Skip to main content
SpringerLink
Log in

Isolation and Characterization of a Novel myovirus Infecting Shigella dysenteriae from the Aeration Tank Water

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

The genome sequence, morphology, and genetic features of a novel phage, named SSE1, is reported here. Phage SSE1 that infects Shigella dysenteriae (China General Microbiological Culture Collection Center number: 1.1869) was isolated from the aeration tank water of a sewage treatment plant. SSE1 showed morphological features associated with those of phages in Myoviridae. The whole genome sequence of phage SSE1 is composed of 169,744 bp with the GC content of 37.51%. The double-stranded DNA of SSE1 contains 270 open reading frameworks (ORFs). Phylogenetically, phage SSE1 showed a stronger homology (whole genome and terminase large subunit protein sequence) to Escherichia phages than other Shigella phages in the NCBI database, but SSE1 did not infect Escherichia stains. This indicates that phage SSE1 should be a novel phage infecting Shigella dysenteriae. Besides, the result of this study provided a new idea for phage therapy. SSE1 may become a candidate for potential therapy against Shigella dysenteriae infection in clinical applications.

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

Availability of Data and Materials

All data generated or analyzed during this study are included in this published article and its supplementary information files.

Abbreviations

S. dysenteriae :

Shigella dysenteriae

CGMCC:

China General Microbiological Culture Collection Center

ORFs:

Open reading frameworks

LEDS:

Laboratory-based Enteric Disease Surveillance

NB:

Nutrient Broth

TEM:

Transmission electron microscopy

EDTA:

Ethylene diamine tetraacetic acid

SDS:

Sodium dodecyl sulfate

E. coli :

Escherichia coli

LB:

Luria-Bertani

CDC:

Chinese Center for Disease Control and Prevention

NCBI:

National Center for Biotechnology Information

ICTV:

International Committee on Taxonomy of Viruses

References

  1. Levine, M. M., DuPont, H. L., Formal, S. B., Hornick, R. B., Takeuchi, A., Gangarosa, E. J., Snyder, M. J., & Libonati, J. P. (1973). Pathogenesis of Shigella dysenteriae 1 (Shiga) dysentery. The Journal of Infectious Diseases, 127(3), 261–270.

    Article  CAS  Google Scholar 

  2. Tóth, I., Sváb, D., Bálint, B., Brown-Jaque, M., & Maróti, G. (2016). Comparative analysis of the Shiga toxin converting bacteriophage first detected in Shigella sonnei. Infection, Genetics and Evolution, 37, 150–157.

    Article  Google Scholar 

  3. Topka, G., Bloch, S., & Boz’ena Nejman-Falen’czyk, etc. (2018). Characterization of bacteriophage vB-EcoS-95, isolated from urban sewage and revealing extremely rapid lytic development. Frontiers in Microbiology, 9, 3326.

  4. Davis, C. L., Wahid, R., Toapanta, F. R., Simon, J. K., & Sztein, M. B. (2018). A clinically parameterized mathematical model of Shigella immunity to inform vaccine design. PLoS One, 13(1), e0189571.

    Article  Google Scholar 

  5. Terry, L. M., Barker, C. R., Day, M. R., Greig, D. R., Dallman, T. J., & Jenkins, C. (2018). Antimicrobial resistance profiles of Shigella dysenteriae isolated from travellers returning to the UK, 2004-2017. Journal of Medical Microbiology, 67(8), 1022–1030.

    Article  CAS  Google Scholar 

  6. Centers for Disease Control and Prevention. National enteric disease surveillance: shigella annual report, 2016. https://www.cdc.gov/nationalsurveillance/pdfs/LEDS-Shig-2016-REPORT-508.pdf.

  7. Centers for Disease Control and Prevention. Travel-related infectious diseases: shigellosis. https://wwwnc.cdc.gov/travel/yellowbook/2020/travelrelated-infectious-diseases/shigellosis.

  8. World Health Organization. Disease Commodity Packages – Shigellosis. https://www.who.int/internal-publications-detail/shigellosis.

  9. Abedon S. T. (2017). Bacteriophage clinical use as antibacterial “drugs”: Utility and precedent. Microbiology Spectrum, 5(4), BAD-0003-2016.

  10. Centers for Disease Control and Prevention. Antibiotic/antimicrobial resistance. https://www.cdc.gov/drugresistance/.

