Skip to main content
SpringerLink
Log in

Antimicrobial Metabolites from Pig Nasal Microbiota

  • Published:
Russian Journal of Bioorganic Chemistry Aims and scope Submit manuscript

Abstract

Objective: Isolation of bacteria and fungi from porcine nasal microbiome and evaluation of antibioticproducing potential among them. Methods: Conventional isolation using Sabouraud and Mueller-Hinton nutrient media was carried out for collected samples. The isolated strains were subjected to antibiotic susceptibility testing and antimicrobial activity screening. Results and Discussion: Taxonomy positions of the 20 isolated strains (18 bacteria, 1 yeast, 1 fungus) were determined by phylogenetic analysis, morphological study and a substrate utilization assay. Pseudomonas aeruginosa SM-11 was found to produce 4 known antibacterial molecules (pyocyanine, pyochelin, pyoluteorin, monorhamnolipid). Production of pyocyanine was induced by cocultivation with test microorganisms. Conclusions: The mammal microbiota might serve as a valuable source of antimicrobialproducing strains, including those of rare taxa. Cocultivation techniques are a promising approach to exploring antimicrobials from silent biosynthetic gene clusters.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.
Fig. 9.
Fig. 10.

Similar content being viewed by others

DATA AVAILABILITY

The data that support the findings of this study are available from the corresponding author upon reasonable request.

REFERENCES

  1. Hutchings, M.I., Truman, A.W., and Wilkinson, B., Curr. Opin. Microbiol., 2019, vol. 51, pp. 72–80. https://doi.org/10.1016/j.mib.2019.10.008

    Article  CAS  PubMed  Google Scholar 

  2. Miethke, M., Pieroni, M., Weber, T., Brönstrup, M., Hammann, P., Halby, L., Arimondo, P.B., Glaser, P., Aigle, B., Bode, H.B., Moreira, R., Li, Y., Luzhetskyy, A., Medema, M. H., Pernodet, J., Stadler, M., Tormo, J.R., Genilloud, O., Truman, A.W., Weissman, K.J., Takano, E., Sabatini, S., Stegmann, E., Brötz-Oesterhelt, H., Wohlleben, W., Seemann, M., Empting, M., Hirsch, A.K.H., Loretz, B., Lehr, C.M., Titz, A., Herrmann, J., Jaeger, T., Alt, S., Hesterkamp, T., Winterhalter, M., Schiefer, A., Pfarr, K., Hoerauf, A., Graz, H., Graz, M., Lindvall, M., Ramurthy, S., Karlén, A., Dongen, M., Petkovic, H., Keller, A., Peyrane, F., Donadio, S., Fraisse, L., Piddock, L.J.V., Gilbert, I.H., Moser, H.E, Müller, R., Nat. Rev. Chem., 2021, vol. 5, pp. 726–749. https://doi.org/10.1038/s41570-021-00313-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Bernal, F.A., Hammann, P., and Kloss F., Curr. Opin. Biotechnol., 2022, vol. 78, Article ID: 102783. https://doi.org/10.1016/j.copbio.2022.102783

  4. Cook, M.A. and Wright, G.D., Sci. Transl. Med., 2022, vol. 14, Article ID: eabo7793. https://doi.org/10.1126/scitranslmed.abo7793

  5. Dai, J., Han, R., Xu, Y., Li, N., Wang, J., and Dan, W., Bioorg. Chem., 2020, vol. 101, Article ID: 103922. https://doi.org/10.1016/j.bioorg.2020.103922

  6. Atanasov, A., Zotchev, S., Dirsch, V., Orhan, I., Banach, M., Rollinger, J., Barreca, D., Weckwerth, W., Bauer, R., Edward, B., Majeed, M., Bishayee, A., Bochkov, V., Bonn, G., Braidy, N., Bucar, F., Cifuentes, A., D’Onofrio, G., Bodkin, M., and Supuran, C., Nat. Rev. Drug Discov., 2021, vol. 20, pp. 200–216. https://doi.org/10.1038/s41573-020-00114-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Newman, D.J. and Cragg, G.M., J. Nat. Prod., 2020, vol. 83, pp. 770–803. https://doi.org/10.1021/acs.jnatprod.9b01285

