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Structural Features, Mechanisms of Action, and Prospects for Practical Application of Class II Bacteriocins

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Abstract

Bacteriocins are antimicrobial peptides ribosomally synthesized by both Gram-negative and Gram-positive bacteria, as well as by archaea. Bacteriocins are usually active against phylogenetically related bacteria, providing competitive advantage to their producers in the natural bacterial environment. However, some bacteriocins are known to have a broader spectrum of antibacterial activity, including activity against multidrug-resistant bacterial strains. Multitude of bacteriocins studied to date are characterized by a wide variety of chemical structures and mechanisms of action. Existing classification systems for bacteriocins take into account structural features and biosynthetic pathways of bacteriocins, as well as the phylogenetic affiliation of their producing organisms. Heat-stable bacteriocins with molecular weight of less than 10 kDa from Gram-positive and Gram-negative producers are divided into post-translationally modified (class I) and unmodified peptides (class II). In recent years there has been an increasing interest in the class II bacteriocins as potential therapeutic agents that can help to combat antibiotic-resistant infections. Advantages of unmodified peptides are relative simplicity of their biotechnological production in heterologous systems and chemical synthesis. Potential for the combined use of bacteriocins with other antimicrobial agents allowing to enhance their efficacy, low probability of cross-resistance development, and ability of probiotic strains to produce bacteriocins in situ make them promising candidate compounds for creation of new drugs. The review focuses on structural diversity of the class II bacteriocins and their practical relevance.

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Abbreviations

ABC transporter:

ATP-binding cassette transporter

AMP:

antimicrobial peptides

LAB:

lactic acid bacteria

Man-PTS:

the mannose phosphotransferase system

References

  1. De Kraker, M. E. A. (2016) Will 10 million people die a year due to antimicrobial resistance by 2050? PLoS Med., 13, 1-6, https://doi.org/10.1371/journal.pmed.1002184.

    Article  Google Scholar 

  2. Drider, D., and Rebuffat, S. (2011) Prokaryotic Antimicrobial Peptides. From Genes to Applications, Springer, pp. 1-451, https://doi.org/10.1007/978-1-4419-7692-5.

  3. Klaenhammer, T. R. (1993) Genetics of bacteriocins produced by lactic acid bacteria, FEMS Microbiol. Rev., 12, 39-85, https://doi.org/10.1111/j.1574-6976.1993.tb00012.x.

    Article  CAS  PubMed  Google Scholar 

  4. Cotter, P. D., Ross, R. P., and Hill, C. (2013) Bacteriocins – a viable alternative to antibiotics? Nat. Rev. Microbiol., 11, 95-105, https://doi.org/10.1038/nrmicro2937.

    Article  CAS  PubMed  Google Scholar 

  5. Alvarez-Sieiro, P., Montalbán-López, M., and Kuipers, O. P. (2016) Bacteriocins of lactic acid bacteria: extending the family, Appl. Microbiol. Biotechnol., 100, 2939-2951, https://doi.org/10.1007/s00253-016-7343-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Nissen-Meyer, J., Rogne, P., Oppegård, C., Haugen, H. S., and Kristiansen, P. E. (2009) Structure-function relationships of the non-lanthionine-containing peptide (class II) bacteriocins produced by Gram-positive bacteria, Curr. Pharm. Biotechnol., 10, 19-37, https://doi.org/10.2174/138920109787048661.

    Article  CAS  PubMed  Google Scholar 

  7. Simons, A., Alhanout, K., and Duval, R. E. (2020) Bacteriocins, antimicrobial peptides from bacterial origin: overview of their biology and their impact against multidrug-resistant bacteria, Microorganisms, 8, 1-31, https://doi.org/10.3390/microorganisms8050639.

    Article  CAS  Google Scholar 

  8. Zouhir, A., Hammami, R., Fliss, I., and Hamida, J. B. (2010) A new structure-based classification of Gram-positive bacteriocins, Protein J., 29, 432-439, https://doi.org/10.1007/s10930-010-9270-4.

    Article  CAS  PubMed  Google Scholar 

  9. Zimina, M., Babich, O., Prosekov, A., Sukhikh, S., Ivanova, S., Shevchenko, M., and Noskova, S. (2020) Overview of global trends in classification, methods of preparation and application of bacteriocins, Antibiotics (Basel), 9, 553-574, https://doi.org/10.3390/antibiotics9090553.

    Article  CAS  Google Scholar 

  10. Field, D., Cotter, P. D., Colin, H., and Ross, R. P. (2015) Bioengineering lantibiotics for therapeutic success, Front. Microbiol., 6, 1-8, https://doi.org/10.3389/fmicb.2015.01363.

    Article  Google Scholar 

  11. Rebuffat, S. (2012) Microcins in action: amazing defence strategies of Enterobacteria, Biochem. Soc. Trans., 40, 1456-1462, https://doi.org/10.1042/BST20120183.

    Article  CAS  PubMed  Google Scholar 

  12. Yanglei, Y., Ping, L., Zhao, F., and Zhang, T. (2022) Current status and potentiality of class II bacteriocins from lactic acid bacteria: structure, mode of action and applications in the food industry, Trends Food Sci. Technol., 120, 387-401, https://doi.org/10.1016/j.tifs.2022.01.018.

    Article  CAS  Google Scholar 

  13. Zhang, T., Zhang, Y., Li, L., and Jiang, X. (2022) Biosynthesis and production of class II bacteriocins of food-associated lactic acid bacteria, Fermentation, 8, 1-32, https://doi.org/10.3390/fermentation8050217.

