Skip to main content
Log in

A novel temperate phage, vB_PstS-pAN, induced from the naphthalene-degrading bacterium Pseudomonas stutzeri AN10

  • Brief Report
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

A novel temperate phage named vB_PstS-pAN was induced by mitomycin C treatment from the naphthalene-degrading bacterium Pseudomonas stutzeri AN10. The phage particles have icosahedral heads and long non-contractile tails, and vB_PstS-pAN can therefore be morphologically classified as a member of the family Siphoviridae. The whole genome of vB_PstS-pAN is 39,466 bp in length, with an 11-nt 3’ overhang cohesive end. There are 53 genes in the vB_PstS-pAN genome, including genes responsible for phage integration, replication, morphogenesis, and bacterial lysis. The vB_PstS-pAN genome has low similarity to other phage genomes in the GenBank database, suggesting that vB_PstS-pAN is a novel member of the family Siphoviridae.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Availability of data and material

The complete genome sequence of vB_PstS-pAN is available in the GenBank database under the accession number MW651859.

References

  1. Touchon M, Bernheim A, Rocha EP (2016) Genetic and life-history traits associated with the distribution of prophages in bacteria. ISME J 10(11):2744–2754. https://doi.org/10.1038/ismej.2016.47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Fortier LC, Sekulovic O (2013) Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 4(5):354–365. https://doi.org/10.4161/viru.24498

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bondy-Denomy J, Qian J, Westra ER, Buckling A, Guttman DS, Davidson AR, Maxwell KL (2016) Prophages mediate defense against phage infection through diverse mechanisms. ISME J 10(12):2854–2866. https://doi.org/10.1038/ismej.2016.79

    Article  PubMed  PubMed Central  Google Scholar 

  4. Cornuault JK, Moncaut E, Loux V, Mathieu A, Sokol H, Petit MA, De Paepe M (2020) The enemy from within: a prophage of Roseburia intestinalis systematically turns lytic in the mouse gut, driving bacterial adaptation by CRISPR spacer acquisition. ISME J 14(3):771–787. https://doi.org/10.1038/s41396-019-0566-x

    Article  CAS  PubMed  Google Scholar 

  5. De Smet J, Hendrix H, Blasdel BG, Danis-Wlodarczyk K, Lavigne R (2017) Pseudomonas predators: understanding and exploiting phage-host interactions. Nat Rev Microbiol 15(9):517–530. https://doi.org/10.1038/nrmicro.2017.61

    Article  CAS  PubMed  Google Scholar 

  6. Rice SA, Tan CH, Mikkelsen PJ, Kung V, Woo J, Tay M, Hauser A, McDougald D, Webb JS, Kjelleberg S (2009) The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. ISME J 3(3):271–282. https://doi.org/10.1038/ismej.2008.109

    Article  CAS  PubMed  Google Scholar 

  7. Martinez-Garcia E, Jatsenko T, Kivisaar M, de Lorenzo V (2015) Freeing Pseudomonas putida KT2440 of its proviral load strengthens endurance to environmental stresses. Environ Microbiol 17(1):76–90. https://doi.org/10.1111/1462-2920.12492

    Article  CAS  PubMed  Google Scholar 

  8. Lalucat J, Bennasar A, Bosch R, Garcia-Valdes E, Palleroni NJ (2006) Biology of Pseudomonas stutzeri. Microbiol Mol Biol Rev 70(2):510–547. https://doi.org/10.1128/MMBR.00047-05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. de Sousa LP (2020) Mobile genetic elements in Pseudomonas stutzeri. Curr Microbiol 77(2):179–184. https://doi.org/10.1007/s00284-019-01812-7

    Article  CAS  PubMed  Google Scholar 

  10. Garcia-Valdes E, Cozar E, Rotger R, Lalucat J, Ursing J (1988) New naphthalene-degrading marine Pseudomonas strains. Appl Environ Microbiol 54(10):2478–2485. https://doi.org/10.1128/AEM.54.10.2478-2485.1988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bosch R, Garcia-Valdes E, Moore ER (1999) Genetic characterization and evolutionary implications of a chromosomally encoded naphthalene-degradation upper pathway from Pseudomonas stutzeri AN10. Gene 236(1):149–157. https://doi.org/10.1016/s0378-1119(99)00241-3

