TSitologiya i Genetika 2021, vol. 55, no. 3, 58-75
Cytology and Genetics 2021, vol. 55, no. 3, 256–269, doi: https://www.doi.org/10.3103/S0095452721030099

Mobile genetic elements (MGE) of bacteria and their hierarchy

Skliar T., Kurahina N., Lavrentieva K., Burlaka V., Lykholat T., Lykholat O.

  1. Oles Honchar Dnipro National University, 72, Gagarina prosp., Dnipro 49010
  2. University of Customs and Finance, 2/4, Volodymyra Vernadskoho Str., Dnipro, Ukraine

SUMMARY. This review highlights mobile genetic elements (MGE) of bacteria, widespread in different genomes. MGE encode the functions that are insignificant for bacteria yet give them some advantages (adjusting to new environmental conditions, «invading» and colonizing a new host, etc.) and play a relevant role in ensuring the mobility of genomes. The article summarizes and analyzes current data on mobile genetic elements of bacteria and the specificities of their interaction, reviews the mechanisms of mobility of genetic elements and incompatibility of bacteriophages, plasmids, and restriction-modification systems. It also underscores the classification and the mechanisms of functioning for restriction-modification systems in bacterial cells. The attention is focused on the incompatibility of mobile genetic elements, as it reflects their individual and egoistic nature and is even used as a basis to classify some of them. Mobile genetic elements are viewed both as promising biotechnological objects for cloning and gene expression, and a «tool» in studying many fundamental issues.

Keywords: mobile genetic elements, pathogenicity islands, bacteriophages, plasmids, RM-systems, incompatibility

TSitologiya i Genetika
2021, vol. 55, no. 3, 58-75

Current Issue
Cytology and Genetics
2021, vol. 55, no. 3, 256–269,
doi: 10.3103/S0095452721030099

Full text and supplemented materials

References

1. Ainsworth, S., Mahony, J., and Douwe van Sinderen, The plasmid complement of Lactococcus lactis UC509.9 encodes multiple bacteriophage resistance systems, Appl. Environ. Microbiol., 2014. https://doi.org/10.1128/AEM.01070-14

2. Abril, A.G., Carrera, M., Böhme, K., Barros-Velázquez, J., Cacas, B., Rama, J.L.R., Villa, T.G., and Calo-Mata, P., Characterization of bacteriophage peptides of pathogenic Streptococcus by LC-ESI-MS/MS: bacteriophage phylogenomics and their relationship to their host, Front. Microbiol., 2020. https://doi.org/10.3389/fmicb.2020.01241

3. Arai, N., Sekizuka, T., Tamamura, Y., Kusumoto, M., Hinenoya, A., Yamasaki, S., Iwata, T., Watanabe-Yanai, A., Kuroda, M., and Akiba, M., Salmonella genomic island 3 is an integrative and conjugative element and contributes to copper and arsenic tolerance of Salmonella enterica, Antimicrob. Agents Chemother., 2019. https://doi.org/10.1128/AAC.00429-19

4. Argov, T., Sapir, S.R., Pasechnek, A., Azulay, G., Stadnyuk, O., Rabinovich, L., Sigal, N., Borovok, I., and Herskovits, A.A., Coordination of cohabiting phage elements supports bacteria–phage cooperation, Nat. Commun., 2019, vol. 21, no. 10 (1), art. 5288.

5. Aussel, L., Beuzyn, C.R., and Cascales, E., Meeting report: adaptation and communication of bacterial pathogens, Virulence, 2016. https://doi.org/10.1080/21505594.2016.1152441

6. Blow, M.J., Clark, T.A., Daum, C.G., Deutschbauer, A.M., Fomenkov, A., Fries, R., et al., The epigenomic landscape of prokaryotes, PLoS Genet., 2016. https://doi.org/10.1371/journal.pgen.1005854

7. Boltner, D., MacMahon, C., Pembroke, J.T., Strike, P., and Osborn, A.M., R391: a conjugative integrating mosaic comprised of phage, plasmid, and transposon elements, J. Bacteriol., 2002, vol. 184, no. 18, pp. 5158–5169.

