Temperate enterococcal bacteriophages: genetic features and practical application

Clinical Microbiology and Antimicrobial Chemotherapy. 2022; 24(3):213-218

​ Tkachev P.V., Goncharov A.E., Dmitriev A.V.
10.36488/cmac.2022.3.213-218
Enterococcus spp temperate bacteriophages antimicrobial resistance phage therapy biotechnology
Section
Diseases and Pathogens
Type
Review
Publication
Clinical Microbiology and Antimicrobial Chemotherapy. 2022; 24(3):213-218

Abstract

Temperate bacteriophages are of interest as carriers and vectors of pathogenicity factors that determine an epidemic potential of opportunistic bacteria as well as biotechnology objects. This review describes studies of temperate bacteriophages infecting bacteria of the genus Enterococcus, including strains associated with the development of nosocomial infections. Genetic features of moderate enterococcal phages as well as their potential for practical application in medicine are considered.

Pavel V. Tkachev

Institute of Experimental Medicine, Saint-Petersburg, Russia

Goncharov A.E.

Institute of Experimental Medicine, Saint-Petersburg, Russia

Dmitriev A.V.

Institute of Experimental Medicine, Saint-Petersburg, Russia

  • 1. Salmond G.P., Fineran P.C. A century of the phage: past, present and future. Nat Rev Microbiol. 2015;13(12):777786. DOI: 10.1038/nrmicro3564
  • 2. Letarov A.V. Sovremennye konczepczii biologii bakteriofagov. M.: DeLi, 2020. 383 p. Russian.
  • 3. Gordillo Altamirano F.L., Barr J.J. Phage therapy in the postantibiotic era. Clin Microbiol Rev. 2019;32(2):e0006618. DOI: 10.1128/CMR.00066-18
  • 4. Monteiro R., Pires D.P., Costa A.R., Azeredo J. Phage therapy: going temperate? Trends Microbiol. 2019;27(4):368-378. DOI: 10.1016/j.tim.2018.10.008
  • 5. Dublanchet A., Fruciano E. A short history of phage therapy. Med Mal Infect. 2008;38(8):415-420. DOI: 10.1016/j.medmal.2008.06.016
  • 6. Ebrahimizadeh W., Rajabibazl M. Bacteriophage vehicles for phage display: biology, mechanism, and application. Curr Microbiol. 2014;69(2):109-120. DOI: 10.1007/s00284-014-0557-0
  • 7. Ju Z., Sun W. Drug delivery vectors based on filamentous bacteriophages and phage-mimetic nanoparticles. Drug Deliv. 2017;24(1):1898-1908. DOI: 10.1080/10717544.2017.1410259
  • 8. Messing J. Cloning in M13 phage or how to use biology at its best. Gene. 1991;100:3-12. DOI: 10.1016/03781119(91)90344-b
  • 9. Chauthaiwale V.M., Therwath A., Deshpande V.V. Bacteriophage lambda as a cloning vector. Microbiol Rev. 1992;56(4):577-591. DOI: 10.1128/mr.56.4.577591.1992
  • 10. Moreno M.R.F., Sarantinopoulos P., Tsakalidou E., De Vuyst L. The role and application of enterococci in food and health. Int J Food Microbiol. 2006;106(1):1-24. DOI: 10.1016/j.ijfoodmicro.2005.06.026
  • 11. Huycke M.M., Sahm D.F., Gilmore M.S. Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerg Infect Dis. 1998;4(2):239. DOI: 10.3201/eid0402.980211
  • 12. Fiore E., Van Tyne D., Gilmore M.S. Pathogenicity of enterococci. Microbiol Spectr. 2019;7(4). DOI: 10.3412/jsb.72.189
  • 13. Ekwanzala M.D., Dewar J.B., Kamika I., Momba M.N.B. Comparative genomics of vancomycin-resistant Enterococcus spp. revealed common resistome determinants from hospital wastewater to aquatic environments. Sci Total Environ. 2020;719:137275. DOI: 10.1016/j.scitotenv.2020.137275
  • 14. Allen H.K., Trachsel J., Looft T., Casey T.A. Finding alternatives to antibiotics. Ann N Y Acad Sci. 2014;1323(1):91-100. DOI: 10.1111/nyas.12468
  • 15. Sherman J.M. The streptococci. Bacteriol Rev. 1937;1(1):397. DOI: 10.1128/br.1.1.3-97.1937
  • 16. Rogers C.G., Sarles W.B. Characterization of Enterococcus bacteriophages from the small intestine of the rat. J Bacteriol. 1963;85(6):1378-1385. DOI: 10.1128/jb.85.6.13781385.1963
  • 17. Kim Y.W., Chang H.I. Isolation and molecular characterization of φFC1, a new temperate phage from Enterococcus faecalis. Mol Cells. 1994;4(2):155-158.
  • 18. Kim M.-J., Lee J.-Y., Kim Y.-W., Sung H.-C., Chang ­H.-I. Molecular characterization of the region encoding integrative functions from enterococcal bacteriophage φFC1. J Biochem Mol Biol. 1996;29(5):448-454.