    Article  CAS  Google Scholar 

  14. Ríos Colombo, N. S., Chalón, M. C., Navarro, S. A., and Bellomio, A. (2018) Pediocin-like bacteriocins: new perspectives on mechanism of action and immunity, Curr. Genet., 64, 345-351, https://doi.org/10.1007/s00294-017-0757-9.

    Article  CAS  PubMed  Google Scholar 

  15. Balandin, S. V., Sheremeteva, E. V., and Ovchinnikova, T. V. (2019) Pediocin-like antimicrobial peptides of bacteria, Biochemistry (Moscow), 84, 464-478, https://doi.org/10.1134/S000629791905002X.

    Article  CAS  Google Scholar 

  16. Oppegård, C., Rogne, P., Emanuelsen, L., Kristiansen, P. E., Fimland, G., and Nissen-Meyer, J. (2007) The two-peptide class II bacteriocins: structure, production, and mode of action, J. Mol. Microbiol. Biotechnol., 13, 210-219, https://doi.org/10.1159/000104750.

    Article  CAS  PubMed  Google Scholar 

  17. Perez, R. D., Zendo, T., and Sonomoto, K. (2018) Circular and leaderless bacteriocins: biosynthesis, mode of action, applications, and prospects, Front. Microbiol., 9, 1-18, https://doi.org/10.3389/fmicb.2018.02085.

    Article  CAS  Google Scholar 

  18. Wu, Y., Pang, X., Wu, Y., Liu, X., and Zhang, X. (2022) Enterocins: classification, synthesis, antibacterial mechanisms and food applications, Molecules, 27, 1-14, https://doi.org/10.3390/molecules27072258.

    Article  CAS  Google Scholar 

  19. Beckwith, J. (2013) The Sec-dependent pathway, Res. Microbiol., 164, 497-504, https://doi.org/10.1016/j.resmic.2013.03.007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Gajic, O., Buist, G., Kojic, M., Topisirovic, L., Kuipers, O. P., and Kok, J. (2003) Novel mechanism of bacteriocin secretion and immunity carried out by lactococcal multidrug resistance proteins, J. Biol. Chem., 278, 34291-34298, https://doi.org/10.1074/jbc.M211100200.

    Article  CAS  PubMed  Google Scholar 

  21. Diep, D. B., Håvarstein, L. S., and Nes, I. F. (1996) Characterization of the locus responsible for the bacteriocin production in Lactobacillus plantarum C11, J. Bacteriol., 178, 4472-4483, https://doi.org/10.1128/jb.178.15.4472-4483.1996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Hauge, H. H., Mantzilas, D., Moll, G. N., Konings, W. N., Driessen, A. J., Eijsink, V. G., and Nissen-Meyer, J. (1998) Plantaricin A is an amphiphilic alpha-helical bacteriocin-like pheromone which exerts antimicrobial and pheromone activities through different mechanisms, Biochemistry, 37, 16026-16032, https://doi.org/10.1021/bi981532j.

    Article  CAS  PubMed  Google Scholar 

  23. Khorshidian, N., Khanniri, E., Mohammadi, M., Mortazavian, A. M., and Yousefi, M. (2021) Antibacterial activity of pediocin and pediocin-producing bacteria against Listeria monocytogenes in meat products, Front. Microbiol., 12, 1-16, https://doi.org/10.3389/fmicb.2021.709959.

    Article  Google Scholar 

  24. Jin, J., Jie, L., Zhang, H., Xie, Y., Liu, H., Gao, X., and Zhang, H. (2020) Pediocin AcH is transcriptionally regulated by a two-component system in Lactobacillus plantarum subsp. plantarum, J. Food Prot., 83, 1693-1700, https://doi.org/10.4315/JFP-19-587.

    Article  PubMed  Google Scholar 

  25. Kanatani, K., Oshimura, M., and Sano, K. (1995) Isolation and characterization of acidocin A and cloning of the bacteriocin gene from Lactobacillus acidophilus, Appl. Environ. Microbiol., 61, 1061-1067, https://doi.org/10.1128/aem.61.3.1061-1067.1995.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Zhang, Y., Yang, J., Liu, Y., and Wu, Y. (2020) A novel bacteriocin PE-ZYB1 produced by Pediococcus pentosaceus zy-B isolated from intestine of Mimachlamys nobilis: Purification, identification and its anti-listerial action, LWT, 118, 1-9, https://doi.org/10.1080/13102818.2020.1830714.

    Article  CAS  Google Scholar 

  27. Stern, N. J., Svetoch, E. A., Eruslanov, B. V., Perelygin, V. V., Mitsevich, E. V., Mitsevich, I. P., Pokhilenko, V. D., Levchuk, V. P., Svetoch, O. E., and Seal, B. S. (2006) Isolation of a Lactobacillus salivarius strain and purification of its bacteriocin, which is inhibitory to Campylobacter jejuni in the chicken gastrointestinal system, Antimicrob. Agents Chemother., 50, 3111-3116, https://doi.org/10.1128/AAC.00259-06.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Zommiti, M., Almohammed, H., and Ferchichi, M. (2016) Purification and characterization of a novel anti-campylobacter bacteriocin produced by Lactobacillus curvatus DN317, Probiotics Antimicrob. Proteins, 8, 191-201, https://doi.org/10.1007/s12602-016-9237-7.

    Article  CAS  PubMed  Google Scholar 

  29. Xiraphi, N., Georgalaki, M., and Driessche, G. V. (2006) Purification and characterization of curvaticin L442, a bacteriocin produced by Lactobacillus curvatus L442, Antonie Van Leeuwenhoek, 89, 19-26, https://doi.org/10.1007/s10482-005-9004-3.

