Prevalence of the phenomenon of production of peptide factors of antagonism among coagulase-negative staphylococci

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Abstract

Coagulase-negative staphylococci (CNS) isolated from clinical hospital environmental objects were screened for their ability to produce antibacterial compounds. It was shown that CNS strains with pronounced antagonistic activity were detected with a frequency of about 1.4%. The antibacterial activity of individual CNS strains was due to the release of low-molecular peptide compounds into the environment. The molecular weight of three isolated peptides was 2985, 2998, and 3004 Da. The peptide secreted by Staphylococcus hominis bacteria contains an unusual amino acid, methyllanthionine, and can be classified as a class I bacteriocin, a lantibiotic. The antibacterial activity of the isolated peptides was demonstrated against gram-positive bacteria of various genera that are phylogenetically unrelated to the producers.

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About the authors

T. V. Polyudova

Institute of Ecology and Genetics of Microorganisms, Ural Branch of the Russian Academy of Sciences; Perm State Agrarian and Technological University

Author for correspondence.
Email: polyudova@iegm.ru
Russian Federation, Perm, 614581; Perm, 614990

L. M. Lemkina

Institute of Ecology and Genetics of Microorganisms, Ural Branch of the Russian Academy of Sciences

Email: polyudova@iegm.ru
Russian Federation, Perm, 614581

M. V. Antipyeva

Institute of Ecology and Genetics of Microorganisms, Ural Branch of the Russian Academy of Sciences; Perm State Agrarian and Technological University

Email: polyudova@iegm.ru
Russian Federation, Perm, 614581; Perm, 614990

A. L. Yesaev

Institute of Ecology and Genetics of Microorganisms, Ural Branch of the Russian Academy of Sciences

Email: polyudova@iegm.ru
Russian Federation, Perm, 614581

V. P. Korobov

Institute of Ecology and Genetics of Microorganisms, Ural Branch of the Russian Academy of Sciences