8. Bower, E.K.M., Cooper, L.P., Roberts, G.A., White, J.H., Luyten, Y., Morgan, R.D., and Dryden, D.T.F., A model for the evolution of prokaryotic DNA restriction-modification systems based upon the structural malleability of type I restriction-modification enzymes, Nucleic Acids Res., 2018. https://doi.org/10.1093/nar/gky760

9. Broecker, F. and Moelling, K., Evolution of immune systems from viruses and transposable elements, Front. Microbiol., 2019, https://doi.org/10.3389/fmicb.2019.00051

10. Cai, R., Wu, M., Zhang, H., Zhang, Y., Cheng, M., Guo, Z., Ji, Y., Xi, H., Wang, X., Xue, Y., Sun, C., Feng, X., Lei, L., Tong, Y., Liu, X., Han, W., and Gu, J., A smooth-type, phage-resistant Klebsiella pneumoniae mutant strain reveals that OmpC is indispensable for infection by phage GH-K3, Appl. Environ. Microbiol., 2018. https://doi.org/10.1128/AEM.01585-18

11. Carraro, N., Rivard, N., Burrus, V., and Ceccarelli, D., Mobilizable genomic islands, different strategies for the dissemination of multidrug resistance and other adaptive traits, Mob. Genet. Elements, 2017. https://doi.org/10.1080/2159256X.2017.1304193

12. Casjens, S.R. and Grose, J.H., Contributions of P2- and P22-like prophages to understanding the enormous diversity and abundance of tailed bacteriophages, Virology, 2016. https://doi.org/10.1016/j.virol.2016.05.022

13. Castillo, D., Kauffman, K., Hussain, F., Kalatzis, P., Rorbo, N., Polz, M.F., and Middelboe, M., Widespread distribution of prophage-encoded virulence factors in marine Vibrio communities, Sci. Rep., 2018. https://doi.org/10.1038/s41598-018-28326-9

14. Cervera-Alamar, M., Guzmán-Markevitch, K., Žiemyte, M., Ortí, L., Bernabé-Quispe, P., Pineda-Lucena, A., Pemán, J., and Tormo-Mas, M., Mobilisation mechanism of pathogenicity islands by endogenous phages in Staphylococcus aureus clinical strains, Sci. Rep., 2018. https://doi.org/10.1038/s41598-018-34918-2

15. Chaudhary, K., BacteRiophage EXclusion (BREX): a novel anti-phage mechanism in the arsenal of bacterial defense system, J. Cell Physiol., 2018. https://doi.org/10.1002/jcp.25973

16. Chen, B., Akusobi, C., Fang, X., and Salmond, G., Environmental T4-family bacteriophages evolve to escape abortive infection via multiple routes in a bacterial host employing “Altruistic Suicide” through type III toxin–antitoxin systems, Front. Microbiol., 2017. https://doi.org/10.3389/fmicb.2017.01006

17. Chervatiuk, N.V. and Tovkach, F.I., Effect of exogenous plasmid R68.45 on productive and lisogenic development of temperate bacteriophage ZF40 Erwinia carotovora, Mikrobiol. Zh., 2006, vol. 68, no. 2, pp. 48–57.

18. Cooper, L.P., Roberts, G.A., White, J.H., Luyten, Y.A., Bower, E.K.M., Morgan, R.D., Roberts, R.J., Lindsay, J.A., and Dryden, D.T.F., DNA target recognition domains in the type I restriction and modification systems of Staphylococcus aureus, Nucleic Acids Res., 2017. https://doi.org/10.1093/nar/gkx067

19. Cuecas, A., Kanoksilapatham, W., and Gonzalez, J.M., Evidence of horizontal gene transfer by transposase gene analyses in Fervidobacterium species, PLoS One, 2017. https://doi.org/10.1371/journal.pone.0173961

20. Delavat, F., Miyazaki, R., Carraro, N., Pradervand, N., and van der Meer, J.R., The hidden life of integrative and conjugative elements, FEMS Microbiol. Rev., 2017. https://doi.org/10.1093/femsre/fux008

21. Dion, M.B., Oechslin, F., and Moineau, S., Phage diversity, genomics, and phylogeny, Nat. Rev. Microbiol., 2020. https://doi.org/10.1038/s41579-019-0311-5

