Skip to main content

Advertisement

SpringerLink
Log in

Isolation and complete genome sequence of a novel cyanophage, S-B05, infecting an estuarine Synechococcus strain: insights into environmental adaptation

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

A new cyanophage, S-B05, infecting a phycoerythrin-enriched (PE-type) Synechococcus strain was isolated by the liquid infection method, and its morphology and genetic features were examined. Phylogenetic analysis and morphological observation confirmed that S-B05 belongs to the family Myoviridae of the order Caudovirales. Its genome was fully sequenced, and found to be 208,857 bp in length with a G + C content of 39.9%. It contained 280 potential open reading frames and 123 conserved domains. Ninety-eight functional genes responsible for cyanophage structuring and packaging, DNA replication and regulation, and photosynthesis were identified, as well as genes encoding 172 hypothetical proteins. The genome of S-B05 is most similar to that of Prochlorococcus phage P-TIM68. Homologues of open reading frames of S-B05 can be found in various marine environments, as revealed by comparison of the S-B05 genome sequence to sequences in marine viral metagenomic databases. The presence of auxiliary metabolic genes (AMGs) related to photosynthesis, carbon metabolism, and phosphorus assimilation, as well as the phylogenetic relationships based on AMGs and the complete genome sequence, reflect the phage-host interaction mechanism or the specific adaptation strategy of the host to environmental conditions. The genome sequence information reported here will provide an important basis for further study of the adaptive evolution and ecological role of cyanophages and their hosts in the marine environment.

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
Fig. 5

Similar content being viewed by others

References

  1. Carmichael W (1994) The toxins of cyanobacteria. Sci Am 270(1):78–86. https://www.jstor.org/stable/24942554

  2. Flombaum P, Gallegos JL, Gordillo RA, Rincón J, Zabala LL, Jiao N, Karl DM, Li WKW, Lomas MW, Veneziano D, Vera CS, Vrugt JA, Martiny AC (2013) Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. PNAS 110(24):9824–9829. https://doi.org/10.1073/pnas.1307701110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Buitenhuis ET, Li WKW, Vaulot D, Lomas MW, Landry MR, Partensky F, Karl DM, Ulloa O, Campbell L, Jacquet S, Lantoine F, Chavez F, Macias D, Gosselin M, McManus GB (2012) Picophytoplankton biomass distribution in the global ocean. Earth Syst Sci Data 4(1):37–46. https://doi.org/10.5194/essd-4-37-2012

    Article  Google Scholar 

  4. Xia X, Vidyarathna NK, Palenik B, Lee P, Liu H (2015) Comparison of the seasonal variations of Synechococcus Assemblage structures in estuarine waters and coastal waters of Hong Kong. Appl Environ Microbiol 81(21):7644. https://doi.org/10.1128/AEM.01895-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Haverkamp T, Schouten D, Doeleman M et al (2009) Colorful microdiversity of Synechococcus strains (picocyanobacteria) isolated from the baltic sea. ISME J 3(4):397. https://doi.org/10.1038/ismej.2008.118

    Article  CAS  PubMed  Google Scholar 

  6. Suttle C, Chan A, Cottrell M (1990) Infection of phytoplankton by viruses and reduction of primary productivity. Nature 347:467–469. https://doi.org/10.1038/347467a0

    Article  Google Scholar 

  7. Suttle C (2000) Cyanophages and their role in the ecology of cyanobacteria. In: Whitton B, Potts M (eds) The ecology of cyanobacteria. Springer, Dordrecht, pp 563–589. https://doi.org/10.1007/0-306-46855-7_20

  8. Suttle C (1994) Dynamics and distribution of cyanophages and their effect on marine Synechococcus spp. Appl Environ Microbiol 60(9):3167–3174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Marston MF, Martiny JB (2016) Genomic diversification of marine cyanophages into stable ecotypes. Environ Microbiol 18(11):4240–4253. https://doi.org/10.1111/1462-2920.13556