    Article  CAS  PubMed  Google Scholar 

  30. Gallagher, N. L. F., Sailer, M., Niemczura, W. P., Nakashima, T. T., Stiles, M. E., and Vederas, J. C. (1997) Three-dimensional structure of leucocin A in trifluoroethanol and dodecylphosphocholine micelles: spatial location of residues critical for biological activity in type IIa bacteriocins from lactic acid bacteria, Biochemistry, 36, 15062-15072, https://doi.org/10.1021/bi971263h.

    Article  CAS  Google Scholar 

  31. Bédard, F., Hammami, R., Zirah, S., Rebuffat, S., Fliss, I., and Biron, E. (2018) Synthesis, antimicrobial activity and conformational analysis of the class IIa bacteriocin pediocin PA-1 and analogs thereof, Sci. Rep., 8, 1-13, https://doi.org/10.1038/s41598-018-27225-3.

    Article  CAS  Google Scholar 

  32. Haugen, H. S., Fimland, G., Nissen-Meyer, J., and Kristiansen, P. E. (2005) Three-dimensional structure in lipid micelles of the pediocin-like antimicrobial peptide curvacin A, Biochemistry, 44, 16149-16157, https://doi.org/10.1021/bi051215u.

    Article  CAS  PubMed  Google Scholar 

  33. Uteng, M., Hauge, H. H., Markwick, P. R., Fimland, G., Mantzilas, D., Nissen-Meyer, J., and Muhle-Goll, C. (2003) Three-dimensional structure in lipid micelles of the pediocin-like antimicrobial peptide sakacin P and a sakacin P variant that is structurally stabilized by an inserted C-terminal disulfide bridge, Biochemistry, 42, 11417-11426, https://doi.org/10.1021/bi034572i.

    Article  CAS  PubMed  Google Scholar 

  34. Arbulu, S., Lohans, C. T., van Belkum, M. J., Cintas, L. M., Herranz, C., Vederas, J. C., and Hernández, P. E. (2015) Solution structure of enterocin HF, an antilisterial bacteriocin produced by Enterococcus faecium M3K31, J. Agric. Food Chem., 63, 10689-10695, https://doi.org/10.1021/acs.jafc.5b03882.

    Article  CAS  PubMed  Google Scholar 

  35. Wang, Y., Henz, M. E., Gallagher, N. L., Chai, S., Gibbs, A. C., Yan, L. Z., Stiles, M. E., Wishart, D. S., and Vederas, J. C. (1999) Solution structure of carnobacteriocin B2 and implications for structure-activity relationships among type IIa bacteriocins from lactic acid bacteria, Biochemistry, 38, 15438-15447, https://doi.org/10.1021/bi991351x.

    Article  CAS  PubMed  Google Scholar 

  36. Nissen-Meyer, J., Holo, H., Håvarstein, L. S., Sletten, K., and Nes, I. F. (1992) A novel lactococcal bacteriocin whose activity depends on the complementary action of two peptides, J. Bacteriol., 74, 5686-5692, https://doi.org/10.1128/jb.174.17.5686-5692.1992.

    Article  Google Scholar 

  37. Anderssen, E. L., Diep, D. B., Nes, I. F., Eijsink, V. G., and Nissen-Meyer, J. (1998) Antagonistic activity of Lactobacillus plantarum C11: two new two-peptide bacteriocins, plantaricins EF and JK, and the induction factor plantaricin A, Appl. Environ. Microbiol., 64, 2269-2272, https://doi.org/10.1128/AEM.64.6.2269-2272.1998.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Tahara, T., Oshimura, M., Umezawa, C., and Kanatani, K. (1996) Isolation, partial characterization, and mode of action of acidocin J1132, a two-component bacteriocin produced by Lactobacillus acidophilus JCM 1132, Appl. Environ. Microbiol., 62, 892-897, https://doi.org/10.1128/aem.62.3.892-897.1996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Fontaine, L., and Pescal, H. (2008) The inhibitory spectrum of thermophilin 9 from Streptococcus thermophilus LMD-9 depends on the production of multiple peptides and the activity of BlpG(St), a thiol-disulfide oxidase, Appl. Environ. Microbiol., 74, 1102-1110, https://doi.org/10.1128/AEM.02030-07.

    Article  CAS  PubMed  Google Scholar 

  40. Rogne, P., Fimland, G., Nissen-Meyer, J., and Kristiansen, P. E. (2008) Three-dimensional structure of the two peptides that constitute the two-peptide bacteriocin lactococcin G, Biochim. Biophys. Acta, 1784, 543-554, https://doi.org/10.1016/j.bbapap.2007.12.002.

    Article  CAS  PubMed  Google Scholar 

  41. Fimland, N., Rogne, P., Fimland, G., Nissen-Meyer, J., and Kristiansen, P. E. (2008) Three-dimensional structure of the two peptides that constitute the two-peptide bacteriocin plantaricin EF, Biochim. Biophys. Acta, 1784, 1711-1719, https://doi.org/10.1016/j.bbapap.2008.05.003.

    Article  CAS  PubMed  Google Scholar 

  42. Rogne, P., Haugen, C., Fimland, G., Nissen-Meyer, J., and Kristiansen, P. E. (2009) Three-dimensional structure of the two-peptide bacteriocin plantaricin JK, Peptides, 30, 1613-1621, https://doi.org/10.1016/j.peptides.2009.06.010.

