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Isolation and characterization of a novel Escherichia coli phage Kayfunavirus ZH4

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Abstract

Escherichia coli, a gram-negative bacterium, was generally considered conditional pathogenic bacteria and the proportion of bacteria resistant to commonly used specified antibacterial drugs exceeded 50%. Phage therapeutic application has been revitalized since antibiotic resistance in bacteria was increasing. Compared with antibiotics, phage is the virus specific to bacterial hosts. However, further understanding of phage–host interactions is required. In this study, a novel phage specific to a E. coli strain, named as phage Kayfunavirus ZH4, was isolated and characterized. Transmission electron microscopy showed that phage ZH4 belongs to the family Autographiviridae. The whole-genome analysis showed that the length of phage ZH4 genome was 39,496 bp with 49 coding domain sequence (CDS) and no tRNA was detected. Comparative genome and phylogenetic analysis demonstrated that phage ZH4 was highly similar to phages belonging to the genus Kayfunavirus. Moreover, the highest average nucleotide identity (ANI) values of phage ZH4 with all the known phages was 0.86, suggesting that ZH4 was a relatively novel phage. Temperature and pH stability tests showed that phage ZH4 was stable from 4° to 50 °C and pH range from 3 to 11. Host range of phage ZH4 showed that there were only 2 out of 17 strains lysed by phage ZH4. Taken together, phage ZH4 was considered as a novel phage with the potential for applications in the food and pharmaceutical industries.

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References

  1. Easwaran M, De Zoysa M, Shin HJ (2020) Application of phage therapy: synergistic effect of phage EcSw (PhiEcSw) and antibiotic combination towards antibiotic-resistant Escherichia coli. Transbound Emerg Dis 67:2809–2817

    Article  CAS  Google Scholar 

  2. Farfan MJ, Torres AG (2012) Molecular mechanisms that mediate colonization of Shiga toxin-producing Escherichia coli strains. Infect Immun 80:903–913

    Article  CAS  Google Scholar 

  3. Yun KW, Park SH, Cho EY, Lee H (2019) Clinical features and outcomes of community-acquired late-onset sepsis: focusing on group B Streptococcus and Escherichia coli. Pediatr Int 61:1210–1215

    Article  CAS  Google Scholar 

  4. Kasimanickam V, Kasimanickam M, Kasimanickam R (2021) Antibiotics use in food animal production: escalation of antimicrobial resistance: where are we now in combating AMR. Med Sci (Basel, Switzerland) 9:14

    CAS  Google Scholar 

  5. Vansia A, Patel R, Dudhagara P (2021) Analysis of multidrug resistance profile of Escherichia coli from clinical samples from companion animals and bird retrospect to five-year (2015–2019) literature data. Biointerface Res Appl Chem 11:12506–12515

    Article  CAS  Google Scholar 

  6. Sayah RS, Kaneene JB, Johnson Y, Miller R (2005) Patterns of antimicrobial resistance observed in Escherichia coli isolates obtained from domestic- and wild-animal fecal samples, human septage, and surface water. Appl Environ Microbiol 71:1394–1404

    Article  CAS  Google Scholar 

  7. Jamal M, Andleeb S, Jalil F, Imran M, Nawaz MA, Hussain T, Ali M, Rahman SU, Das CR (2019) Isolation, characterization and efficacy of phage MJ2 against biofilm forming multi-drug resistant Enterobacter cloacae. Folia Microbiol 64:101–111

    Article  CAS  Google Scholar 

  8. Jamal M, Bukhari S, Andleeb S, Ali M, Raza S, Nawaz MA, Hussain T, Rahman SU, Shah SSA (2019) Bacteriophages: an overview of the control strategies against multiple bacterial infections in different fields. J Basic Microbiol 59:960

    Article  Google Scholar 

  9. Briers Y, Lavigne R (2015) Breaking barriers: expansion of the use of endolysins as novel antibacterials against Gram-negative bacteria. Future Microbiol 10:377–390

    Article  CAS  Google Scholar 

  10. Capparelli R, Ventimiglia I, Roperto S, Fenizia D, Iannelli D (2006) Selection of an Escherichia coli O157:H7 bacteriophage for persistence in the circulatory system of mice infected experimentally. Clin Microbiol Infect 12:248–253