    Article  CAS  PubMed  Google Scholar 

  8. Baranova, A.A., Alferova, V.A., Korshun, V.A., and Tyurin, A.P., Life, 2023, vol. 13, Article ID: 1073. https://doi.org/10.3390/life13051073

  9. Walesch, S., Birkelbach, J., Jézéquel, G., Haeckl, F.P.J., Hegemann, J.D., Hesterkamp, T., Hirsch, A.K.H., Hammann, P., and Müller, R., EMBO Rep., 2023, vol. 24, Article ID: e56033. https://doi.org/10.15252/embr.202256033

  10. Baranova, A.A., Alferova, V.A., Korshun, V.A., and Tyurin, A.P., Russ. J. Bioorg. Chem., 2020, vol. 46, pp. 903–971. https://doi.org/10.1134/S1068162020060023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Baranova, A.A., Zakalyukina, Y.V., Ovcharenko, A.A., Korshun, V.A., and Tyurin, A.P., Biology, 2022, vol. 11, Article ID: 1676. https://doi.org/10.3390/biology11111676

  12. Abdelaleem, E.R., Samy, M.N., Abdelmohsen, U.R., and Desoukey, S.Y., Lett. Appl. Microbiol., 2022, vol. 74, pp. 8–16. https://doi.org/10.1111/lam.13559

    Article  CAS  PubMed  Google Scholar 

  13. Imai, Y., Meyer, K.J., Iinishi, A., Favre-Godal, Q., Green, R., Manuse, S., Caboni, M., Mori, M., Niles, S., Ghiglieri, M., Honrao, C., Ma, X., Guo, J.J., Makriyannis, A., Linares-Otoya, L., Böhringer, N., Wuisan, Z.G., Kaur, H., Wu, R., Mateus, A., Typas, A., Savitski, M.M., Espinoza, J.L., O’Rourke, A., Nelson, K.E., Hiller, S., Noinaj, N., Schäberle, T.F., D’Onofrio, A., and Lewis, K., Nature, 2019, vol. 576, pp. 459–464. https://doi.org/10.1038/s41586-019-1791-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Wang, L., Ravichandran, V., Yin, Y., Yin, J., and Zhang, Y., Tr. Biotechnol., 2019, vol. 37, pp. 492–504. https://doi.org/10.1016/j.tibtech.2018.10.003

    Article  CAS  Google Scholar 

  15. Donia, M.S. and Fischbach, M.A., Science, 2015, vol. 349, Article ID: 1254766. https://doi.org/10.1126/science.1254766

  16. Mousa, W.K., Athar, B., Merwin, N.J., and Magarvey, N.A., Nat. Prod. Rep., 2017, vol. 34, pp. 1302–1331. https://doi.org/10.1039/C7NP00021A

    Article  CAS  PubMed  Google Scholar 

  17. Chiumento, S., Roblin, C., Kieffer-Jaquinod, S., Tachon, S., Leprètre, C., Basset, C., Aditiyarini, D., Olleik, H., Nicoletti, C., Bornet, O., Iranzo, O., Maresca, M., Hardré, R., Fons, M., Giardina, T., Devillard, E., Guerlesquin, F., Couté, Y., Atta, M., Perrier, J., Lafond, M., and Duarte, V., Sci. Adv., 2019, vol. 5, Article ID: eaaw9969. https://doi.org/10.1126/sciadv.aaw9969

  18. Barber, C.C. and Zhang, W., J. Ind. Microbiol. Biotechnol., 2021, vol. 48, Article ID: kuab010. https://doi.org/10.1093/jimb/kuab010

  19. Lewis, K., Cell, 2020, vol. 181, pp. 29–45. https://doi.org/10.1016/j.cell.2020.02.056

    Article  CAS  PubMed  Google Scholar 

  20. Pirolo, M., Espinosa-Gongora, C., Alberdi, A., Eisenhofer, R., Soverini, M., Eriksen, E.Ø., Pedersen, K.S., and Guardabassi, L., Animal Microbiome, 2023, vol. 5, Article ID: 5. https://doi.org/10.1186/s42523-023-00226-y