    Article  CAS  PubMed  Google Scholar 

  43. Ekblad, B., and Kristiansen, P. E. (2019) NMR structures and mutational analysis of the two peptides constituting the bacteriocin plantaricin S, Sci. Rep., 9, 1-10, https://doi.org/10.1038/s41598-019-38518-6.

    Article  Google Scholar 

  44. Acedo, J. Z., Towle, K. M., Lohans, C. T., Miskolzie, M., McKay, R. T., Doerksen, T. A., Vederas, J. C., and Martin-Visscher, L. A. (2017) Identification and three-dimensional structure of carnobacteriocin XY, a class IIb bacteriocin produced by Carnobacteria, FEBS Lett., 591, 1349-1359, https://doi.org/10.1002/1873-3468.12648.

    Article  CAS  PubMed  Google Scholar 

  45. Netz, D. J., Pohl, R., Beck-Sickinger, A. G., Selmer, T., Pierik, A. J., Bastos, M. D. C. F., and Sahl, H. G. (2002) Biochemical characterization and genetic analysis of aureocin A53, a new, atypical bacteriocin from Staphylococcus aureus, J. Mol. Biol., 319, 745-756, https://doi.org/10.1016/S0022-2836(02)00368-6.

    Article  CAS  PubMed  Google Scholar 

  46. Singh, P. K., Chittpurna, Ashish, Sharma, V., Patil, P. B., and Korpole, S. (2012) Identification, purification and characterization of laterosporulin, a novel bacteriocin produced by Brevibacillus sp. strain GI-9, PLoS One, 7, 1-8, https://doi.org/10.1371/journal.pone.0031498.

    Article  CAS  Google Scholar 

  47. Kim, Y. S., Kim, M. J., Kim, P., and Kim, J. H. (2006) Cloning and production of a novel bacteriocin, lactococcin K, from Lactococcus lactis subsp. lactis MY23, Biotechnol. Lett., 28, 357-362, https://doi.org/10.1007/s10529-005-5935-z.

    Article  CAS  PubMed  Google Scholar 

  48. Wang, J., Xu, H., Liu, S., Song, B., Liu, H., Li, F., Deng, S., Wang, G., Zeng, H., Zeng, X., Xu, D., Zhang, B., and Xin, B. (2021) Toyoncin, a novel leaderless bacteriocin that is produced by Bacillus toyonensis XIN-YC13 and specifically targets B. cereus and Listeria monocytogenes, Appl. Environ. Microbiol., 87, 1-14, https://doi.org/10.1128/AEM.00185-21.

    Article  Google Scholar 

  49. Liu, X., Vederas, J. C., Whittal, R. M., Zheng, J., Stiles, M. E., Carlson, D., Franz, C. M., McMullen, L. M., and van Belkum, M. J. (2011) Identification of an N-terminal formylated, two-peptide bacteriocin from Enterococcus faecalis 710C, J. Agric. Food Chem., 59, 5602-5608, https://doi.org/10.1021/jf104751v.

    Article  CAS  PubMed  Google Scholar 

  50. Ovchinnikov, K. V., Chi, H., Mehmeti, I., Holo, H., Nes, I. F., and Diep, D. B. (2016) Novel group of leaderless multipeptide bacteriocins from Gram-positive bacteria, Appl. Environ. Microbiol., 82, 5216-5224, https://doi.org/10.1128/AEM.01094-16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Cintas, L. M., Casaus, P., Holo, H., Hernandez, P. E., Nes, I. F., and Håvarstein, L. S. (1998) Enterocins L50A and L50B, two novel bacteriocins from Enterococcus faecium L50, are related to staphylococcal hemolysins, J. Bacteriol., 180, 1988-1994, https://doi.org/10.1128/JB.180.8.1988-1994.1998.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Acedo, J. Z., van Belkum, M. J., Lohans, C. T., Towle, K. M., Miskolzie, M., and Vederas, J. C. (2016) Nuclear magnetic resonance solution structures of lacticin Q and aureocin A53 reveal a structural motif conserved among leaderless bacteriocins with broad-spectrum activity, Biochemistry, 55, 733-742, https://doi.org/10.1021/acs.biochem.5b01306.

    Article  CAS  PubMed  Google Scholar 

  53. Hammond, K., Lewis, H., Halliwell, S., Desriac, F., Nardone, B., Ravi, J., Hoogenboom, B. W., Upton, M., Derrick, J. P., and Ryadnov, M. G. (2020) Flowering poration – a synergistic multi-mode antibacterial mechanism by a bacteriocin fold, iScience, 23, 1-30, https://doi.org/10.1016/j.isci.2020.101423.

    Article  CAS  Google Scholar 

  54. Śmiałek, J., Nowakowski, M., Bzowska, M., Bocheńska, O., Wlizło, A., Kozik, A., Dubin, G., and Mak, P. (2021) Structure, biosynthesis, and biological activity of succinylated forms of bacteriocin BacSp222, Int. J. Mol. Sci., 22, 1-21, https://doi.org/10.3390/ijms22126256.

    Article  CAS  Google Scholar 

  55. Ovchinnikov, K. V., Kristiansen, P. E., Uzelac, G., Topisirovic, L., Kojic, M., Nissen-Meyer, J., Nes, I. F., and Diep, D. B. (2014) Defining the structure and receptor binding domain of the leaderless bacteriocin LsbB, J. Biol. Chem., 289, 23838-23845, https://doi.org/10.1074/jbc.M114.579698.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Ovchinnikov, K. V., Kristiansen, P. E., Straume, D., Jensen, M. S., Aleksandrzak-Piekarczyk, T., Nes, I. F., and Diep, D. B. (2017) The leaderless bacteriocin enterocin K1 is highly potent against Enterococcus faecium: a study on structure, target spectrum and receptor, Front. Microbiol., 8, 1-12, https://doi.org/10.3389/fmicb.2017.00774.

