (2002) Characterization of marine bacteriophages isolated from the Alboran Sea (Western Mediterranean). J Plankton Res 24(10):1079–1087.  https://doi.org/10.1093/plankt/24.10.1079 CrossRefGoogle Scholar
  20. 20.
    Alagappan KM et al (2010) Occurrence of Vibrio parahaemolyticus and its specific phages from shrimp ponds in East Coast of India. Curr Microbiol 61:235–240.  https://doi.org/10.1007/s00284-010-9599-0 CrossRefGoogle Scholar
  21. 21.
    DrulisKawa Z, Mackiewicz P, KesikSzeloch A et al (2011) Isolation and characterisation of KP34-a novel uKMV-like bacteriophage for Klebsiella pneumoniae. Appl Microbiol Biotechnol 90:1333–1345.  https://doi.org/10.1007/s00253-011-3149-y CrossRefGoogle Scholar
  22. 22.
    Othman BA, Askora A, Abo-Senna AS (2015) Isolation and characterization of a Siphoviridae phage infecting Bacillus megaterium from a heavily trafficked holy site in Saudi Arabia. Folia Microbiol 60:289–295.  https://doi.org/10.1007/s12223-015-0375-1 CrossRefGoogle Scholar
  23. 23.
    Yang Y, Cai L, Ma R, Xu Y, Tong Y, Huang Y, Jiao NZ, Zhang R (2017) A novel Roseosiphophage isolated from the oligotrophic South China Sea. Viruses 9:1–16.  https://doi.org/10.3390/v9050109 Google Scholar
  24. 24.
    Kang I, Kang D, Cho JC (2016) Complete genome sequence of bacteriophage P2559Y, a marine phage that infects Croceibacter atlanticus HTCC2559. Marine Genom 29:35–38.  https://doi.org/10.1016/j.margen.2016.07.001 CrossRefGoogle Scholar
  25. 25.
    Liu ZY, Wang M, Meng X, Li Y, Wang DB, Jiang Y, Shao HB, Zhang YY (2017) Isolation and genome sequencing of a novel Pseudoalteromonas phage PH1. Curr Microbiol 74:1–7.  https://doi.org/10.1007/s00284-016-1175-9 CrossRefGoogle Scholar
  26. 26.
    Xu YQ, Ma YY, Yao S, Jiang ZY, Pei JS, Cheng C (2016) Characterization, genome sequence, and analysis of Escherichia phage CICC 80001, a bacteriophage infecting an efficient l-aspartic acid producing Escherichia coli. Food Environ Virol 8:18–26.  https://doi.org/10.1007/s12560-015-9218-0 CrossRefGoogle Scholar
  27. 27.
    Sullivan MJ, Petty NK, Beatson SA (2011) Easyfig: a genome comparison visualizer. Bioinformatics 27:1009–1010.  https://doi.org/10.1093/bioinformatics/btr039 CrossRefGoogle Scholar
  28. 28.
    Lipps G, Weinzierl AO, von Scheven G, Buchen C, Cramer P (2004) Structure of a bifunctional DNA primase-polymerase. Nat Struct Mol Biol 11:157–162.  https://doi.org/10.1038/nsmb723 CrossRefGoogle Scholar
  29. 29.
    Gao Y, Liu Q, Wang M, Zhao GH, Jiang Y, Malin G, Gong Z, Meng X, Liu ZY, Lin TT, Li YT, Shao HB (2017) Characterization and genome sequence of marine Alteromonas gracilis phage PB15 isolated from the Yellow Sea, China. Curr Microbiol 74:821–826.  https://doi.org/10.1007/s00284-017-1251-9 CrossRefGoogle Scholar
  30. 30.
    Yuan L, Cui Z, Wang Y, Guo X, Zhao Y (2014) Complete genome sequence of virulent bacteriophage SHOU24, which infects foodborne pathogenic Vibrio parahaemolyticus. Adv Virol 159:3089–3093.  https://doi.org/10.1007/s00705-014-2160-x Google Scholar
  31. 31.