  • 19. Yang H.Y., Kim Y.W., Chang H.I. Construction of an integration-proficient vector based on the site-specific recombination mechanism of enterococcal temperate phage φFC1. J Bacteriol. 2002;184(7):1859-1864. DOI: 10.1128/JB.184.7.1859-1864.2002
  • 20. Strizhov N., Tikhomirova L. Construction of recombinant plasmid carrying the λ DNA fragment responsible for prophage integration. Nucleic Acids Res. 1978;5(6):17671777. DOI: 10.1093/nar/5.6.1767
  • 21. Kim H.Y., Yoon B.H., Chang H.I. Site-specific recombination by the integrase MJ1 on mammalian cell. Hanguk Misaengmul Saengmyong Konghakhoe Chi. 2011;39(4):337-344.
  • 22. Paulsen I.T., Banerjei L., Myers G.S.A., Nelson K.E., Seshadri R., Read T.D., et al. Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science. 2003;299(5615):2071-2074. DOI: 10.1126/science.1080613
  • 23. Duerkop B.A., Clements C., Rollins D., Rodrigues J., Hooper L. A composite bacteriophage alters colonization by an intestinal commensal bacterium. Proc Natl Acad Sci. 2012;109(43):17621-17626. DOI: 10.1073/pnas.1206136109
  • 24. Matos R.C., Lapaque N., Riggottier-Gois L., Debarbieux L., Meylheuc T., Gonzalez-Zorn B., et al. Enterococcus faecalis prophage dynamics and contributions to pathogenic traits. PLoS Genet. 2013;99(6):e1003539. DOI: 10.1371/journal.pgen.1003539
  • 25. Lossouarn J., Briet A., Moncaut E., Furlan S., Bouteau A., Son O., et al. Enterococcus faecalis countermeasures defeat a virulent Picovirinae bacteriophage. Viruses. 2019;11(1):48. DOI: 10.3390/v11010048
  • 26. Yasmin A., Kenny J., Shankar J., Darby C.A., Hall N., Edwards C., Horsburgh J.M. Comparative genomics and transduction potential of Enterococcus faecalis temperate bacteriophages. J Bacteriol. 2010;192(4):1122-1130. DOI: 10.1128/JB.01293-09
  • 27. Mitchell J., Sullam P.M. Streptococcus mitis phage-encoded adhesins mediate attachment to α2-8-linked sialic acid residues on platelet membrane gangliosides. Infect Immun. 2009;77(8):3485-3490. DOI: 10.1128/IAI.01573-08
  • 28. Bensing B.A., Siboo I.R., Sullam P.M. Proteins PblA and PblB of Streptococcus mitis, which promote binding to human platelets, are encoded within a lysogenic bacteriophage. Infect Immun. 2001;69(10):6186-6192. DOI: 10.1128/IAI.69.10.6186-6192.2001
  • 29. Zhao Z., Sagulenko E., Ding Z., Christie P. Activities of VirE1 and the VirE1 secretion chaperone in export of the multifunctional VirE2 effector via an Agrobacterium type IV secretion pathway. J Bacteriol. 2001;183(13):3855-3865. DOI: 10.1128/JB.183.13.3855-3865.2001
  • 30. Viboud G.I., Bliska J.B. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu Rev Microbiol. 2005;59:69-89. DOI: 10.1146/annurev.micro.59.030804.121320
  • 31. Aslanov B.I., Dolgiy A.A., Goncharov A.E., Archangelskiy A.I. Epidemiological features of the forming of pathogenic properties of Enterococcus faecalis and Enterococcus faecium in urological hospital. Profilakticheskaja i klinicheskaja medicina. 2012;2(43):5257. Russian.
  • 32. Arndt D., Grant R.J., Marcu A., Sajed T., Pon A., Liang R.J., Marcu A., et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res. 2016;44(W1):W16-W21. DOI: 10.1093/nar/gkw387
  • 33. Stevens R.H., Porras O.D., Delisle A.L. Bacteriophages induced from lysogenic root canal isolates of Enterococcus faecalis. Oral Microbiol Immunol. 2009;24(4):278-284. DOI: 10.1111/j.1399-302X.2009.00506.x
  • 34. Stevens R.H., Ektefaie M.R., Fouts D.E. The annotated complete DNA sequence of Enterococcus faecalis bacteriophage φEf11 and its comparison with all available phage and predicted prophage genomes. FEMS Microbiol Lett. 2011;317(1):9-26. DOI: 10.1111/j.15746968.2010.02203.x
  • 35. Zhang H., Fouts D.E., DePew J., Stevens R.H. Genetic modifications to temperate Enterococcus faecalis phage ϕEf11 that abolish the establishment of lysogeny and sensitivity to repressor, and increase host range and productivity of lytic infection. Microbiology (Reading). 2013;159(Pt 6):1023. DOI: 10.1099/mic.0.067116-0