    Article  CAS  Google Scholar 

  57. Lohans, C., Towle, K. M., Miskolzie, M., McKay, R. T., van Belkum, M. J., McMullen, L. M., and Vederas, J. C. (2013) Solution structures of the linear leaderless bacteriocins enterocin 7A and 7B resemble carnocyclin A, a circular antimicrobial peptide, Biochemistry, 52, 3987-3994, https://doi.org/10.1021/bi400359z.

    Article  CAS  PubMed  Google Scholar 

  58. Singh, P. K., Solanki, V., Sharma, S., Thakur, K. G., Krishnan, B., and Korpole, S. (2015) The intramolecular disulfide-stapled structure of laterosporulin, a class IId bacteriocin, conceals a human defensin-like structural module, FEBS J., 282, 203-214, https://doi.org/10.1111/febs.13129.

    Article  CAS  PubMed  Google Scholar 

  59. Baindara, P., Singh, N., Ranjan, M., Nallabelli, N., Chaudhry, V., Pathania, G. L., Sharma, N., Kumar, A., Patil, P. B., and Korpole, S. (2016) Laterosporulin10: a novel defensin like class IId bacteriocin from Brevibacillus sp. strain SKDU10 with inhibitory activity against microbial pathogens, Microbiology (Reading), 162, 1286-1299, https://doi.org/10.1099/mic.0.000316.

    Article  CAS  Google Scholar 

  60. Li, H. W., Xiang, Y. Z., Zhang, M., Jiang, Y. H., Zhang, Y., Liu, Y. Y., Lin, L. B., and Zhang, Q. L. (2021) A novel bacteriocin from Lactobacillus salivarius against Staphylococcus aureus: Isolation, purification, identification, antibacterial and antibiofilm activity, LWT, 140, 1-10, https://doi.org/10.1016/j.lwt.2020.110826.

    Article  CAS  Google Scholar 

  61. Angelopoulou, A., Warda, A. K., O’Connor, P. M., Stockdale, S. R., Shkoporov, A. N., Field, D., Draper, L. A., Stanton, C., Hill, C., and Ross, R. P. (2020) Diverse bacteriocins produced by strains from the human milk microbiota, Front. Microbiol., 11, 1-19, https://doi.org/10.3389/fmicb.2020.00788.

    Article  Google Scholar 

  62. Brede, D. A., Faye, T., Johnsborg, O., Odegård, I., Nes, I. F., and Holo, H. (2004) Molecular and genetic characterization of propionicin F, a bacteriocin from Propionibacterium freudenreichii, Appl. Environ. Microbiol., 70, 7303-7310, https://doi.org/10.1128/AEM.70.12.7303-7310.2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Holo, H., Nilssen, O., and Nes, I. F. (1991) Lactococcin A, a new bacteriocin from Lactococcus lactis subsp. cremoris: isolation and characterization of the protein and its gene, J. Bacteriol., 173, 3879-3887, https://doi.org/10.1128/jb.173.12.3879-3887.1991.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Martínez, B., Suárez, J. E., and Rodríguez, A. (1996) Lactococcin 972: a homodimeric lactococcal bacteriocin whose primary target is not the plasma membrane, Microbiology (Reading), 142, 2393-2398, https://doi.org/10.1099/00221287-142-9-2393.

    Article  Google Scholar 

  65. Faye, T., Langsrud, T., Nes, I. F., and Holo, H. (2000) Biochemical and genetic characterization of propionicin T1, a new bacteriocin from Propionibacterium thoenii, Appl. Environ. Microbiol., 66, 4230-4236, https://doi.org/10.1128/aem.66.10.4230-4236.2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Gong, W., Wang, J., Chen, Z., Xia, B., and Lu, G. (2011) Solution structure of LCI, a novel antimicrobial peptide from Bacillus subtilis, Biochemistry, 50, 3621-3627, https://doi.org/10.1021/bi200123w.

    Article  CAS  PubMed  Google Scholar 

  67. Garnier, T., and Cole, S. T. (1988) Complete nucleotide sequence and genetic organization of the bacteriocinogenic plasmid, pIP404, from Clostridium perfringens, Plasmid, 19, 134-150, https://doi.org/10.1016/0147-619x(88)90052-2.

    Article  CAS  PubMed  Google Scholar 

  68. Tymoszewska, A., Walczak, P., and Aleksandrzak-Piekarczyk, T. (2020) BacSJ – another bacteriocin with distinct spectrum of activity that targets Man-PTS, Int. J. Mol. Sci., 21, 1-18, https://doi.org/10.3390/ijms21217860.

    Article  CAS  Google Scholar 

  69. Tymoszewska, A., Diep, D. B., and Aleksandrzak-Piekarczyk, T. (2018) The extracellular loop of Man-PTS subunit IID is responsible for the sensitivity of Lactococcus garvieae to garvicins A, B and C, Sci. Rep., 8, 1-15, https://doi.org/10.1038/s41598-018-34087-2.

    Article  CAS  Google Scholar 

  70. Mohamed, S. E., and Tahoun, M. K. (2015) The expression of propionicin PLG-1 gene (plg-1) by lactic starters, J. Dairy Res., 82, 209-214, https://doi.org/10.1017/S0022029915000011.