    Article  CAS  PubMed  Google Scholar 

  10. Gregory A, Solonenko S, Ignacio-Espinoza J et al (2016) Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer. BMC Genom. https://doi.org/10.1186/s12864-016-3286-x

    Article  Google Scholar 

  11. Yang Q, Gao C, Jiang Y, Wang M, Zhou X, Shao H, Gong Z, McMinn A (2019) Metagenomic characterization of the viral community of the South Scotia Ridge. Viruses 11(2):95. https://doi.org/10.3390/v11020095

    Article  CAS  PubMed Central  Google Scholar 

  12. Wilhelm S, Carberry M, Eldridge M et al (2006) Marine and freshwater cyanophages in a Laurentian Great Lake: evidence from infectivity assays and molecular analyses of g20 genes. Appl Environ Microbiol 72(7):4957–4963. https://doi.org/10.1128/AEM.00349-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Wilson W, Joint I, Carr N et al (1993) Isolation and molecular characterization of five marine cyanophages propagated on Synechococcus sp. Strain WH7803. Appl Environ Microbiol 59(11):3736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Caroline C, Sandra K, Lauro FM (2018) Complete genome sequence of the cyanophage S-PRM1 isolated from Singapore coastal waters. Mar Genom 43:58–60. https://doi.org/10.1016/j.margen.2018.08.005

    Article  Google Scholar 

  15. Vidaver AK, Koski RK, Etten JLV (1973) Bacteriophage φ6: a lipid-containing virus of pseudomonas phaseolicola. J Virol 11(5):799–805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Deveau H, Labrie SJ, Chopin MC et al (2006) Biodiversity and classification of lactococcal phages. Appl Environ Microbiol 72(6):4338–4346. https://doi.org/10.1128/AEM.02517-05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. You S, Wang M, Jiang Y et al (2019) The genome sequence of a novel cyanophage S-B64 from the Yellow Sea, China. Curr Microbiol 76:681–686. https://doi.org/10.1007/s00284-019-01680-1

    Article  CAS  PubMed  Google Scholar 

  18. Buttimer C, Born Y, Lucid A, Loessner MJ, Fieseler L, Coffey A (2018) Erwinia amylovora phage vB_EamM_Y3 represents another lineage of hairy Myoviridae. Res Microbiol 169(9):505–514. https://doi.org/10.1016/j.resmic.2018.04.006

    Article  CAS  PubMed  Google Scholar 

  19. 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. https://doi.org/10.1093/nar/25.5.955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Nishimura Y, Yoshida T, Kuronishi M, Uehara H, Ogata H, Goto S (2017) ViPTree: the viral proteomic tree server. Bioinformatics 33:2379–2380. https://doi.org/10.1093/bioinformatics/btx157

    Article  CAS  PubMed  Google Scholar 

  21. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454

    Article  CAS  PubMed  Google Scholar 

  22. Lee I, Kim YO, Park SC, Chun J (2015) OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 66(2):1100. https://doi.org/10.1099/ijsem.0.000760

    Article  CAS  PubMed  Google Scholar 

  23. Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S et al (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Hurwitz BL, Sullivan MB (2013) The Pacific Ocean Virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS ONE 8:e57355. https://doi.org/10.1371/journal.pone.0057355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Xu Y, Zhang R, Wang N, Cai L, Tong Y, Sun Q, Chen F, Jiao N (2018) Novel phage–host interactions and evolution as revealed by a cyanomyovirus isolated from an estuarine environment. Environ Microbiol 20:2974–2989. https://doi.org/10.1111/1462-2920.14326

    Article  CAS  PubMed  Google Scholar 

  26. Lu L, Cai L, Jiao N et al (2017) Isolation and characterization of the first phage infecting ecologically important marine bacteria Erythrobacter. Virol J. https://doi.org/10.1186/s12985-017-0773-x

    Article  PubMed  PubMed Central  Google Scholar 

  27. Liu Z, Wang M, Meng X et al (2017) Isolation and genome sequencing of a novel Pseudoalteromonas phage PH1. Curr Microbiol 74(2):1–7. https://doi.org/10.1007/s00284-016-1175-9