    Article  CAS  PubMed  Google Scholar 

  12. Bosch R, Garcia-Valdes E, Moore ER (2000) Complete nucleotide sequence and evolutionary significance of a chromosomally encoded naphthalene-degradation lower pathway from Pseudomonas stutzeri AN10. Gene 245(1):65–74. https://doi.org/10.1016/s0378-1119(00)00038-x

    Article  CAS  PubMed  Google Scholar 

  13. Brunet-Galmes I, Busquets A, Pena A, Gomila M, Nogales B, Garcia-Valdes E, Lalucat J, Bennasar A, Bosch R (2012) Complete genome sequence of the naphthalene-degrading bacterium Pseudomonas stutzeri AN10 (CCUG 29243). J Bacteriol 194(23):6642–6643. https://doi.org/10.1128/JB.01753-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Zhang W, Mi Z, Yin X, Fan H, An X, Zhang Z, Chen J, Tong Y (2013) Characterization of Enterococcus faecalis phage IME-EF1 and its endolysin. PLoS ONE 8(11):e80435. https://doi.org/10.1371/journal.pone.0080435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Feng Z, Liu X, Liu W, Nie Y, Wu X (2020) Complete genome sequence of a novel Bacillus phage, P59, that infects Bacillus oceanisediminis. Arch Virol 165(11):2679–2683. https://doi.org/10.1007/s00705-020-04761-w

    Article  CAS  PubMed  Google Scholar 

  16. Liu X, Feng Z, Fan X, Nie Y, Wu XL (2021) Isolation and characterization of the novel Pseudomonas stutzeri bacteriophage 8P. Arch Virol 166(2):601–606. https://doi.org/10.1007/s00705-020-04912-z

    Article  CAS  PubMed  Google Scholar 

  17. Kropinski AM, Prangishvili D, Lavigne R (2009) Position paper: the creation of a rational scheme for the nomenclature of viruses of Bacteria and Archaea. Environ Microbiol 11(11):2775–2777. https://doi.org/10.1111/j.1462-2920.2009.01970.x

    Article  PubMed  Google Scholar 

  18. Wang R, Xing S, Zhao F, Li P, Mi Z, Shi T, Liu H, Tong Y (2018) Characterization and genome analysis of novel phage vB_EfaP_IME195 infecting Enterococcus faecalis. Virus Genes 54(6):804–811. https://doi.org/10.1007/s11262-018-1608-6

    Article  CAS  PubMed  Google Scholar 

  19. Schubert M, Lindgreen S, Orlando L (2016) AdapterRemoval v2: rapid adapter trimming, identification, and read merging. BMC Res Notes 9:88. https://doi.org/10.1186/s13104-016-1900-2

    Article  PubMed  PubMed Central  Google Scholar 

  20. Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y, Tang J, Wu G, Zhang H, Shi Y, Liu Y, Yu C, Wang B, Lu Y, Han C, Cheung DW, Yiu SM, Peng S, Xiaoqian Z, Liu G, Liao X, Li Y, Yang H, Wang J, Lam TW, Wang J (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1(1):18. https://doi.org/10.1186/2047-217X-1-18