  21. Petrelli, S., Buglione, M., Rivieccio, E., Ricca, E., Baccigalupi, L., Scala, G., and Fulgione, D., Animal Microbiome, 2023, vol. 5, Article ID: 14. https://doi.org/10.1186/s42523-023-00235-x

  22. Vasco, K., Guevara, N., Mosquera, J., Zapata, S., and Zhang, L., Animal Microbiome, 2022, vol. 4, Article ID: 65. https://doi.org/10.1186/s42523-022-00218-4

  23. Kauter, A., Epping, L., Semmler, T., Antao, E.-M., Kannapin, D., Stoeckle, S.D., Gehlen, H., Lübke-Becker, A., Günther, S., Wieler, L.H., and Walther, B., Animal Microbiome, 2019, vol. 1, Article ID: 14. https://doi.org/10.1186/s42523-019-0013-3

  24. O’Sullivan, J.N., Rea, M.C., O’Connor, P.M., Hill, C., and Ross, R.P., FEMS Microbiol. Ecol., 2019, vol. 95, Article ID: fiy241. https://doi.org/10.1093/femsec/fiy241

  25. Wertz, P.W. and De Szalay, S., Antibiotics, 2020, vol. 9, Article ID: 159. https://doi.org/10.3390/antibiotics9040159

  26. O’Sullivan, J.N., O’Connor, P.M., Rea, M.C., O’Sullivan, O., Walsh, C.J., Healy, B., Mathur, H., Field, D., Hill, C., and Ross, R.P., J. Bact., 2020, vol. 202, Article ID: e00639-19. https://doi.org/10.1128/JB.00639-19

  27. O’Neill, A.M., Worthing, K.A., Kulkarni, N., Li, F., Nakatsuji, T., McGrosso, D., Mills, R.H., Kalla, G., Cheng, J.Y., Norris, J.M., Pogliano, K., Pogliano, J., Gonzalez, D.J., and Gallo, R.L., eLife, 2021, vol. 10, Article ID: e66793. https://doi.org/10.7554/eLife.66793

  28. Swaney, M.H. and Kalan, L.R., Infect. Immunity, 2021, vol. 89, Article ID: e00695-20. https://doi.org/10.1128/IAI.00695-20

  29. Heilbronner, S., Krismer, B., Brötz-Oesterhelt, H., and Peschel, A., Nat. Rev. Microbiol., 2021, vol. 19, pp. 726–739. https://doi.org/10.1038/s41579-021-00569-w

    Article  CAS  PubMed  Google Scholar 

  30. Terekhov, S.S., Smirnov, I.V., Malakhova, M.V., Samoilov, A.E., Manolov, A.I., Nazarov, A.S., Danilov, D.V., Dubiley, S.A., Osterman, I.A., Rubtsova, M.P., Kostryukova, E.S., Ziganshin, R.H., Kornienko, M.A., Vanyushkina, A.A., Bukato, O.N., Ilina, E.N., Vlasov, V.V., Severinov, K.V., Gabibov, A.G., and Altman, S., Proc. Natl. Acad. Sci. USA, 2018, vol. 115, pp. 9551–9556. https://doi.org/10.1073/pnas.1811250115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Covington, B.C. and Seyedsayamdost, M.R., J. Am. Chem. Soc., 2022, vol. 144, pp. 14997–15001. https://doi.org/10.1021/jacs.2c05790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Egerszegi, I., Rátky, J., Solti, L., and Brüssow, K.-P., Arch. Anim. Breed., 2003, vol. 46, pp. 245–256. https://doi.org/10.5194/aab-46-245-2003

    Article  Google Scholar 

  33. Breed Cards: Mangalitsa (Swallow-Belly Mangalitsa) Pig. https://www.pig333.com/articles/breed-cards-mangalitsa-swallow-belly-mangalitsa-pig_15977/

  34. Alhede, M., Qvortrup, K., Liebrechts, R., Høiby, N., Givskov, M., and Bjarnsholt, T., FEMS Immunol. Med. Microbiol., 2012, vol. 65, pp. 335–342. https://doi.org/10.1111/j.1574-695X.2012.00956.x