  11. Rohde, C., Resch, G., Pirnay, J. P., Blasdel, B. G., Debarbieux, L., Gelman, D., et al. (2018). Expert opinion on three phage therapy related topics: Bacterial phage resistance, phage training and prophages in bacterial production strains. Viruses., 10(4), e178.

    Article  Google Scholar 

  12. Mertz, L. (2019). Battling superbugs: How phage therapy went from obscure to promising. IEEE Pulse, 10(1), 3–9.

    Article  Google Scholar 

  13. Dedrick, R. M., Guerrero-Bustamante, C. A., Garlena, R. A., Daniel A. Russell, et al. (2019). Engineered bacteriophages for treatment of a patient with a disseminated drug-resistant Mycobacterium abscessus. Nature Medicine, 25(5), 730–733.

    Article  CAS  Google Scholar 

  14. Schooley, R. T., Biswas, B., Gill, J. J., Hernandez-Morales, A., Lancaster, J., Lessor, L., et al. (2017). Development and use of personalized bacteriophage-based therapeutic cocktails to treat a patient with a disseminated resistant Acinetobacter baumannii infection. Antimicrobial Agents and Chemotherapy, 61(10), e00954–e00917. https://doi.org/10.1007/s12010-020-03310-0.

  15. Solovieva, E. V., Myakinina, V. P., Kislichkina, A. A., Krasilnikova, V. M., Verevkin, V. V., Mochalov, V. V., Lev, A. I., Fursova, N. K., & Volozhantsev, N. V. (2018). Comparative genome analysis of novel podoviruses lytic for hypermucoviscous Klebsiella pneumoniae of K1, K2, and K57 capsular types. Virus Research, 243, 10–18.

    Article  CAS  Google Scholar 

  16. Tomat, D., Casabonnea, C., Aquilia, V., Balaguéa, C., & Quiberoni, A. (2018). Evaluation of a novel cocktail of six lytic bacteriophages against Shiga toxinproducing Escherichia coli in broth, milk and meat. Food Microbiology, 76, 434–442.

    Article  CAS  Google Scholar 

  17. Kakasis, A., & Panitsa, G. (2019). Bacteriophage therapy as an alternative treatment for human infections. A comprehensive review. Journal of Antimicrobial Agents, 53, 16–21.

    Article  CAS  Google Scholar 

  18. Zhao, Y., Ye, M., Zhang, X., Sun, M., Zhang, Z., Chao, H., Huang, D., Wan, J., Zhang, S., Jiang, X., Sun, D., Yuan, Y., & Hu, F. (2019). Comparing polyvalent bacteriophage and bacteriophage cocktails for controlling antibiotic-resistant bacteria in soil-plant system. Science of the Total Environment, 657, 918–925.

    Article  CAS  Google Scholar 

  19. El-Dougdoug, N. K., Cucic, S., Abdelhamid, A. G., Brovko, L., Kropinski, A. M., Griffiths, M. W., & Anany, H. (2019). Control of Salmonella Newport on cherry tomato using a cocktail of lytic bacteriophages. International Journal of Food Microbiology, 293, 60–71.

    Article  CAS  Google Scholar 

  20. Soffer, N., Woolston, J., Li, M., et al. (2017). Bacteriophage preparation lytic for Shigella significantly reduces Shigella sonnei contamination in various foods. PLoS One, 12, e0175256.

    Article  Google Scholar 

  21. Sváb, D., Falgenhauer, L., Rohde, M., Chakraborty, T., & Tóth, I. (2019). Complete genome sequence of C130_2, a novel myovirus infecting pathogenic escherichia coli and shigella strains. Archives of Virology, 164(1), 321–324.

    Article  Google Scholar 

  22. Domingo-Calap, P., & Delgado-Martínez, J. (2018). Bacteriophages: Protagonists of a post-antibiotic era. Antibiotics., 7, 66.

    Article  CAS  Google Scholar 

  23. Doore, S. M., Schrad, J., Dean, W. F., Dover, J. A., & Parent, K. N. (2018). Shigella phages isolated during a dysentery outbreak reveal uncommon structures and broad species diversity. Journal of Virology, 92, JVI.02117–JVI.02117.

    Article  Google Scholar 

  24. Jurczak-Kurek, A., Gasior, T., Nejman-Falenczyk, B., Bloch, S., Dydecka, A., Topka, G., et al. (2016). Biodiversity of bacteriophages: morphological and biological properties of a large group of phages isolated from urban sewage. Scientific Reports, 6, 34338.