    Article  CAS  PubMed  Google Scholar 

  71. Worobo, R. W., Henkel, T., Sailer, M., Roy, K. L., Vederas, J. C., and Stiles, M. E. (1994) Characteristics and genetic determinant of a hydrophobic peptide bacteriocin, carnobacteriocin A, produced by Carnobacterium piscicola LV17A, Microbiology (Reading), 140, 517-526, https://doi.org/10.1099/00221287-140-3-517.

    Article  CAS  Google Scholar 

  72. Sawa, N., Koga, S., Okamura, K., Ishibashi, N., Zendo, T., and Sonomoto, K. (2013) Identification and characterization of novel multiple bacteriocins produced by Lactobacillus sakei D98, J. Appl. Microbiol., 115, 61-69, https://doi.org/10.1111/jam.12226.

    Article  CAS  PubMed  Google Scholar 

  73. Ehrmann, M. A., Remiger, A., Eijsink, V. G. H., and Vogel, R. F. (2000) A gene cluster encoding plantaricin 1.25β and other bacteriocin-like peptides in Lactobacillus plantarum TMW1.25, Biochim. Biophys. Acta, 1490, 355-361, https://doi.org/10.1016/S0167-4781(00)00003-8.

    Article  CAS  PubMed  Google Scholar 

  74. O’Shea, E. F., O’Connor, P. M., O’Sullivan, O., Cotter, P. D., Ross, P., and Hill, C. (2013) Bactofencin A, a new type of cationic bacteriocin with unusual immunity, mBio, 4, 1-9, https://doi.org/10.1128/mBio.00498-13.

    Article  CAS  Google Scholar 

  75. Jiang, Y. H., Xin, W. G., Yang, L. Y., Yinp, J. P., Zhao, Z. S., Lin, L. B., Li, X. Z., and Zhang, Q. L. (2022) A novel bacteriocin against Staphylococcus aureus from Lactobacillus paracasei isolated from Yunnan traditional fermented yogurt: purification, antibacterial characterization, and antibiofilm activity, J. Dairy Sci., 105, 2094-2107, https://doi.org/10.3168/jds.2021-21126.

    Article  CAS  PubMed  Google Scholar 

  76. Yoneyama, F., Imura, Y., Ohno, K., Zendo, T., Nakayama, J., Matsuzaki, K., and Sonomoto, K. (2009) Peptide-lipid huge toroidal pore, a new antimicrobial mechanism mediated by a lactococcal bacteriocin, lacticin Q, Antimicrob. Agents Chemother., 53, 3211-3217, https://doi.org/10.1128/AAC.00209-09.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Jeckelmann, J. M., and Erni, B. (2020) The mannose phosphotransferase system (Man-PTS) – Mannose transporter and receptor for bacteriocins and bacteriophages, Biochim. Biophys. Acta Biomembr., 862, 1-18, https://doi.org/10.1016/j.bbamem.2020.183412.

    Article  CAS  Google Scholar 

  78. Diep, D. B., Skaugen, M., Salehian, Z., Holo, H., and Nes, I. F. (2007) Common mechanisms of target cell recognition and immunity for class II bacteriocins, Proc. Natl. Acad. Sci. USA, 104, 2384-2389, https://doi.org/10.1073/pnas.0608775104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Kjos, M., Salehian, Z., Nes, I. F., and Diep, D. B. (2010) An extracellular loop of the mannose phosphotransferase system component IIC is responsible for specific targeting by class IIa bacteriocins, J. Bacteriol., 192, 5906-5913, https://doi.org/10.1128/JB.00777-10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Zhu, L., Zheng, J., Wang, C., and Wang, J. (2022) Structural basis of pore formation in the mannose phosphotransferase system by pediocin PA-1, Appl. Environ. Microbiol., 88, 1-13, https://doi.org/10.1128/AEM.01992-21.

    Article  Google Scholar 

  81. Kjos, M., Oppegård, C., Diep, D. B., Nes, I. F., Veening, J. W., Nissen-Meyer, J., and Kristensen, T. (2014) Sensitivity to the two-peptide bacteriocin lactococcin G is dependent on UppP, an enzyme involved in cell-wall synthesis, Mol. Microbiol., 92, 1177-1187, https://doi.org/10.1111/mmi.12632.

    Article  CAS  PubMed  Google Scholar 

  82. Oppegård, C., Kjos, M., Veening, J. W., Nissen-Meyer, J., and Kristensen, T. (2016) A putative amino acid transporter determines sensitivity to the two-peptide bacteriocin plantaricin JK, Microbiologyopen, 5, 700-708, https://doi.org/10.1002/mbo3.363.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Ekblad, B., Nissen-Meyer, J., and Kristensen, T. (2017) Whole-genome sequencing of mutants with increased resistance against the two-peptide bacteriocin plantaricin JK reveals a putative receptor and potential docking site, PLoS One, 12, 1-11, https://doi.org/10.1371/journal.pone.0185279.

    Article  Google Scholar 

  84. Heeney, D. D., Yarov-Yarovoy, V., and Marco, M. L. (2019) Sensitivity to the two peptide bacteriocin plantaricin EF is dependent on CorC, a membrane-bound, magnesium/cobalt efflux protein, Microbiologyopen, 8, 1-16, https://doi.org/10.1002/mbo3.827.