    Article  PubMed  PubMed Central  Google Scholar 

  21. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25(14):1754–1760. https://doi.org/10.1093/bioinformatics/btp324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079. https://doi.org/10.1093/bioinformatics/btp352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Arndt D, Grant JR, Marcu A, Sajed T, Pon A, Liang YJ, Wishart DS (2016) PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 44(W1):W16–W21. https://doi.org/10.1093/nar/gkw387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Mavrich TN, Casey E, Oliveira J, Bottacini F, James K, Franz C, Lugli GA, Neve H, Ventura M, Hatfull GF, Mahony J, van Sinderen D (2018) Characterization and induction of prophages in human gut-associated Bifidobacterium hosts. Sci Rep 8(1):12772. https://doi.org/10.1038/s41598-018-31181-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Garneau JR, Depardieu F, Fortier LC, Bikard D, Monot M (2017) PhageTerm: a tool for fast and accurate determination of phage termini and packaging mechanism using next-generation sequencing data. Sci Rep 7(1):8292. https://doi.org/10.1038/s41598-017-07910-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Fan X, Yan J, Xie L, Zeng L, Young RF 3rd, Xie J (2015) Genomic and proteomic features of mycobacteriophage SWU1 isolated from China soil. Gene 561(1):45–53. https://doi.org/10.1016/j.gene.2015.02.053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Coil D, Jospin G, Darling AE (2015) A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data. Bioinformatics 31(4):587–589. https://doi.org/10.1093/bioinformatics/btu661

    Article  CAS  PubMed  Google Scholar 

  28. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477. https://doi.org/10.1089/cmb.2012.0021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL (2004) Versatile and open software for comparing large genomes. Genome Biol 5(2):R12. https://doi.org/10.1186/gb-2004-5-2-r12

    Article  PubMed  PubMed Central  Google Scholar 

  30. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK, Earl AM (2014) Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9(11):e112963. https://doi.org/10.1371/journal.pone.0112963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Zulkower V, Rosser S (2020) DNA features viewer: a sequence annotation formatting and plotting library for Python. Bioinformatics 36(15):4350–4352. https://doi.org/10.1093/bioinformatics/btaa213

    Article  CAS  PubMed  Google Scholar 

  32. Kala S, Cumby N, Sadowski PD, Hyder BZ, Kanelis V, Davidson AR, Maxwell KL (2014) HNH proteins are a widespread component of phage DNA packaging machines. Proc Natl Acad Sci USA 111(16):6022–6027. https://doi.org/10.1073/pnas.1320952111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Fogg PC, Colloms S, Rosser S, Stark M, Smith MC (2014) New applications for phage integrases. J Mol Biol 426(15):2703–2716. https://doi.org/10.1016/j.jmb.2014.05.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Song J, Xia F, Jiang H, Li X, Hu L, Gong P, Lei L, Feng X, Sun C, Gu J, Han W (2016) Identification and characterization of HolGH15: the holin of Staphylococcus aureus bacteriophage GH15. J Gen Virol 97(5):1272–1281. https://doi.org/10.1099/jgv.0.000428

    Article  CAS  PubMed  Google Scholar 

  35. Bie L, Fang M, Li Z, Wang M, Xu H (2018) Identification and characterization of new resistance-conferring SGI1s (Salmonella Genomic Island 1) in Proteus mirabilis. Front Microbiol 9:3172. https://doi.org/10.3389/fmicb.2018.03172

    Article  PubMed  PubMed Central  Google Scholar 

  36. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Tuttle MJ, Buchan A (2020) Lysogeny in the oceans: lessons from cultivated model systems and a reanalysis of its prevalence. Environ Microbiol 22(12):4919–4933. https://doi.org/10.1111/1462-2920.15233

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key R&D Program of China (2018YFA0902100 and 2018YFA0902103), and the National Natural Science Foundation of China (91951204).

Funding

This work was supported by the National Key R&D Program of China (2018YFA0902100 and 2018YFA0902103), and the National Natural Science Foundation of China (91951204).

Author information

Authors and Affiliations

Authors

Contributions

X-LW and YN designed the study. ZF, XL, and MW performed experiments and analyzed data. The first draft of the manuscript was written by ZF. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Yong Nie or Xiao-Lei Wu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Johannes Wittmann.

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Feng, Z., Liu, X., Wang, M. et al. A novel temperate phage, vB_PstS-pAN, induced from the naphthalene-degrading bacterium Pseudomonas stutzeri AN10. Arch Virol 166, 2267–2272 (2021). https://doi.org/10.1007/s00705-021-05098-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-021-05098-8

Navigation