    Article  CAS  Google Scholar 

  28. Dreher TW, Brown N, Bozarth CS, Schwartz AD, Riscoe E, Thrash C et al (2011) A freshwater cyanophage whose genome indicates close relationships to photosynthetic marine cyanomyophages. Environ Microbiol 13(7):1858–1874. https://doi.org/10.1111/j.1462-2920.2011.02502.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Mann NH, Clokie MRJ, Millard A et al (2005) The genome of S-PM2, a "Photosynthetic" T4-Type bacteriophage that infects marine Synechococcus strains. J Bacteriol 187(9):3188–3200. https://doi.org/10.1128/JB.187.9.3188-3200.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Enav H, Béjà O, Mandel-Gutfreund Y (2012) Cyanophage tRNAs may have a role in cross-infectivity of oceanic Prochlorococcus and Synechococcus hosts. ISME J 6:619–628. https://doi.org/10.1038/ismej.2011.146

    Article  CAS  PubMed  Google Scholar 

  31. Sullivan MB, Huang KH, Ignacio-Espinoza JC et al (2010) Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ Microbiol 12(11):3035–3056. https://doi.org/10.1111/j.1462-2920.2010.02280.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Crummett LT, Puxty RJ, Weihe C (2016) The genomic content and context of auxiliary metabolic genes in marine cyanomyoviruses. Virology 499:219–229. https://doi.org/10.1016/j.virol.2016.09.016

    Article  CAS  PubMed  Google Scholar 

  33. Mann N, Cook A, Millard A, Bailey S, Clokie M (2003) Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424:741–741. https://doi.org/10.1038/424741a

    Article  CAS  PubMed  Google Scholar 

  34. Philosof A, Battchikova N, Aro E, Beja O (2011) Marine cyanophages: tinkering with the electron transport chain. ISME J 5:1568–1570. https://doi.org/10.1038/ismej.2011.43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Thompson L, Zeng Q, Kelly L, Huang K, Singer A, Stubbe J, Chisholm S (2011) Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. PNAS 108(39):E757–E764. https://doi.org/10.1073/pnas.1102164108

    Article  PubMed  PubMed Central  Google Scholar 

  36. Dwivedi B, Xue B, Lundin D, Edwards R, Breitbart M (2013) A bioinformatic analysis of ribonucleotide reductase genes in phage genomes and metagenomes. BMC Evol Biolss. https://doi.org/10.1186/1471-2148-13-33

  37. Hagay E, Mandel-Gutfreund Y, Béjà O (2014) Comparative metagenomics analyses reveal viral-induced shifts of host metabolism towards nucleotide biosysnthesis. Microbiome. https://doi.org/10.1186/2049-2618-2-9

    Article  Google Scholar 

  38. Kelly L, Ding H, Huang K, Osburne M, Chisholm S (2013) Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent. ISME J 7:1827–1841. https://doi.org/10.1038/ismej.2013.58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Millard AD, Zwirglmaier K, Downey MJ et al (2009) Comparative genomics of marine cyanomyoviruses reveals the widespread occurrence of Synechococcus host genes localized to a hyperplastic region: implications for mechanisms of cyanophage evolution. Environ Microbiol 11(9):2370–2387. https://doi.org/10.1111/j.1462-2920.2009.01966.x

    Article  CAS  PubMed  Google Scholar 

  40. Huang S, Wang K, Jiao N (2012) Genome sequences of siphoviruses infecting marine Synechococcus unveil a diverse cyanophage group and extensive phage–host genetic exchanges. Environ Microbiol 14(2):540–558. https://doi.org/10.1111/j.1462-2920.2011.02667.x

    Article  CAS  PubMed  Google Scholar 

  41. Gao E, Ning D (2014) Advances in researches on cyanophage auxiliary metabolic genes. Microbiol China 41(8):1667–1674. https://doi.org/10.13344/j.microbiol.china.130650

  42. Lindell D, Jaffe JD, Johnson ZI et al (2005) Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438(7064):86–89. https://doi.org/10.1038/nature04111