    Article  CAS  Google Scholar 

  85. Uzelac, G., Kojic, M., Lozo, J., Aleksandrzak-Piekarczyk, T., Gabrielsen, C., Kristensen, T., Nes, I. F., Diep, D. B., and Topisirovic, L. (2013) A Zn-dependent metallopeptidase is responsible for sensitivity to LsbB, a class II leaderless bacteriocin of Lactococcus lactis subsp. lactis BGMN1-5, J. Bacteriol., 195, 5614-5621, https://doi.org/10.1128/JB.00859-13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Miljkovic, M., Uzelac, G., Mirkovic, N., Devescovi, G., Diep, D. B., Venturi, V., and Kojic, M. (2016) LsbB bacteriocin interacts with the third transmembrane domain of the YvjB receptor, Appl. Environ. Microbiol., 82, 5364-5374, https://doi.org/10.1128/AEM.01293-16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Martínez, B., Guez, A. R., and Suárez, J. E. (2000) Lactococcin 972, a bacteriocin that inhibits septum formation in lactococci, Microbioogy (Reading), 146, 949-955, https://doi.org/10.1099/00221287-146-4-949.

    Article  Google Scholar 

  88. Martínez, B., Böttiger, T., Schneider, T., Rodríguez, A., Sahl, H. G., and Wiedemann, I. (2008) Specific interaction of the unmodified bacteriocin lactococcin 972 with the cell wall precursor lipid II, Appl. Environ. Microbiol., 74, 4666-4670, https://doi.org/10.1128/AEM.00092-08.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Soltani, S., Hammami, R., Cotter, P. D., Rebuffat, S., Said, L. B., Gaudreau, H., Bédard, F., Biron, E., Drider, D., and Fliss, I. (2021) Bacteriocins as a new generation of antimicrobials: toxicity aspects and regulations, FEMS Microbiol. Rev., 45, 1-24, https://doi.org/10.1093/femsre/fuaa039.

    Article  CAS  Google Scholar 

  90. Settanni, L., and Corsetti, A. (2008) Application of bacteriocins in vegetable food biopreservation, Int. J. Food Microbiol., 121, 123-138, https://doi.org/10.1016/j.ijfoodmicro.2007.09.001.

    Article  CAS  PubMed  Google Scholar 

  91. Santos, C. P. J., Sousa, R. C. S., Otoni, C. G., Moraes, A. R. F., Souza, V. G. L., Medeiros, E. A. A., Espitia, P. J. P., Pires, A. C. S., Coimbra, J. S. R., and Soares, N. F. F. (2018) Nisin and other antimicrobial peptides: Production, mechanisms of action, and application in active food packaging, Innov. Food Sci. Emerg. Technol., 48, 179-194, https://doi.org/10.1016/j.ifset.2018.06.008.

    Article  CAS  Google Scholar 

  92. Aymerich, T., Jofré, A., and Bover-Cid, S. (2022) Enterocin A-based antimicrobial film exerted strong antilisterial activity in sliced dry-cured ham immediately and after 6 months at 8 °C, Food Microbiol., 105, 104005, https://doi.org/10.1016/j.fm.2022.104005.

    Article  CAS  PubMed  Google Scholar 

  93. Dabour, N., Zihler, A., Kheadr, E., Lacroix, C., and Fliss, I. (2009) In vivo study on the effectiveness of pediocin PA-1 and Pediococcus acidilactici UL5 at inhibiting Listeria monocytogenes, Int. J. Food Microbiol., 133, 225-233, https://doi.org/10.1016/j.ijfoodmicro.2009.05.005.

    Article  CAS  PubMed  Google Scholar 

  94. Ermolenko, E. L., Desheva, Y. A., Kolobov, M. P., Kotyleva, M. P., Sychev, I. A., and Suvorov, A. N. (2019) Anti-influenza activity of enterocin B in vitro and protective effect of bacteriocinogenic Enterococcal probiotic strain on influenza infection in mouse model, Probiotics Antimicrob. Proteins, 11, 705-712, https://doi.org/10.1007/s12602-018-9457-0.

    Article  CAS  PubMed  Google Scholar 

  95. Okuda, K., Zendo, T., Sugimoto, S., Iwase, T., Tajima, A., Yamada, S., Sonomoto, K., and Mizunoe, Y. (2013) Effects of bacteriocins on methicillin-resistant Staphylococcus aureus biofilm, Antimicrob. Agents Chemother., 57, 5572-5579, https://doi.org/10.1128/AAC.00888-13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Kranjec, C., Ovchinnikov, K. V., Grønseth, T., Ebineshan, K., Srikantam, A., and Diep, D. B. (2020) A bacteriocin-based antimicrobial formulation to effectively disrupt the cell viability of methicillin-resistant Staphylococcus aureus (MRSA) biofilms, NPJ Biofilms Microbiomes, 6, 1-13, https://doi.org/10.1038/s41522-020-00166-4.

    Article  CAS  Google Scholar 

  97. Lin, X., Xu, J., Shi, Z., Xu, Y., Fu, T., Zhang, L., and He, F. (2021) Evaluation of the antibacterial effects and mechanism of plantaricin 149 from Lactobacillus plantarum NRIC 149 on the peri-implantitis pathogens, Sci. Rep., 11, 1-8, https://doi.org/10.1038/s41598-021-00497-y.

    Article  CAS  Google Scholar 

  98. Caly, D., Chevalier, M., Flahaut, C., Cudennec, B., Al Atya, A. K., Chataigné, G., D’Inca, R., Auclair, E., and Drider, D. (2017) The safe enterocin DD14 is a leaderless two-peptide bacteriocin with anti-Clostridium perfringens activity, Int. J. Antimicrob. Agents, 49, 282-289, https://doi.org/10.1016/j.ijantimicag.2016.11.016.

    Article  CAS  PubMed  Google Scholar 

  99. Buss, G. P., and Wilson, C. (2021) Exploring the cytotoxic mechanisms of pediocin PA-1 towards HeLa and HT29 cells by comparison to known bacteriocins: microcin E492, enterocin heterodimer and divercin V41, PLoS One, 16, 1-13, https://doi.org/10.1371/journal.pone.0251951.