    Article  CAS  Google Scholar 

  25. Joseph, S., & David, W. R. (2001). Molecular cloning: a laboratory manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  26. Fan, N., Qi, R., & Yang, M. (2017). Isolation and characterization of a virulent bacteriophage infecting Acinetobacter johnsonii from activated sludge. Research in Microbiology, 5, 472–481.

    Article  Google Scholar 

  27. Turner, D., Reynolds, D., Seto, D., & Mahadevan, P. (2013). Coregenes3.5: a webserver for the determination of core genes from sets of viral and small bacterial genomes. BMC Research Notes, 6(1), 140.

    Article  Google Scholar 

  28. Pettengill, J. B., Luo, Y., Davis, S., Chen, Y., & Strain, E. (2014). An evaluation of alternative methods for constructing phylogenies from whole genome sequence data: A case study with salmonella. PeerJ., 2(6), e620.

    Article  Google Scholar 

  29. Yoda, T., Tanabe, M., Tsuji, T., et al. (2017). Exonuclease processivity of archaeal replicative DNA polymerase in association with PCNA is expedited by mismatches in DNA. Scientific Reports-UK, 7, 44582.

    Article  Google Scholar 

  30. Konomura, N., Arai, N., Shinohara, T., et al. (2017). Rad51 and RecA juxtapose dsDNA ends ready for DNA ligase-catalyzed end-joining under recombinase-suppressive conditions. Nucleic Acids Research, 45(1), 337–352.

    Article  CAS  Google Scholar 

  31. Shlomai, J., & Linial, M. (1986). A nicking enzyme from trypanosomatids which specifically affects the topological linking of duplex DNA circles. Purification and characterization. The Journal of Biological Chemistry, 261(34), 16219–16225.

    CAS  PubMed  Google Scholar 

  32. Jin, J., Li, Z. J., Wang, S. W., et al. (2014). Genome organisation of the Acinetobacter lytic phage ZZ1 and comparison with other T4-like Acinetobacter phages. BMC Genomics, 15(1), 793.

    Article  Google Scholar 

  33. Young, R., & Blasi, U. (1995). Holins: Form and function in bacteriophage lysis. FEMS Microbiology Reviews, 17(1-2), 191–205.

    Article  CAS  Google Scholar 

  34. Rui, H., Li, M., Tang, T., et al. (2018). Construction of Lactobacillus casei ghosts by Holin-mediated inactivation and the potential as a safe and effective vehicle for the delivery of DNA vaccines. BMC Microbiology, 18(1), 80.

    Article  Google Scholar 

  35. Roach, D. R., & Donovan, D. M. (2015). Antimicrobial bacteriophage derived proteins and therapeutic applications. Bacteriophage., 5(3), e1062590.

    Article  CAS  Google Scholar 

  36. Nikhat, Z., Raja, M., & Donald, S. (2002). CoreGenes: A computational tool for identifying and cataloging "core" genes in a set of small genomes. BMC Bioinformatics, 3(1), 12–12.

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the Institute of Microbiology, Chinese Academy of Sciences for electron microscopy.

Funding

This study was funded by grant from the National Natural Science Foundation of China (No. 50978250 and No. 51378485).

Author information

Authors and Affiliations

  1. College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, 101408, China

    Han Lu, Honghui Liu, Min Lu, Jingwei Wang, Xinchun Liu & Ruyin Liu

Authors
  1. Han Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Honghui Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Min Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jingwei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xinchun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ruyin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

H. Lu and H. Liu performed the experiments, analyzed the data, and wrote the paper. ML helped design the experiment and put forward suggestions for the smooth progress of the experiment. JW reviewed the first draft of the paper. XL and RL revised the manuscript. All authors had read and approved the manuscript.

Corresponding authors

Correspondence to Xinchun Liu or Ruyin Liu.

Ethics declarations

Ethics Approval and Consent to Participate

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

Consent for Publication

Not applicable.

Conflict of Interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

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

Electronic supplementary material

ESM 1

(DOCX 82 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lu, H., Liu, H., Lu, M. et al. Isolation and Characterization of a Novel myovirus Infecting Shigella dysenteriae from the Aeration Tank Water. Appl Biochem Biotechnol 192, 120–131 (2020). https://doi.org/10.1007/s12010-020-03310-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-020-03310-0

Keywords

Search

Navigation