22. Doron, S., Melamed, S., Ofir, G., Leavitt, A., Lopatina, A., Keren, M., Amitai, G., and Sorek, R., Systematic discovery of antiphage defense systems in the microbial pangenome, Science, 2018. https://doi.org/10.1126/science.aar4120

23. Dufresne, K., Saulnier-Bellemare, J., and Daigle, F., Functional analysis of the Chaperone-Usher fimbrial gene clusters of Salmonella enterica serovar typhi, Front. Cell Infect. Microbiol., 2018. https://doi.org/10.3389/fcimb.2018.00026

24. Dydecka, A., Bloch, S., Necel, A., Topka, G., Wegrzyn, A., Tong, J., Donaldson, L.W., Wegrzyn, G., and Nejman-Falenczyk, B., The ea22 gene of lambdoid phages: preserved prolysogenic function despite of high sequence diversity, Virus Genes, 2020. https://doi.org/10.1007/si1262-020-01734-8

25. Fernández, La, Rodríguez, A., and Garchí, P., Phage or foe: an insight into the impact of viral predation on microbial communities, ISME J., 2018. https://doi.org/10.1038/s41396-018-0049-5

26. Fillol-Salom, A., Martínez-Rubio, R., Abdulrahman, R., Chen, J., Davies, R., and Penadés, J., Phage-inducible chromosomal islands are ubiquitous within the bacterial universe, ISME J., 2018. https://doi.org/10.1038/s41396-018-0156-3

27. Flodman, K., Tsai, R., Xu, M.Y., Cornea, I.R., Alyssa, C., Lee, Y.-J., Xu, M.-Q., Weigele, P., and Xu, S-yong, Type II restriction of bacteriophage DNA with 5hmdU-derived base modifications, Front. Microbiol., 2019. https://doi.org/10.3389/fmicb.2019.00584

28. Fuller, J.R. and Rice, P.A., Target DNA bending by the Mu transpososome promotes careful transposition and prevents its reversal, eLife, 2017. https://doi.org/10.7554/eLife.21777

29. González-Montes, L., del Campo, I., Garcillán-Barcia, M.P., de la Cruz, F., and Moncalián, G., ArdC, a ssDNA-binding protein with a metalloprotease domain, overpasses the recipient hsdRMS restriction system broadening conjugation host range, PLoS Genet., 2016. https://doi.org/10.1371/journal.pgen.l008750

30. Goryanin, I.I., Kudryavtseva, A.A., Balabanov, V.P., Biryukova, V.S., Manukhov, I.V., and Zavilgelsky, G.B., Antirestriction activities of KlcA (RP4) and ArdB (R64) proteins, FEMS Microbiol. Lett., 2018. https://doi.org/10.1093/femsle/fny227

31. Guo, F., Xiong, L., Zhang, K.-Y., Dong, C., Zhang, F.-Z., and Woo, P.C.Y., Identification and analysis of genomic islands in Burkholderia cenocepacia AU 1054 with emphasis on pathogenicity islands, BMC Microbiol., 2017. https://doi.org/10.1186/sl2866-017-0986-6

32. Guo, Y., Quiroga, C., Chen, Q., McAnulty, M.J., Benedik, M.J., Wood, T.K., and Wang, X., RalR (a DNase) and RalA (a small RNA) form a type I toxin-antitoxin system in Escherichia coli, Nucleic Acids Res., 2014. https://doi.org/10.1093/nar/gku279

33. Hacker, J. and Kaper, J., Pathogenicity islands and the evolution of microbes, Annu. Rev. Microbiol., 2000. https://doi.org/10.1146/annurev.micro.54.1.641

34. Hampton, H., Watson, B., and Fineran, P., The arms race between bacteria and their phage foes, Nature, 2020. https://doi.org/10.1038/s41586-019-1894-8

35. Harms, A., Brodersen, D., Mitarai, N., and Gerdes, K., Toxins, targets, and triggers: an overview of toxin-antitoxin biology, Mol. Cell, 2018. https://doi.org/10.1016/j.molcel.2018.01.003

36. Harrison, E., Hall, J.P.J., Paterson, S., Spiers, A.J., and Brockhurstn, M.A., Conflicting selection alters the trajectory of molecular evolution in a tripartite bacteria–plasmid–phage interaction, Mol. Ecol., 2017. https://doi.org/10.1111/mec.14080

37. Harshey, R.M., Transposable phage Mu, Microbiol. Spectr., 2014. https://doi.org/10.1128/microbiolspec.MDNA3-0007-2014

38. Hatfull, G.F., Molecular biology of bacteriophages, in Molecular Genetics of Mycobacteria, Washington: ASM Press, 2000, pp. 37–54.