    Article  CAS  Google Scholar 

  100. Baindara, P., Gautam, A., Raghava, G. P. S., and Korpole, S. (2017) Anticancer properties of a defensin like class IId bacteriocin laterosporulin 10, Sci. Rep., 7, 1-9, https://doi.org/10.1038/srep46541.

    Article  CAS  Google Scholar 

  101. Ankaiah, D., Palanichamy, E., Antonyraj, C. B., Ayyanna, R., Perumal, V., Ahamed, S. I. B., and Arul, V. (2018) Cloning, overexpression, purification of bacteriocin enterocin-B and structural analysis, interaction determination of enterocin-A, B against pathogenic bacteria and human cancer cells, Int. J. Biol. Macromol., 116, 502-512, https://doi.org/10.1016/j.ijbiomac.2018.05.002.

    Article  CAS  PubMed  Google Scholar 

  102. Teiar, R., Pérez-Ramos, A., Zgheib, H., Cudennec, B., Belguesmia, Y., and Drider, D. (2022) Anti-adhesion and anti-inflammatory potential of the leaderless class IIb bacteriocin enterocin DD14, Probiotics Antimicrob. Proteins, 14, 613-619, https://doi.org/10.1007/s12602-022-09954-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Śmiałek, J., Bzowska, M., Hinz, A., Mężyk-Kopeć, R., Sołtys, K., and Mak, P. (2022) Bacteriocin BacSp222 and its succinylated forms exhibit proinflammatory activities toward innate immune cells, J. Inflamm. Res., 15, 4601-4621, https://doi.org/10.2147/JIR.S362066.

    Article  PubMed  PubMed Central  Google Scholar 

  104. Hanny, E. L. L., Mustopa, A. Z., Budiarti, S., Darusman, H. S., Ningrum, R. A., and Fatimah (2019) Efficacy, toxicity study and antioxidant properties of plantaricin E and F recombinants against enteropathogenic Escherichia coli K1.1 (EPEC K1.1), Mol. Biol. Rep., 46, 6501-6512, https://doi.org/10.1007/s11033-019-05096-9.

    Article  CAS  PubMed  Google Scholar 

  105. Halliwell, S., Warn, P., Sattar, A., Derrik, J. P., and Upron, M. (2017) A single dose of epidermicin NI01 is sufficient to eradicate MRSA from the nares of cotton rats, J. Antimicrob. Chemother., 72, 778-781, https://doi.org/10.1093/jac/dkw457.

    Article  CAS  PubMed  Google Scholar 

  106. Wosinska, L., Walsh, C. J., O’Connor, P. M., Lawton, E. M., Cotter, P. D., Guinane, C. M., and O’Sullivan, O. (2022) In vitro and in silico based approaches to identify potential novel bacteriocins from the athlete gut microbiome of an elite athlete cohort, Microorganisms, 10, 1-17, https://doi.org/10.3390/microorganisms10040701.

    Article  CAS  Google Scholar 

  107. Coyne, M. J., Béchon, N., Matano, L. M., McEneany, V. L., Chatzidaki-Livanis, M., and Comstock, L. E. (2019) A family of anti-Bacteroidales peptide toxins wide-spread in the human gut microbiota, Nat. Commun., 10, 1-14, https://doi.org/10.1038/s41467-019-11494-1.

    Article  CAS  Google Scholar 

  108. Umu, Ö. C., Bäuerl, C., Oostindjer, M., Pope, P. B., Hernández, P. E., Pérez-Martínez, G., and Diep, D. B. (2016) The potential of class II bacteriocins to modify gut microbiota to improve host health, PLoS One, 11, 1-22, https://doi.org/10.1371/journal.pone.0164036.

    Article  CAS  Google Scholar 

  109. Strompfová, V., Kubašová, I., and Ščerbová, J. (2019) Oral administration of bacteriocin-producing and non-producing strains of Enterococcus faecium in dogs, Appl. Microbiol. Biotechnol., 103, 4953-4965, https://doi.org/10.1007/s00253-019-09847-3.

    Article  CAS  PubMed  Google Scholar 

  110. Soltani, S., Zirah, S., and Rebuffat, S. (2022) Gastrointestinal stability and cytotoxicity of bacteriocins from Gram-positive and Gram-negative bacteria: a comparative in vitro study, Front. Microbiol., 12, 1-13, https://doi.org/10.3389/fmicb.2021.780355.

    Article  Google Scholar 

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Funding

This work was financially supported by the Russian Science Foundation (grant no. 22-14-00380).

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  1. M. M. Shemyakin and Yu. A. Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997, Moscow, Russia

    Daria V. Antoshina, Sergey V. Balandin & Tatiana V. Ovchinnikova

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D. V. Antoshina and S. V. Balandin collected and analyzed literature data, and prepared the first version of the review. T. V. Ovchinnikova formulated the concept, provided coordination and funding for the work, analyzed collected literature data, edited, and prepared the manuscript for publication. The final version of the review was confirmed by all authors.

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Correspondence to Tatiana V. Ovchinnikova.

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The authors declare no conflict of interest in financial or any other sphere. This review does not contain any studies with human participants or animals performed by any of the authors.

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Antoshina, D.V., Balandin, S.V. & Ovchinnikova, T.V. Structural Features, Mechanisms of Action, and Prospects for Practical Application of Class II Bacteriocins. Biochemistry Moscow 87, 1387–1403 (2022). https://doi.org/10.1134/S0006297922110165

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