Skip to main content

Advertisement

SpringerLink
Log in

Characterization and Complete Genome Sequences of Three N4-Like Roseobacter Phages Isolated from the South China Sea

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Three bacteriophages (RD-1410W1-01, RD-1410Ws-07, and DS-1410Ws-06) were isolated from the surface water of Sanya Bay, northern South China Sea, on two marine bacteria type strains of the Roseobacter lineage. These phages have an isometric head and a short tail, morphologically belonging to the Podoviridae family. Two of these phages can infect four of seven marine roseobacter strains tested and the other one can infect three of them, showing relatively broader host ranges compared to known N4-like roseophages. One-step growth curves showed that these phages have similar short latent periods (1–2 h) but highly variable burst sizes (27–341 pfu cell−1). Their complete genomes show high level of similarities to known N4-like roseophages in terms of genome size, G + C content, gene content, and arrangement. The morphological and genomic features of these phages indicate that they belong to the N4likevirus genus. Moreover, comparative genomic analysis based on 43 N4-like phages (10 roseobacter phages and 33 phages infecting other lineages of bacteria) revealed a core genome of 18 genes shared by all the 43 phages and 38 genes shared by all the ten roseophages. The 38 core genes of N4-like roseophages nearly make up 70 % of each genome in length. Phylogenetic analysis based on the concatenated core gene products showed that our phage isolates represent two new phyletic branches, suggesting the broad genetic diversity of marine N4-like roseophages remains.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Angly F, Youle M, Nosrat B et al (2009) Genomic analysis of multiple Roseophage SIO1 strains. Environ Microbiol 11(11):2863–2873

    Article  CAS  PubMed  Google Scholar 

  2. Ankrah NY, Budinoff CR, Wilson WH et al (2014) Genome sequence of the Sulfitobacter sp. strain 2047-infecting lytic phage ΦCB2047-B. Genome Announc 2(1):e00945-00913

    Article  Google Scholar 

  3. Ankrah NY, Budinoff CR, Wilson WH et al (2014) Genome sequences of two temperate phages, ΦCB2047-A and ΦCB2047-C, infecting Sulfitobacter sp. strain 2047. Genome Announc 2(3):e00108-00114

    Article  Google Scholar 

  4. Breitbart M, Thompson LR, Suttle CA et al (2007) Exploring the vast diversity of marine viruses. Oceanography 20(2):135–139

    Article  Google Scholar 

  5. Cai L, Yang Y, Jiao N et al (2015) Complete genome sequence of vB_DshP-R2C, a N4-like lytic roseophage. Mar Genomics 22:15–17

    Article  PubMed  Google Scholar 

  6. Chan JZ, Millard AD, Mann NH et al (2014) Comparative genomics defines the core genome of the growing N4-like phage genus and identifies N4-like Roseophage specific genes. Front Microbiol 5(506):506

    PubMed  PubMed Central  Google Scholar 

  7. Holmfeldt K, Howard-Varona C, Solonenko N et al (2014) Contrasting genomic patterns and infection strategies of two co-existing Bacteroidetes podovirus genera. Environ Microbiol 16(8):2501–2513

    Article  CAS  PubMed  Google Scholar 

  8. Huang S, Zhang S, Jiao N et al (2015) Comparative genomic and phylogenomic analyses reveal a conserved core genome shared by estuarine and oceanic cyanopodoviruses. PLoS One 10(11):e0142962

    Article  PubMed  PubMed Central  Google Scholar 

  9. Huang S, Zhang Y, Chen F et al (2011) Complete genome sequence of a marine roseophage provides evidence into the evolution of gene transfer agents in alphaproteobacteria. Virol J 8:124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Ji J, Zhang R, Jiao N (2014) Complete genome sequence of Roseophage vB_DshP-R1, which infects Dinoroseobacter shibae DFL12. Stand Genomic Sci 9:31

    PubMed  Google Scholar 

  11. Kang I, Jang H, Oh HM et al (2012) Complete genome sequence of Celeribacter bacteriophage P12053L. J Virol 86(15):8339–8340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Krumsiek J, Arnold R, Rattei T (2007) Gepard: a rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics 23(8):1026–1028

    Article  CAS  PubMed  Google Scholar 

  13. Labrie SJ, Frois-Moniz K, Osburne MS et al (2013) Genomes of marine cyanopodoviruses reveal multiple origins of diversity. Environ Microbiol 15(5):1356–1376

    Article  CAS  PubMed  Google Scholar 

  14. Larkin MA, Blackshields G, Brown NP et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948

    Article  CAS  PubMed  Google Scholar 

  15. Liang Y, Zhang Y, Zhou C et al (2016) Complete genome sequence of the siphovirus Roseophage RDJLPhi 2 infecting Roseobacter denitrificans OCh114. Mar Genomics 25:17–19

    Article  PubMed  Google Scholar 

  16. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25(5):955–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Lukashin AV, Borodovsky M (1998) GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res 26(4):1107–1115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Newton RJ, Griffin LE, Bowles KM et al (2010) Genome characteristics of a generalist marine bacterial lineage. ISME J 4(6):784–798

    Article  CAS  PubMed  Google Scholar 

  19. Rohwer F, Segall A, Steward G et al (2000) The complete genomic sequence of the marine phage Roseophage SIO1 shares homology with nonmarine phages. Limnol Oceanogr 45(2):408–418

    Article  CAS  Google Scholar 

  20. Suttle CA (2005) Viruses in the sea. Nature 437(7057):356–361

    Article  CAS  PubMed  Google Scholar 

  21. Suttle CA (2007) Marine viruses–major players in the global ecosystem. Nat Rev Microbiol 5(10):801–812

    Article  CAS  PubMed  Google Scholar 

  22. Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56(4):564–577

    Article  CAS  PubMed  Google Scholar 

  23. Tamura K, Stecher G, Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Wagner-Dobler I, Biebl H (2006) Environmental biology of the marine Roseobacter lineage. Annu Rev Microbiol 60:255–280

    Article  PubMed  Google Scholar 

  25. Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28(2):127–181

    Article  CAS  PubMed  Google Scholar 

  26. Wittmann J, Klumpp J, Moreno Switt AI et al (2015) Taxonomic reassessment of N4-like viruses using comparative genomics and proteomics suggests a new subfamily—“Enquartavirinae”. Arch Virol 160(12):3053–3062

    Article  CAS  PubMed  Google Scholar 

  27. Zhao Y, Wang K, Jiao N et al (2009) Genome sequences of two novel phages infecting marine roseobacters. Environ Microbiol 11(8):2055–2064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank our colleagues at the CAS Tropical Marine Biological Research Station in Hainan for their help in sampling. We also thank Li Yinyin at Sun Yat-sen University for her assistance in TEM. This work was supported by the NSFC grants 41576126 (SH), 41206131 (SH), and 41230962 (SZ).

Author information

Authors and Affiliations

  1. CAS Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Science, 164 Xingangxi St., Guangzhou, China

    Baolian Li, Si Zhang, Lijuan Long & Sijun Huang

  2. Graduate University of CAS, Beijing, China

    Baolian Li

Authors
  1. Baolian Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Si Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lijuan Long
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sijun Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Lijuan Long or Sijun Huang.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 34 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, B., Zhang, S., Long, L. et al. Characterization and Complete Genome Sequences of Three N4-Like Roseobacter Phages Isolated from the South China Sea. Curr Microbiol 73, 409–418 (2016). https://doi.org/10.1007/s00284-016-1071-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-016-1071-3

Keywords

Search

Navigation