    Article  CAS  PubMed  Google Scholar 

  35. Tihlaříková, E., Neděla, V., and Đorđević, B., Sci. Rep., 2019, vol. 9, Article ID: 2300. https://doi.org/10.1038/s41598-019-38835-w

  36. Muscariello, L., Rosso, F., Marino, G., Giordano, A., Barbarisi, M., Cafiero, G., and Barbarisi, A., J. Cell. Physiol., 2005, vol. 205, pp. 328–334. https://doi.org/10.1002/jcp.20444

    Article  CAS  PubMed  Google Scholar 

  37. Bergmans, L., Moisiadis, P., Van Meerbeek, B., Quirynen, M., and Lambrechts, P., Int. Endodont. J., 2005, vol. 38, pp. 775–788. https://doi.org/10.1111/j.1365-2591.2005.00999.x

    Article  CAS  Google Scholar 

  38. Grund, E. and Kroppenstedt, R.M., Int. J. Syst. Bacteriol., 1990, vol. 40, pp. 5–11. https://doi.org/10.1099/00207713-40-1-5

    Article  Google Scholar 

  39. Wei, Q. and Ma, L., Int. J. Mol. Sci., 2013, vol. 14, pp. 20983–21005. https://doi.org/10.3390/ijms141020983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Brandel, J., Humbert, N., Elhabiri, M., Schalk, I.J., Mislin, G.L.A., and Albrecht-Gary, A.-M., Dalton Trans., 2012, vol. 41, pp. 2820–2834. https://doi.org/10.1039/c1dt11804h

    Article  CAS  PubMed  Google Scholar 

  41. Abdelaziz, A.A., Kamer, A.M.A., Al-Monofy, K.B., and Al-Madboly, L.A., Microb. Cell Fact., 2022, vol. 21, Article ID: 262. https://doi.org/10.1186/s12934-022-01988-x

  42. Brodhagen, M., Henkels, M.D., and Loper, J.E., Appl. Environment. Microbiol., 2004, vol. 70, pp. 1758–1766. https://doi.org/10.1128/AEM.70.3.1758-1766.2004

    Article  CAS  Google Scholar 

  43. Esposito, R., Speciale, I., De Castro, C., D’Errico, G., and Russo Krauss, I., Int. J. Mol. Sci., 2023, vol. 24, Article ID: 5395. https://doi.org/10.3390/ijms24065395

  44. Gogineni, V., Chen, X., Hanna, G., Mayasari, D., and Hamann, M.T., J. Antibiot., 2020, vol. 73, pp. 490–503. https://doi.org/10.1038/s41429-020-0321-6

    Article  CAS  Google Scholar 

  45. Masson, F. and Lemaitre, B., Microbiol. Mol. Biol. Rev., 2020, vol. 84, Article ID: e00089-20. https://doi.org/10.1128/MMBR.00089-20

  46. Olofsson, T.C., Butler, È., Markowicz, P., Lindholm, C., Larsson, L., and Vásquez, A., Int. Wound J., 2016, vol. 13, pp. 668–679. https://doi.org/10.1111/iwj.12345

    Article  PubMed  Google Scholar 

  47. Varijakzhan, D., Loh, J.-Y., Yap, W.-S., Yusoff, K., Seboussi, R., Lim, S.-H.E., Lai, K.-S., and Chong, C.-M., Marine Drugs, 2021, vol. 19, Article ID: 246. https://doi.org/10.3390/md19050246

  48. Abd-Elgawad, M.M.M., Life, 2022, vol. 12, Article ID: 1360. https://doi.org/10.3390/life12091360

  49. Bassols, A., Costa, C., Eckersall, P.D., Osada, J., Sabrià, J., and Tibau, J., Proteomics Clin. Appl., 2014, vol. 8, pp. 715–731. https://doi.org/10.1002/prca.201300099