39. Hayes, S., Rajamanickam, K., and Hayes, C., Complementation studies of bacteriophage λ O amber mutants by allelic forms of O expressed from plasmid, and O-P interaction phenotypes, Antibiotics (Basel), 2018. https://doi.org/10.3390/antibiotics7020031

40. Hernandez-Doria, J.D. and Sperandio, V., Bacteriophage transcription factor Cro regulates virulence gene expression in enterohemorrhagic Escherichia coli, Cell Host Microbe, Author Manuscript, 2018. https://doi.org/10.1016/j.chom.2018.04.007

Book

41. Iranzo, J., Cuesta, J., Manrubia, S., Katsnelson, M.I., and Koonin, E., Disentangling the effects of selection and loss bias on gene dynamics, Proc. Natl. Acad. Sci. U. S. A., 2017. https://doi.org/10.1073/pnas.1704925114

42. Isaev, A., Drobiazko, A., Sierro, N., Gordeeva, J., Yosef, I., Qimron, U., Ivanov, N., and Severinov, K., Phage T7 DNA mimic protein Ocr is a potent inhibitor of BREX defence, Nucleic Acids Res., 2020. https://doi.org/10.1093/nar/gkaa290

43. Kajun, G.L., Doszpoly, A., Tarjun, Z.L., Vidovszky, M.Z., and Papp, T., Virus–host coevolution with a focus on animal and human DNA Viruses, J. Mol. Evol., 2020. https://doi.org/10.1007/s00239-019-09913-4

44. Kamruzzaman, M., Shoma, S., Thomas, C.M., Partridge, S.R., and Iredell, J.R., Plasmid interference for curing antibiotic resistance plasmids in vivo, PLoS One, 2020. https://doi.org/10.1371/journal.pone.0172913

45. Karkouri, K., Pontarotti, P., Raoult, D., and Fournier, P.-E., Origin and evolution of rickettsial plasmids, PLoS One, 2016. https://doi.org/10.1371/journal.pone.0147492

46. Kelleher, P., Bottacini, F., Mahony, J., Kilcawley, K.N., and van Sinderen, D., Comparative and functional genomics of the Lactococcus lactis taxon; insights into evolution and niche adaptation, BMC Genomics, 2017. https://doi.org/10.1186/s12864-017-3650-5

47. Kelleher, P., Mahony, J., Bottacini, F., Lugli, G.A., Ventura, M., and van Sinderen, D., The Lactococcus lactis Pan-plasmidome, Front. Microbiol., 2019. https://doi.org/10.3389/fmicb.2019.00707

48. Kobayashi, I., Behavior of restriction-modification system as mobile elements and their impact on genome evolution, Nucleic Acids Res., 2001. https://doi.org/10.1093/nar/29.18.3742

49. Koonin, E.V., Makarova, K.S., and Wolf, Y.I., Evolutionary genomics of defense systems in archaea and bacteria, Annu. Rev. Microbiol., 2017. https://doi.org/10.1146/annurev-micro-090816-093830

50. Kushkina, A.I. and Tovkach, F.I., Bacteria lysogeny and its significance for biotechnology, Biotechnologiya, 2011, no. 1, pp. 29–40.