Email: polyudova@iegm.ru
Russian Federation, Perm, 614581

References

  1. Дерябин Д. Г. Стафилококки: экология и патогенность. Екатеринбург: УрО РАН, 2000. 240 с.
  2. Коробов В. П., Лемкина Л. М., Полюдова Т. В., Акименко В. К. Выделение и характеристика нового низкомолекулярного антибактериального пептида семейства лантибиотиков // Микробиология. 2010. Т. 79. С. 228‒238.
  3. Korobov V. P., Lemkina L. M., Polyudova T. V., Akimenko V. K. Isolation and characterization of new low-molecular antibacterial peptide of the lantibiotics family // Microbiology (Moscow). 2010. V. 79. P. 206‒215.
  4. Пипия С. О., Терехов С. С., Мокрушина Ю. А., Кнорре В. Д., Смирнов И. В., Габибов А. Г. Использование расширенного химического пространства лантибиотиков для создания искусственного биоразнообразия генетически кодируемых антибиотиков // Биохимия. 2020. Т. 85. С. 1550‒1568.
  5. Pipiya S. O., Terekhov S. S., Mokrushina Y. A., Knorre V. D., Smirnov I. V., Gabibov A. G. Engineering artificial biodiversity of lantibiotics to expand chemical space of DNA-encoded antibiotics // Biochemistry (Moscow). 2020. V. 85. P. 1319‒1334.
  6. Патент РФ. 2006. № 2274654.
  7. Полюдова Т. В., Лемкина Л. М., Лихацкая Г. Н., Коробов В. П. Оптимизация условий получения и моделирование 3D-cтруктуры нового антибактериального пептида семейства лантибиотиков // Прикл. биохимия и микробиология. 2017. Т. 53. С. 47‒54.
  8. Polyudova T. V., Lemkina L. M., Korobov V. P., Likhatskaya G. N. Optimization of production conditions and 3D-structure of novel antibacterial peptide of lantibiotic family // Appl. Biochem. Microbiol. 2017. V. 53. P. 40‒46.
  9. Патент РФ. 2014. № 2528055.
  10. Atlas R. M. Handbook of Microbiological Media. CRC Press, 1993. 1079 р.
  11. Bastos M., Ceotto H., Coelho M. L.V., Nascimento J. S. Staphylococcal antimicrobial peptides: relevant properties and potential biotechnological applications // Curr. Pharm. Biotechnol. 2009. V. 10. P. 38‒61.
  12. Bastos M., de Farias M.., Fagundes C., Coelho M. Staphylococcins: an update on antimicrobial peptides produced by staphylococci and their diverse potential applications // Appl. Microbiol. Biotechnol. 2020. V. 104. P. 10339‒10368.
  13. Bierbaum G., Sahl H. Lantibiotics: mode of action and bioenginering // Curr. Pharm. Biotechnol. 2009. V. 10. P. 2‒18.
  14. Bierbaum G., Götz F., Peschel A., Kupke T., van de Kamp M., Sahl H. G. The biosynthesis of the lantibiotics epidermin, gallidermin, Pep5 and epilancin K7 // Antonie van Leeuwenhoek. 1996. V. 69. P. 119‒127.
  15. Braem G., Stijlemans B., Van Haken W., de Vliegher S., de Vuyst L., Leroy F. Antibacterial activities of coagulase-negative staphylococci from bovine teat apex skin and their inhibitory effect on mastitis-related pathogens // J. Appl. Microbiol. 2014. V. 116. P. 1084 –1093.
  16. Cotter P., Ross R., Hill C. Bacteriocins ‒ a viable alternative to antibiotics? // Nat. Rev. Microbiol. 2013. P. 95‒105.
  17. Fernández-Fernández R., Lozano C., Eguizábal P., Ruiz-Ripa L., Martínez-Álvarez S., Abdullahi I. N., Zarazaga M., Torres C. Bacteriocin-like inhibitory substances in Staphylococc i of different origins and species with activity against relevant pathogens // Front. Microbiol. 2022. V. 13. Art. 870510.
  18. Freitas F. S., Vidigal P. M.P., Siqueira T. P., de Barros M., Totola M. R. The draft genome of Staphylococcus warneri TRPF4, a bacteriocin producer with potent activity against the causative agent of Legionnaires’ Disease // 3 Biotech. 2020. V. 10. Art. 232.
  19. Gallo R. L., Nakatsuji T. Microbial symbiosis with the innate immune defense system of the skin // J. Invest Dermatol. 2011. V. 131. P. 1974‒1980.
  20. Heilbronner S., Krismer B., Brötz-Oesterhelt H., Peschel A. The microbiome-shaping roles of bacteriocins // Nat. Rev. Microbiol. 2021. V. 19. P. 726‒739.
  21. Joglekar P., Conlan S., Lee-Lin S.Q., Deming C., Kashaf S. S., Kong H. H., Segre J. A. Integrated genomic and functional analyses of human skin-associated Staphylococcus reveal extensive inter- and intra-species diversity // Proc. Natl. Acad. Sci. USA. 2023. V. 120. Art. e2310585120.
  22. Kassem M., Saafan A., Bayomy F., El-Gendy A. Exploring clinically isolated Staphylococcus sp. bacteriocins revealed the production of amonabactin, micrococcin, and α-circulocin // Iranian J. Microbiol . 2021. V. 13. P. 212‒224.