    Article  CAS  PubMed  Google Scholar 

  43. Lindell D, Sullivan MB, Johnson ZI et al (2004) Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci 101(30):11013–11018. https://doi.org/10.1073/pnas.0401526101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Zeidner G, Bielawski JP, Shmoish M et al (2010) Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environ Microbiol 7(10):1505–1513. https://doi.org/10.1111/j.1462-2920.2005.00833.x

    Article  CAS  Google Scholar 

  45. Sullivan MB, Lindell D, Lee JA, Thompson LR, Bielawski JP, Chisholm SW (2006) Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol. https://doi.org/10.1371/journal.pbio.0040234

    Article  PubMed  PubMed Central  Google Scholar 

  46. Bograh A, Gingras Y, Tajmir-Riahi HA et al (1997) The effects of spermine and spermidine on the structure of photosystem II proteins in relation to inhibition of electron transport. FEBS Lett 402(1):41–44. https://doi.org/10.1016/S0014-5793(96)01453-6

    Article  CAS  PubMed  Google Scholar 

  47. Sullivan MB, Coleman ML, Weigele P et al (2005) Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3(5):e144. https://doi.org/10.1371/journal.pbio.0030144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Bryan MJ, Burroughs NJ, Spence EM et al (2008) Evidence for the intense exchange of MazG in marine cyanophages by horizontal gene transfer. PLoS ONE 3(4):e2048. https://doi.org/10.1371/journal.pone.0002048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Ignacio-Espinoza JC, Sullivan MB (2012) Phylogenomics of T4 cyanophages: lateral gene transfer in the ‘core’ and origins of host genes. Environ Microbiol 14(8):2113–2126. https://doi.org/10.1111/j.1462-2920.2012.02704.x

    Article  CAS  PubMed  Google Scholar 

  50. Li X, Sun Y, Wang X, Liu J, Wang G (2017) Research progress of new biomarker gene of phoH for bacteriophage genetic diversity. Biotechnol Bull 33(10):40–45. https://doi.org/10.13560/j.cnki.biotech.bull.1985.2017-0725

  51. Xu J, Glibert PM, Liu H et al (2012) Nitrogen sources and rates of phytoplankton uptake in different regions of Hong Kong waters in summer. Estuaries Coasts 35(2):559–571. https://doi.org/10.1007/s12237-011-9456-9

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the Natural Science Foundation of China (No. 41906126; 41976117; 41676178), and the Open Research Fund of LMB, SCSIO (LMB20091001). We sincerely thank Dr. Xia X. from SCSIO for isolating and providing the Synechococcus culture. We also thank the captain and crew of R/V Dongfanghong II, as well as the students and staff on board the cruise.

Author information

Authors and Affiliations

  1. College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, China

    Tong Jiang, Cui Guo, Min Wang, Meiwen Wang, Siyuan You, Yundan Liu, Xinran Zhang, Yong Jiang, Hongbing Shao, Yantao Liang & Andrew McMinn

  2. Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, 266003, China

    Cui Guo, Min Wang, Yong Jiang & Yantao Liang

  3. Key Lab of Polar Oceanography and Global Ocean Change, Ocean University of China, Qingdao, 266003, China

    Cui Guo, Min Wang, Yong Jiang & Yantao Liang

  4. Department of Ocean Science, Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong SAR, China

    Hongbin Liu

  5. Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Australia

    Andrew McMinn

Authors
  1. Tong Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cui Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Min Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Meiwen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Siyuan You
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yundan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xinran Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hongbin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yong Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hongbing Shao
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yantao Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Andrew McMinn
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cui Guo.

Additional information

Handling Editor: Johannes Wittmann.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 1731 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, T., Guo, C., Wang, M. et al. Isolation and complete genome sequence of a novel cyanophage, S-B05, infecting an estuarine Synechococcus strain: insights into environmental adaptation. Arch Virol 165, 1397–1407 (2020). https://doi.org/10.1007/s00705-020-04595-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-020-04595-6

Search

Navigation