51. Kwong, S.M., Ramsay, J.P., Jensen, S.O., and Firth, N., Replication of staphylococcal resistance plasmids, Front. Microbiol., 2017. https://doi.org/10.3389/fmicb.2017.02279

52. Lewis, K., Programmed death in bacteria, Microbiol. Mol. Biol. Rev., 2000. https://doi.org/10.1128/mmbr.64.3.503-514.2000

53. Li, Y., Liu, X., Tang, K., Wang, P., Zeng, Z., Guo, Y., and Wang, X., Excisionase in Pf filamentous prophage controls lysis–lysogeny decision-making in Pseudomonas aeruginosa, Mol. Microbiol., 2019. https://doi.org/10.1111/mmi.14170

54. Magaziner, S., Zeng, Z., Chen, B., and Salmond, G., The prophages of Citrobacter rodentium represent a conserved family of horizontally acquired mobile genetic elements associated with enteric evolution towards pathogenicity, J. Bacteriol., 2019. https://doi.org/10.1128/JB.00638-18

55. Martínez-Rubio, R., Quiles-Puchalt, N., Martí, M., Humphrey, S., Ram, G., Smyth, D., Chen, J., Novick, R.P., and Penadés, J.R., Phage-inducible islands in the Gram-positive cocci, ISME J., 2017. https://doi.org/10.1038/ismej.2016.163

56. Masuda, H. and Inouye, M., Toxins of prokaryotic toxin–antitoxin systems with sequence-specific endo-ribonuclease activity, Toxins (Basel), 2017. https://doi.org/10.3390/toxins9040140

57. McGurk, M.P. and Barbash, D.A., Double insertion of transposable elements provides a substrate for the evolution of satellite DNA, Genome Res., 2018. https://doi.org/10.1101/gr.231472.117

58. McInerney, J.O., McNally, A., and O’Connell, M.J., Why prokaryotes have pangenomes, Nat. Microbiol., 2017. https://doi.org/10.1038/nmicrobiol.2017.40

59. Mei, H., Arbeithuber, B., Cremona, M.A., DeGiorgio, M., and Nekrutenko, A., A high-resolution view of adaptive event dynamics in a plasmid genome, Biol. Evol., 2019. https://doi.org/10.1093/gbe/evz197

60. Moon, B., Park, J.Y., Robinson, D.A., Thomas, J.C., Park, Y.H., Thornton, J.A., and Seo, K.S., Mobilization of genomic islands of Staphylococcus aureus by temperate bacteriophage, PLoS One, 2016. https://doi.org/10.1371/journal.pone.0151409

61. Morozova, N., Sabantsev, A., Bogdanova, E., Fedorova, Y., Maikova, A., Vedyaykin, A., Rodic, A., Djordjevic, M., Khodorkovskii, M., and Severinov, K., Temporal dynamics of methyltransferase and restriction endonuclease accumulation in individual cells after introducing a restriction-modification system, Nucleic Acids Res., 2016. https://doi.org/10.1093/nar/gkv1490

62. Mruk, I. and Kobayashi, I., To be or not to be: regulation of restriction-modification systems and other toxin-antitoxin systems, Nucleic Acids Res., 2014. https://doi.org/10.1093/nar/gkt711

63. Mutai, W.C., Waiyaki, P.G., Kariuki, S., and Muigai, A.W.T., Plasmid profiling and incompatibility grouping of multidrug resistant Salmonella enterica serovar Typhi isolates in Nairobi, Kenya, BMC Res Notes, 2019. https://doi.org/10.1186/s13104-019-4468-9

64. Nagamalleswari, E., Rao, S., Vasu, K., and Nagaraja, V., Restriction endonuclease triggered bacterial apoptosis as a mechanism for long time survival, Nucleic Acids Res., 2017. https://doi.org/10.1093/nar/gkx576

65. Nicolas, E., Oger, C., Nguyen, N., Lambin, M., Draime, A., Leterme, S., Chandler, M., and Hallet, B., Unlocking Tn3-family transposase activity in vitro unveils an asymmetric pathway for transposome assembly, Proc. Natl. Acad. Sci. U. S. A., 2017. https://doi.org/10.1073/pnas.1611701114

66. Novick, R.P., Plasmid incompatibility, Microbiol. Rev., 1987, vol. 51, no. 4, pp. 381–395.

67. Novick, R.P. and Ram, G., Staphylococcal pathogenicity islands—movers and shakers in the genomic firmament, Curr. Opin. Microbiol., 2017. https://doi.org/10.1016/j.mib.2017.08.001