  23. Kim P., Sohng J., Sung C., Joo H., Kim E., Yamaguchi T., Park D., Kim B. Characterization and structure identification of an antimicrobial peptide, hominicin, produced by Staphylococcus hominis MBBL 2 –9 // Biochem. Biophys. Res. Commun. 2010. V. 399. P. 133‒138.
  24. Minamikawa M., Kawai Y., Inoue N., Yamazaki K. Purification and characterization of Warnericin RB4, anti- Alicyclobacillus bacteriocin, produced by Staphylococcus warneri RB4 // Curr. Microbiol. 2005. V. 51. P. 22‒26.
  25. Nascimento J., Fagundes P., Brito M., Santos K., Bastos M. Production of bacteriocins by coagulase-negative staphylococci involved in bovine mastitis // Veter. Microbiol. 2005. V. 106. P. 61 –71.
  26. Onyango L. A., Alreshidi M. M. Adaptive metabolism in staphylococci: survival and persistence in environmental and clinical settings // J. Pathog. 2018. V. 2018. Art. 1092632.
  27. Patil G., Agarwala P., Das P., Pathak S. Rise in the pathogenic status of coagulase-negative staphylococci causing bloodstream infection // Cureus. 2024. V. 16. Art. e57250.
  28. Petersen J., Boysen A., Fogh L., Tabermann K., Kofoed T., King A., Schrotz-King P., Hansen M. C. Identification and characterization of a bioactive lantibiotic produced by Staphylococcus warneri // Biol. Chem. 2009. V. 390. P. 437‒444.
  29. Pinheiro-Hubinger L., Moraes Riboli D., Abraao L., Pereira Franchi E., Ribeiro de Souza da Cunha M. Coagulase-negative staphylococci clones are widely distributed in the hospital and community // Pathogens. 2021. V. 10. Art. 792.
  30. Rahmdel S., Shekarforoush S., Hosseinzadeh S., Torriani S., Gatto V. Antimicrobial spectrum activity of bacteriocinogenic Staphylococcus strains isolated from goat and sheep milk // J. Dairy Sci. 2019. V. 102. P. 2928‒2940.
  31. Sashihara T., Kimura H., Higuchi T., Adachi A., Matsusaki H., Sonomoto K., Ishizaki A. A novel lantibiotic, nukacin ISK-1, of Staphylococcus warneri ISK-1: cloning of the structural gene and identification of the structure // Biosci. Biotechnol. Biochem. 2000. V. 64. P. 2420‒2428.
  32. Severn M., Williams M., Shahbandi A., Bunch Z., Lyon L., Nguyen A., Zaramela L., Todd D., Zengler K., Cech N., Gallo R., Horswill A. The ubiquitous human skin commensal Staphylococcus hominis protects against opportunistic pathogens // mBio. 2022. V. 13. P. 930‒952.
  33. Stein T., Borchert S., Conrad B., Feesche J., Hofemeister B., Hofemeister J., Entian K. Two different lantibiotic-like peptides originate from the ericin gene cluster of Bacillus subtilis A1/3 // J. Bacteriol. 2002. V. 184. P. 1703‒1711.
  34. Suda S., Hill C., Cotter P. D., Ross R. P. Investigating the importance of charged residues in lantibiotics // Bioeng. Bugs. 2010. V. 1. P. 345‒351.
  35. Wilaipun P., Zendo T., Okuda K., Nakayama J., Sonomoto K . Identification of the nukacin KQU-131, a new type-A(II) lantibiotic produced by Staphylococcus hominis KQU-131 isolated from Thai fermented fish product (Pla-ra) // Biosci. Biotechnol. Biochem. 2008. V. 72. P. 2232‒2235.
  36. Wojtyczka R., Orlewska K., Kępa M., Idzik D., Dziedzic A., Mularz T., Krawczyk M., Miklasińska M., Wąsik T. Biofilm formation and antimicrobial susceptibility of Staphylococcus epidermidis strains from a hospital environment // Int. J. Environ. Res. Publ. Health. 2014. V. 11. P. 4619‒4633.
  37. Wolden R., Ovchinnikov K. V., Venter H. J., Oftedal T. F., Diep D. B., Cavanagh J. P. The novel bacteriocin romsacin from Staphylococcus haemolyticus inhibits Gram-positive WHO priority pathogens // Microbiol. Spectrum. 2023. V. 11. P. 869‒892.

Supplementary files

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2. Fig. 1. Detection of ABA in cell-free culture fluids of the KNS by the agarose diffusion method using the S. cohnii VKM-3165 test bacteria.

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3. Fig. 2. Growth curves (1) and antibacterial activities of culture fluids (2) of S. haemolyticus 117 (a), S. hominis GISK-284 (b) and S. warneri 1535 (c).

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4. Fig. 3. Mass spectra of purified peptides from culture fluids of S. haemolyticus 117 (a), S. hominis GISK 284 (b) and S. warneri 1535 (c).

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