    Article  CAS  PubMed  Google Scholar 

  50. Heinritz, S.N., Mosenthin, R., and Weiss, E., Nutrit. Res. Rev., 2013, vol. 26, pp. 191–209. https://doi.org/10.1017/S0954422413000152

    Article  Google Scholar 

  51. Espinosa-Gongora, C., Larsen, N., Schønning, K., Fredholm, M., and Guardabassi, L., PLoS One, 2016, vol. 11, Article ID: e0160331. https://doi.org/10.1371/journal.pone.0160331

  52. Chlebicz, A. and Śliżewska, K., Int. J. Environment. Res. Publ. Health, 2018, vol. 15, Article ID: 863. https://doi.org/10.3390/ijerph15050863

  53. Meurens, F., Summerfield, A., Nauwynck, H., Saif, L., and Gerdts, V., Tr. Microbiol., 2012, vol. 20, pp. 50–57. https://doi.org/10.1016/j.tim.2011.11.002

    Article  CAS  Google Scholar 

  54. Gaskins, H.R., Swine Nutrition, Eds. Lewis, A.J. and Southern, L.L., CRC Press, 2000, pp. 585–609. https://doi.org/10.1201/9781420041842

  55. Crespo-Piazuelo, D., Estellé, J., Revilla, M., CriadoMesas, L., Ramayo-Caldas, Y., Óvilo, C., Fernández, A.I., Ballester, M., and Folch, J.M., Sci. Rep., 2018, vol. 8, Article ID: 12727. https://doi.org/10.1038/s41598-018-30932-6

  56. Isaacson, R. and Kim, H.B., Animal Health Res. Rev., 2012, vol. 13, pp. 100–109. https://doi.org/10.1017/S1466252312000084

    Article  Google Scholar 

  57. Correa-Fiz, F., Gonçalves dos Santos, J.M., Illas, F., and Aragon, V., Sci. Rep., 2019, vol. 9, Article ID: 6545. https://doi.org/10.1038/s41598-019-43022-y

  58. Correa-Fiz, F., Fraile, L., and Aragon, V., BMC Genomics, 2016, vol. 17, Article ID: 404. https://doi.org/10.1186/s12864-016-2700-8

  59. Obregon-Gutierrez, P., Aragon, V., and Correa-Fiz, F., Pathogens, 2021, vol. 10, Article ID: 697. https://doi.org/10.3390/pathogens10060697

  60. Correa-Fiz, F., Neila-Ibáñez, C., López-Soria, S., Napp, S., Martinez, B., Sobrevia, L., Tibble, S., Aragon, V., and Migura-Garcia, L., Sci. Rep., 2020, vol. 10, Article ID: 20354. https://doi.org/10.1038/s41598-020-77313-6

  61. Wang, T., He, Q., Yao, W., Shao, Y., Li, J., and Huang, F., Front. Microbiol., 2019, vol. 10, Article ID: 1083. https://doi.org/10.3389/fmicb.2019.01083

  62. Dai, H., Chen, A., Wang, Y., Lu, B., Wang, Y., Chen, J., Huang, Y., Li, Z., Fang, Y., Xiao, T., Cai, H., Du, Z., Wei, Q., Kan, B., and Wang, D., Int. J. Syst. Evol. Microbiol., 2019, vol. 69, pp. 852–858. https://doi.org/10.1099/ijsem.0.003248

    Article  CAS  PubMed  Google Scholar 

  63. Matias Rodrigues, J.F., Schmidt, T.S.B., Tackmann, J., and Mering, C. von, Bioinformatics, 2017, vol. 33, pp. 3808–3810. https://doi.org/10.1093/bioinformatics/btx517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Wang, F., Gai, Y., Chen, M., and Xiao, X., Int. J. Syst. Evol. Microbiol., 2009, vol. 59, pp. 2759–2762. https://doi.org/10.1099/ijs.0.008912-0

    Article  CAS  PubMed  Google Scholar 

  65. Touchette, D., Altshuler, I., Gostinčar, C., Zalar, P., Raymond-Bouchard, I., Zajc, J., McKay, C.P., GundeCimerman, N., and Whyte, L.G., ISME J., 2022, vol. 16, pp. 221–232. https://doi.org/10.1038/s41396-021-01030-9