68. Oliveira, L.C., Saraiva, T.D.L., Silva, W.M., Pereira, U.P., Campos, B.C., Benevides, L.J., Rocha, F.S., Figueiredo, H.C.P., Azevedo, V., and Soares, S.C., Analyses of the probiotic property and stress resistance-related genes of Lactococcus lactis subsp. lactis NCDO 2118 through comparative genomics and in vitro assays, PLoS One, 2017. https://doi.org/10.1371/journal.pone.0175116

69. Oliveira, P.H., Touchon, M., and Rocha, E.P., Regulation of genetic flux between bacteria by restriction-modification systems, Proc. Natl. Acad. Sci. U. S. A., 2016. https://doi.org/10.1073/pnas.1603257113

70. Orlek, A., Stoesser, N., Anjum, M.F., Doumith, M., Ellington, M.J., Peto, T., Crook, D., Woodford, N., Walker, A.S., Phan, H., and Sheppard, A.E., Plasmid classification in an era of whole-genome sequencing: application in studies of antibiotic resistance epidemiology, Front. Microbiol., 2017. https://doi.org/10.3389/fmicb.2017.00182

71. Partridge, S., Kwong, S., Firth, N., and Jensen, S., Mobile genetic elements associated with antimicrobial resistance, Clin. Microbiol. Rev., 2018. https://doi.org/10.1128/CMR.00088-17

72. Petrovska, L., Mather, A.E., Abuoun, M., Branchu, P., Harris, S.R., Connor, T., Hopkins, K.L., Underwood, A., Lettini, A.A., Page, A., Bagnall, M., Wain, J., Parkhill, J., Dougan, G., Davies, R., and Kingsley, R.A., Microevolution of monophasic Salmonella typhimurium during epidemic, United Kingdom, 2005–2010, Emerg. Infect. Dis., 2016. https://doi.org/10.3201/eid2204.150531

73. Pica-Iturbe, A., Ulloa-Allendes, D., Pardo-Roa, C., Coronado-Arrázola, I., Salazar-Eegarai, F.J., Sclavi, B., González, P.A., and Bueno, S.M., Comparative and phylogenetic analysis of a novel family of Enterobacteriaceae-associated genomic islands that share a conserved excision/integration module, Sci. Rep., 2018. https://doi.org/10.1038/s41598-018-28537-0

74. Pingoud, A., Wilson, G.G., and Wende, W., Type II restriction endonucleases — a historical perspective and more, Nucleic Acids Res., 2016. https://doi.org/10.1093/nar/gkw513

75. Plejbka, M., Qian, L., Okura, R., Bergmiller, T., Wakamoto, Y., Kussell, E., et al., Bacterial autoimmunity due to a restriction-modification system, Curr. Biol., 2016. https://doi.org/10.10l6/j.cub.2015.12.041

76. Porter, S., Faber-Hammond, J., Montoya, A., Friesen, M., and Sackos, C., Dynamic genomic architecture of mutualistic cooperation in a wild population of Mesorhizobium, ISME J., 2019. https://doi.org/10.1038/s41396-018-0266-y

77. Ramisetty, B.C.M. and Sudhakari, P.A., Bacterial ‘grounded’ prophages: hotspots for genetic renovation and innovation, Front. Genet., 2019. https://doi.org/10.3389/fgene.2019.00065

78. Roberts, R.J., Belford, M., Bestor, T., Bhagwat, A.S., Bickle, T.A., et al., A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases, and their genes, Nucl. Acids Res., 2017. https://doi.org/10.1093/nar/gkg274

79. Ronayne, E.A., Wan, S., Boudreau, B.A., Landick, R., and Cox, M.M., PI Ref endonuclease: a molecular mechanism for phage-enhanced antibiotic lethality, PLoS Genet., 2016. https://doi.org/10.1371/journal.pgen.l005797

80. Ruiz-Masy, J., Luengo, L.M., Moreno-Cyrdoba, I., Diaz-Orejas, R., and del Solar, G., Successful establishment of plasmids Rl and pMV158 in a new host requires the relief of the transcriptional repression of their essential rep genes, Front. Microbiol., 2017. https://doi.org/10.3389/fmicb.2017.02367