  • 36. Tinoco J.M., Buttaro B., Zhang H., Liss N., Sassone L., Stevens R. Effect of a genetically engineered bacteriophage on Enterococcus faecalis biofilms. Arch Oral Biol. 2016;71; 80-86. DOI: 10.1016/j.archoralbio.2016.07.001
  • 37. Tinoco J.M. Buttaro B., Zhang H., Liss N., Nissan R., Gordon W., et al. Antibacterial effect of geneticallyengineered bacteriophage ϕEf11/ϕFL1C (Δ36) PnisA on dentin infected with antibiotic-resistant Enterococcus faecalis. Arch Oral Biol. 2017;82:166-170. DOI: 10.1016/j.archoralbio.2017.06.005
  • 38. Stevens R.H., Zhang H., Hsiao C., Kachlany S., Tinnoco E., DePew J., Fouts D. Structural proteins of Enterococcus faecalis bacteriophage φEf11. Bacteriophage. 2016;6(4):e1251381. DOI: 10.1080/21597081.2016.1251381
  • 39. Zhang H., Buttaro B., Fouts D., Sanjari S., Evans B., Stevens R. Bacteriophage φEf11 ORF28 endolysin, a multifunctional lytic enzyme with properties distinct from all other identified Enterococcus faecalis phage endolysins. Appl Environ Microbiol. 2019;85(13):e00555-19. DOI: 10.1128/AEM.00555-19
  • 40. Yoon B.H., Chang H.I. Genomic annotation for the temperate phage EFC-1, isolated from Enterococcus faecalis KBL101. Arch Virol. 2015;160(2):601-604. DOI: 10.1007/s00705-014-2263-4
  • 41. Askora A., El-Telbany M., El-Didamony G., Ariny E., Askoura M. Characterization of φEf-vB1 prophage infecting oral Enterococcus faecalis and enhancing bacterial biofilm formation. J Med Microbiol. 2020;69(9):1151-1168. DOI: 10.1099/jmm.0.001246
  • 42. Santajit S., Indrawattana N. Mechanisms of antimicrobial resistance in ESKAPE pathogens. Biomed Res Int. 2016;2016:2475067. DOI: 10.1155/2016/2475067
  • 43. Adesida S.A. Ezenta C., Abagbada A., Aladesokan A., Coker A. Carriage of multidrug resistant Enterococcus faecium and Enterococcus faecalis among apparently healthy humans. Afr J Infect Dis. 2017;11(2):83-89. DOI: 10.21010/ajid.v11i2.11
  • 44. Mulani M.S. Kamble E., Kumbar S., Tawre M., Pardesi K. Emerging strategies to combat ESKAPE pathogens in the era of antimicrobial resistance: a review. Front Microbiol. 2019;10:539. DOI: 10.3389/fmicb.2019.00539
  • 45. Lee Y.D., Park J.H. Isolation and characterization of temperate phages in Enterococcus faecium from sprouts. Food Sci Biotechnol. 2014;46(3):323-327. DOI: 10.9721/KJFST.2014.46.3.323
  • 46. Nigutova K., Styriak I., Javorsky P., Pristas P. Partial characterization of Enterococcus faecalis bacteriophage F4. Folia Microbiol. 2008;53(3):234-236. DOI: 10.1007/s12223-008-0033-y
  • 47. Lavigne R., Darius P., Summer E.J., Seto D., Mahadevan P., Nilsson A.S., et al. Classification of Myoviridae bacteriophages using protein sequence similarity. BMC Microbiol. 2009;9(1):1-16. DOI: 10.1186/1471-2180-9-224
  • 48. Ely B., Berrios L., Thomas Q. A temperate bacteriophage that infects Caulobacter Crescentus strain CB15. Curr Microbiol. 2022;79(4):1-5. DOI: 10.1007/s00284-02202799-4
  • 49. Gillis A., Mahillon J. Tectiviruses preying on the Bacillus cereus group. Proceedings of the 21st Evergreen International Phage Biology Meeting. 2015.
  • 50. Gillis A., Mahillon J. Phages preying on Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis: past, present and future. Viruses. 2014;6(7):2623-2672. DOI: 10.3390/v6072623
  • 51. Frost L.S. Conjugative pili and pilus-specific phages. Bacterial conjugation. Springer, Boston, MA, 1993:189221. DOI: 10.1007/978-1-4757-9357-4_7
  • 52. Hobbs Z., Abedon S.T. Diversity of phage infection types and associated terminology: the problem with ‘Lytic or lysogenic’. FEMS Microbiol Lett. 2016;363(7). DOI: 10.1093/femsle/fnw047
  • 53. Kim A.Y., Blaschek H.P. Isolation and characterization of a filamentous viruslike particle from Clostridium acetobutylicum NCIB 6444. J Bacteriol. 1991;173(2):530535. DOI: 10.1128/jb.173.2.530-535.1991
  • 54. Katzif S., Danavall D., Bowers S., Balthazar J.T., Shafer W.M. The major cold shock gene, cspA, is involved in the susceptibility of Staphylococcus aureus to an antimicrobial peptide of human cathepsin G. Infect Immun. 2003;71(8):4304-4312. DOI: 10.1128/IAI.71.8.43044312.2003
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