    Article  CAS  Google Scholar 

  11. O’Flynn G, Ross RP, Fitzgerald GF, Coffey A (2004) Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7. Appl Environ Microbiol 70:3417–3424

    Article  CAS  Google Scholar 

  12. Han JE, Kim JH, Hwang SY, Choresca CH, Shin SP, Jun JW, Chai JY, Park YH, Park SC (2013) Isolation and characterization of a Myoviridae bacteriophage against Staphylococcus aureus isolated from dairy cows with mastitis. Res Vet Sci 95:758–763

    Article  CAS  Google Scholar 

  13. Chang HC, Chen CR, Lin J-W, Shen GH, Chang KM, Tseng YH, Weng SF (2005) Isolation and characterization of novel giant Stenotrophomonas maltophilia phage phiSMA5. Appl Environ Microbiol 71:1387–1393

    Article  CAS  Google Scholar 

  14. Yoon H, Yun J, Lim JA, Roh E, Jung KS, Chang Y, Ryu S, Heu S (2013) Characterization and genomic analysis of two Staphylococcus aureus bacteriophages isolated from poultry/livestock farms. J Gen Virol 94:2569–2576

    Article  CAS  Google Scholar 

  15. Zhang L, Bao H, Wei C, Zhang H, Zhou Y, Wang R (2015) Characterization and partial genomic analysis of a lytic Myoviridae bacteriophage against Staphylococcus aureus isolated from dairy cows with mastitis in Mid-east of China. Virus Genes 50:111–117

    Article  CAS  Google Scholar 

  16. Zhang Q, Xing S, Sun Q, Pei G, Cheng S, Liu Y, An X, Zhang X, Qu Y, Tong Y (2017) Characterization and complete genome sequence analysis of a novel virulent Siphoviridae phage against Staphylococcus aureus isolated from bovine mastitis in Xinjiang, China. Virus Genes 53:464–476

    Article  CAS  Google Scholar 

  17. Shende RK, Hirpurkar SD, Sannat C, Rawat N, Pandey V (2017) Isolation and characterization of bacteriophages with lytic activity against common bacterial pathogens. Vet World 10:973–978

    Article  CAS  Google Scholar 

  18. Zhang C, Yuan J, Guo C, Ge C, Wang X, Wei D, Li X, Si H, Hu CJVR (2021) Identification and complete genome of lytic “Kp34likevirus” phage vB_KpnP_Bp5 and therapeutic potency in the treatment of lethal Klebsiella pneumoniae infections in mice. Virus Res 297:198348

    Article  CAS  Google Scholar 

  19. Sullivan MJ, Petty NK, Beatson SA (2011) Easyfig: a genome comparison visualizer. Bioinformatics 27:1009–1010

    Article  CAS  Google Scholar 

  20. Kleinheinz KA, Joensen KG, Larsen MV (2014) Applying the ResFinder and VirulenceFinder web-services for easy identification of acquired antibiotic resistance resistance and E. coli virulence genes in bacteriophage and prophage nucleotide sequences. Bacteriophage 4:e27943

    Article  Google Scholar 

  21. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  Google Scholar 

  22. Yuan X, Zhang S, Wang J, Li C, Li N, Yu S, Kong L, Zeng H, Yang G, Huang Y, Li H, Zhang J, Wu Q, Ding Y (2021) Isolation and characterization of a novel Escherichia coli Kayfunavirus phage DY1. Virus Res 293:198274

    Article  CAS  Google Scholar 

  23. Liu JL, Zabetakis D, Breger JC, Anderson GP, Goldman ER (2020) Multi-enzyme assembly on T4 phage scaffold. Front Bioeng Biotechnol 8:571

    Article  Google Scholar 

  24. Manohar P, Tamhankar AJ, Lundborg CS, Nachimuthu R (2019) Therapeutic characterization and efficacy of bacteriophage cocktails infecting Escherichia coli, Klebsiella pneumoniae, and Enterobacter species. Front Microbiol. https://doi.org/10.3389/fmicb.2019.00574

    Article  PubMed  PubMed Central  Google Scholar 

  25. Casjens SR, Thuman-Commike PA (2011) Evolution of mosaically related tailed bacteriophage genomes seen through the lens of phage P22 virion assembly. Virology 411:393–415