    Li P, Chen B, Song Z, Song Y, Yang Y, Ma P, Wang H, Ying J, Ren P, Yang L, Gao G, Jin S, Bao Q, Yang H (2012) Bioinformatic analysis of the Acinetobacter baumannii phage AB1 genome. Gene 507:125–134.  https://doi.org/10.1016/j.gene.2012.07.029 CrossRefGoogle Scholar
  32. 32.
    Halgasova N, Mesarosova I, Bukovska G (2012) Identification of a bifunctional primase–polymerase domain of corynephage BFK20 replication protein gp43. Virus Res 163:454–460.  https://doi.org/10.1016/j.virusres.2011.11.005 CrossRefGoogle Scholar
  33. 33.
    Black LW (1989) DNA Packaging in dsDNA bacteriophages. Annu Rev Microbiol 43:267–292.  https://doi.org/10.1146/annurev.mi.43.100189.001411 CrossRefGoogle Scholar
  34. 34.
    Roy A, Bhardwaj A, Datta P, Lander GC, Cingolani G (2012) Small terminase couples viral DNA binding to genome-packaging atpase activity. Structure 20:1403–1413.  https://doi.org/10.1016/j.str.2012.05.014 CrossRefGoogle Scholar
  35. 35.
    Li E, Xiao W, Ma Y, Zhe Y, Li H, Lin W, Wang X, Li C, Shen Z, Zhao R, Yang H, Jiang A, Yang W, Yuan J, Zhao X (2016) Isolation and characterization of a bacteriophage phiEap-2 infecting multidrug resistant enterobacter aerogenes. Sci Rep 6:28338.  https://doi.org/10.1038/srep28338 CrossRefGoogle Scholar
  36. 36.
    Xu J, Hendrix RW, Duda RL (2004) Conserved translational frameshift in dsDNA bacteriophage tail assembly genes. Mol Cell 16:11–21.  https://doi.org/10.1016/j.molcel.2004.09.006 CrossRefGoogle Scholar
  37. 37.
    Kropinski AM, Waddell T, Meng J, Franklin K, Ackermann HW, Ahmed R, Mazzocco A, Yates J, Lingohr EJ, Johnson RP (2013) The host-range, genomics and proteomics of Escherichia coli, O157:H7 bacteriophage rV5. Virol J 10:1–12.  https://doi.org/10.1186/1743-422X-10-76 CrossRefGoogle Scholar
  38. 38.
    Colangelo-Lillis JR, Deming JW (2013) Genomic analysis of cold-active Colwelliaphage 9A and psychrophilic phage-host interactions. Extremophiles 17:99–114.  https://doi.org/10.1007/s00792-012-0497-1 CrossRefGoogle Scholar
  39. 39.
    Lavigne R, Seto D, Mahadevan P, Ackermann HW, Kropinski AM (2008) Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using blastp-based tools. Res Microbiol 159:406–414.  https://doi.org/10.1016/j.resmic.2008.03.005 CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Yundan Liu
    • 1
  • Lei Zhao
    • 3
  • Min Wang
    • 1
    • 2
    • 4
    Email author
  • Qi Wang
    • 1
  • Xinran Zhang
    • 1
  • Yuye Han
    • 1
  • Meiwen Wang
    • 1
  • Tong Jiang
    • 1
  • Hongbing Shao
    • 1
    • 2
  • Yong Jiang
    • 1
    • 2
    • 4
  • Andrew McMinn
    • 5
  1. 1.College of Marine Life SciencesOcean University of ChinaQingdaoPeople’s Republic of China
  2. 2.Institute of Evolution and Marine BiodiversityOcean University of ChinaQingdaoPeople’s Republic of China
  3. 3.Qing Dao Municipal HospitalQingdaoPeople’s Republic of China
  4. 4.Key Lab of Polar Oceanography and Global Ocean ChangeOcean University of ChinaQingdaoPeople’s Republic of China
  5. 5.Institute for Marine and Antarctic StudiesUniversity of TasmaniaHobartAustralia

Personalised recommendations