81. Sánchez-Busy, L., Golparian, D., Parkhill, J., Unemo, M., and Harris, S.R., Genetic variation regulates the activation and specificity of restriction-modification systems in Neisseria gonorrhoeae, Sci. Rep., 2019. https://doi.org/10.1038/s41598-019-51102-2

82. Sezonov, G., Possoz, C., Friedmann, A., Pernodet, J.-L., and Guérineau, M., KorSA from the Streptomyces integrative element pSAM2 is a central transcriptional repressor: target genes and binding sites, J. Bacteriol., 2000. https://doi.org/10.1128/jb.182.5.1243-1250.2000

83. Silva, C., Calva, E., Fernández-Mora, M., Puente, J.L., and Vinuesa, P., Population analysis of D6-like plasmid prophage variants associated with specific IncC plasmid types in the emerging Salmonella typhimurium ST213 genotype, PLoS One, 2019.https://doi.org/10.1371/journal.pone.0223975/

84. Silveira, C.B., Coutinho, F.H., Cavalcanti, G.S., Benler, S., Doane, M.P., Dinsdale, E.A., Edwards, R.A., Francini-Filho, R.B., Thompson, C.C., Luque, A., Rohwer, F.L., and Thompson, F., Genomic and ecological attributes of marine bacteriophages encoding bacterial virulence genes, BMC Genomics, 2020. https://doi.org/10.1186/sl2864-020-6523-2

85. Sinha, A. and Maurice, C.F., Bacteriophages: uncharacterized and dynamic regulators of the immune system mediators, Inflammation, 2019. https://doi.org/10.1155/2019/3730519

86. Sklyar, T.V., Lavrentiev, K.V., Gavrilyuk, V.G., Kurahina, N.V., Vereshchaha, M.O., and Lykholat, O.A., Monitoring of multiresistant community-associated MRSA strains from patients with pathological processes of different localization, Reg. Mech. Biol., 2018, no. 2, pp. 281–286. https://doi.org/10.15421/021841

87. Staehlin, B.M., Gibbons, J.G., Rokas, A., O’Halloran, T.V., and Slot, J.C., Evolution of a heavy metal homeostasis/resistance island reflects increasing copper stress in enterobacteria, Genome Biol. Evol., 2016. https://doi.org/10.1093/gbe/evw031

88. Tarazanova, M., Beerthuyzen, M., Siezen, R., Fernandez-Gutierrez, M.M., de Jong, A., van der Meulen, S., Kok, J., and Bachmann, H., Plasmid complement of Lactococcus lactis NCDO712 reveals a novel pilus gene cluster, PLoS One, 2016. https://doi.org/10.1371/journal.pone.0167970

89. Thomas, A.T., Brammar, W.J., and Wilkins, B.M., Plasmid R16 ArdA Protein preferentially targets restriction activity of the type i restriction-modification system EcoKI, J. Bacteriol., 2003. https://doi.org/10.1128/JB.185.6.2022-2025.2003

90. Tock, M.R. and Dryden, D.T., The biology of restriction and anti-restriction, Curr. Opin. Microbiol., 2005, vol. 8, pp. 466–472. https://doi.org/10.1016/j.mib.2005.06.003

91. Tovkach, F.I. and Chervatiuk, N.V., Phage system for studying the restriction-modification of Erwinia carotovora, Mikrobiol. Zh., 2006, vol. 68, no. 6, pp. 27–35.

92. Toussaint, A., My Life with Mu Bacteriophage, 2015. https://doi.org/10.1080/21597081.2015.1034336

93. Val-Calvo, J., Luque-Ortega, J.R., Crespo, I., Miguel-Arribas, A., Abia, D., Sánchez-Hevia, D.L., Serrano, E., Gago-Cyrdoba, C., Ares, S., Alfonso, C., Rojo, F., Wu, L.J., Boer, D.R., and Meijer, W.J.J., Novel regulatory mechanism of establishment genes of conjugative plasmids, Nucleic Acids Res., 2017. https://doi.org/10.1093/nar/gky996

94. van Houte, S., Buckling, A., and Westra, E.R., Evolutionary ecology of prokaryotic immune mechanisms, Microbiol. Mol. Biol. Rev., 2016.https://doi.org/10.1128/MMBR.00011-16