    Article  CAS  Google Scholar 

  26. Sharma M, Kumar D, Poluri KM (2016) Elucidating the pH-dependent structural transition of T7 bacteriophage endolysin. Biochemistry 55:4614–4625

    Article  CAS  Google Scholar 

  27. Nelson DC, Schmelcher M, Rodriguez-Rubio L, Klumpp J, Pritchard DG, Dong S, Donovan DM (2012) Endolysins as antimicrobials. Adv Virus Res 83:299–365

    Article  CAS  Google Scholar 

  28. Young R (1992) Bacteriophage lysis: mechanism and regulation. Microbiol Rev 56:430–481

    Article  CAS  Google Scholar 

  29. Wang IN, Smith DL, Young R (2000) Holins: the protein clocks of bacteriophage infections. Annu Rev Microbiol 54:799–825

    Article  CAS  Google Scholar 

  30. Dewey JS, Savva CG, White RL, Vitha S, Holzenburg A, Young R (2010) Micron-scale holes terminate the phage infection cycle. Proc Natl Acad Sci USA 107:2219–2223

    Article  CAS  Google Scholar 

  31. Park T, Struck DK, Dankenbring CA, Young R (2007) The pinholin of lambdoid phage 21: control of lysis by membrane depolarization. J Bacteriol 189:9135–9139

    Article  CAS  Google Scholar 

  32. Breitbart M, Miyake JH, Rohwer F (2004) Global distribution of nearly identical phage-encoded DNA sequences. FEMS Microbiol Lett 236:249–256

    Article  CAS  Google Scholar 

  33. Monteiro R, Pires DP, Costa AR, Azeredo J (2019) Phage therapy: going temperate. Trends Microbiol 27:368–378

    Article  CAS  Google Scholar 

  34. Van den Bossche A, Ceyssens P-J, De Smet J, Hendrix H, Bellon H, Leimer N, Wagemans J, Delattre A-S, Cenens W, Aertsen A, Landuyt B, Minakhin L, Severinov K, Noben J-P, Lavigne R (2014) Systematic identification of hypothetical bacteriophage proteins targeting key protein complexes of Pseudomonas aeruginosa. J Proteome Res 13:4446–4456

    Article  Google Scholar 

  35. Spruit CM, Wicklund A, Wan X, Skurnik M, Pajunen MI (2020) Discovery of three toxic proteins of Klebsiella Phage fHe-Kpn01. Viruses 12:544

    Article  CAS  Google Scholar 

  36. Delesalle VA, Tanke NT, Vill AC, Krukonis GPJB (2016) Testing hypotheses for the presence of tRNA genes in mycobacteriophage genomes. Bacteriophage 6:e1219441

    Article  CAS  Google Scholar 

  37. Yoshikawa G, Askora A, Blanc-Mathieu R, Kawasaki T, Li Y, Nakano M, Ogata H, Yamada T (2018) Xanthomonas citri jumbo phage XacN1 exhibits a wide host range and high complement of tRNA genes. Sci Rep 8:4486

    Article  Google Scholar 

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Funding

This study was funded by National Natural Science Foundation of China (Grant Nos. 31502079 and 31660700); National Natural Science Foundation of Guangxi (Grant No. 2017GXNSFAA198071); Science and Technology Development Program of Nanning (Grant No. 20180526); Science and Technology Plan Project of Chongzuo (Grant No. FA2019006); the Science and Technology Development Program of Wuming District in Nanning (Grant No. 20190101).

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LL: Methodology, investigation, validation, formal analysis, writing—original draft. DM: formal analysis, software, data curation, writing—original draft, visualization. YZ: writing—review & editing, funding acquisition. LW: formal analysis, writing—review & editing. XW: conceptualization, supervision, project administration, funding acquisition, writing—review & editing.

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Correspondence to Xiaoye Wang.

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Li, L., Wu, Y., Ma, D. et al. Isolation and characterization of a novel Escherichia coli phage Kayfunavirus ZH4. Virus Genes 58, 448–457 (2022). https://doi.org/10.1007/s11262-022-01916-6

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  • DOI: https://doi.org/10.1007/s11262-022-01916-6

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