95. Wahl, A., Battesti, A., and Ansaldi, M., Prophages in Salmonella enterica: a driving force in reshaping the genome and physiology of their bacterial host?, Mol. Microbiol., 2019. https://doi.org/10.1111/mmi.14167

96. Wan, T.-W., Higuchi, W., Khokhlova, O., Hung, W.-C., Iwao, Y., Wakayama, M., Inomata, N., Takano, T., Lin, Y.-T., Peryanova, O., Kojima, K., Salmina, A., Teng, L.-J., and Yamamoto, T., Genomic comparison between Staphylococcus aureus GN strains clinically isolated from a familial infection case: IS1272 transposition through a novel inverted repeat-replacing mechanism, PLoS One, 2017. https://doi.org/10.1371/journal.pone.0187288

97. Wang, B., Zhao, A., Xie, Q., Olinares, P.D., Chait, B.T., Novick, R.P., and Muir, T.W., Functional plasticity of the AgrC receptor histidine kinase required for staphylococcal virulence, Cell Chem. Biol., 2017. https://doi.org/10.1016/j.chembiol.2016.12.008

98. Wang, H.-.C., Lin, S.-.J., Mohapatra, A., Kumar, R., and Wang, H.-C., A review of the functional annotations of important genes in the AHPND-causing pVA1 plasmid, Microorganisms, 2020. https://doi.org/10.3390/micro-organisms8070996

99. Wegrzyn, K.E., Gross, M., Uciechowska, U., and Konieczny, I., Replisome assembly at bacterial chromosomes and iteron plasmids, Front. Mol. Biosci., 2016. https://doi.org/10.3389/fmolb.2016.00039

100. Wilkowska, K., Mruk, I., Furmanek-Blaszk, B., and Sektas, M., Low-level expression of the type II restriction-modification system confers potent bacteriophage resistance in Escherichia coli, DNA Res., 2020. https://doi.org/10.1093/dnares/dsaa003

101. Wons, E., Mruk, I., and Kaczorowski, T., Isospecific adenine DNA methyltransferases show distinct preferences towards DNA substrates, Sci. Rep., 2018. https://doi.org/10.1038/s41598-018-26434-0

102. Wright, R., Brockhurst, M.A., and Harrison, E., Ecological conditions determine extinction risk in co-evolving bacteria–phage populations, 2016. https://doi.org/10.1186/s12862-016-0808-8

103. Yano, H., Wegrzyn, K., Loftie-Eaton, W., et al., Evolved plasmid–host interactions reduce plasmid interference cost, Mol. Microbiol., 2016. https://doi.org/10.1111/mmi.13407

104. Yano, H., Wegrzyn, K., Loftie-Eaton, W., Johnson, J., Deckert, G.E., Rogers, L.M., Konieczny, I., and Top, E.M., Evolved plasmid–host interactions reduce plasmid interference cost, Mol. Microbiol., 2017. https://doi.org/10.1111/mmi.13407

105. Yano, H., Shintani, M., Tomita, M., Suzuki, H., and Oshima, T., Reconsidering plasmid maintenance factors for computational plasmid design, Comput. Struct. Biotechnol. J., 2019. https://doi.org/10.1016/j.csbj.2018.12.001

106. Yarmolinsky, M.B., Bacteriophage P1 in retrospect and in prospect, J. Bacteriol., 2004. https://doi.org/10.1128/JB.186.21.7025-7028.2004

107. Zhang, Y., Matsuzaka, T., Yano, H., Furuta, Y., Nakano, T., Ishikawa, K., Fukuyo, M., Takahashi, N., Suzuki, Y., Sugano, S., Ide, H., and Kobayashi, I., Restriction glycosylases: involvement of endonuclease activities in the restriction process, Nucleic Acids Res., 2017. https://doi.org/10.1093/nar/gkw1250

108. Zheng, H., Dietrich, C., Hongoh, Y., and Brune, A., Restriction-modification systems as mobile genetic elements in the evolution of an intracellular symbiont, Mol. Biol. Evol., 2016. https://doi.org/10.1093/molbev/msv-264