    Article  CAS  PubMed  Google Scholar 

  66. Raza, M., Zhang, Z.-F., Hyde, K.D., Diao, Y.-Z., and Cai, L., Fungal Divers., 2019, vol. 99, pp. 1–104. https://doi.org/10.1007/s13225-019-00434-5

  67. Bennur, T., Ravi Kumar, A., Zinjarde, S.S., and Javdekar, V., J. Appl. Microbiol., 2016, vol. 120, pp. 1–16. https://doi.org/10.1111/jam.12950

    Article  CAS  PubMed  Google Scholar 

  68. Xu, D., Nepal, K.K., Chen, J., Harmody, D., Zhu, H., McCarthy, P.J., Wright, A.E., and Wang, G., Synth. Syst. Biotechnol., 2018, vol. 3, pp. 246–251. https://doi.org/10.1016/j.synbio.2018.10.008

    Article  PubMed  PubMed Central  Google Scholar 

  69. Vela, A.I., Sánchez-Porro, C., Aragón, V., Olvera, A., Domínguez, L., Ventosa, A., and Fernández-Garayzábal, J.F., Int. J. Syst. Evol. Microbiol., 2010, vol. 60, pp. 2446–2450. https://doi.org/10.1099/ijs.0.016626-0

    Article  CAS  PubMed  Google Scholar 

  70. Vela, A.I., Arroyo, E., Aragon, V., Sanchez-Porro, C., Latre, M.V., Cerda-Cuellar, M., Ventosa, A., Dominguez, L., and Fernandez-Garayzabal, J.F., Int. J. Syst. Evol. Microbiol., 2009, vol. 59, pp. 671–674. https://doi.org/10.1099/ijs.0.006205-0

    Article  CAS  PubMed  Google Scholar 

  71. Fusco, V., Quero, G.M., Cho, G.-S., Kabisch, J., Meske, D., Neve, H., Bockelmann, W., and Franz, C.M.A.P., Front. Microbiol., 2015, vol. 6, Article ID: 155. https://doi.org/10.3389/fmicb.2015.00155

  72. Borgo, F., Ballestriero, F., Ferrario, C., and Fortina, M.G., Ann. Microbiol., 2015, vol. 65, pp. 833–839. https://doi.org/10.1007/s13213-014-0924-x

    Article  CAS  Google Scholar 

  73. Fisher, K. and Phillips, C., Microbiology, 2009, vol. 155, pp. 1749–1757. https://doi.org/10.1099/mic.0.026385-0

    Article  CAS  PubMed  Google Scholar 

  74. Liu, L., Chen, D., Liu, L., Lan, R., Hao, S., Jin, W., Sun, H., Wang, Y., Liang, Y., and Xu, J., Front. Cell. Infect. Microbiol., 2018, vol. 8, Article ID: 233. https://doi.org/10.3389/fcimb.2018.00233

  75. Rieusset, L., Rey, M., Muller, D., Vacheron, J., Gerin, F., Dubost, A., Comte, G., and Prigent-Combaret, C., Microb. Biotechnol., 2020, vol. 13, pp. 1562–1580. https://doi.org/10.1111/1751-7915.13598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Kudo, S., Morimoto, Y.V., and Nakamura, S., Microbiology, 2015, vol. 161, pp. 701–707. https://doi.org/10.1099/mic.0.000031

    Article  CAS  PubMed  Google Scholar 

  77. Dickerman, A., Bandara, A.B., and Inzana, T.J., Int. J. Syst. Evol. Microbiol., 2020, vol. 70, pp. 180–186. https://doi.org/10.1099/ijsem.0.003730

    Article  CAS  PubMed  Google Scholar 

  78. Nasu, M., Tohoku J. Exp. Med., 1981, vol. 133, pp. 33–43. https://doi.org/10.1620/tjem.133.33

    Article  CAS  PubMed  Google Scholar 

  79. Stein, T., Mol. Microbiol., 2005, vol. 56, pp. 845–857. https://doi.org/10.1111/j.1365-2958.2005.04587.x

    Article  CAS  PubMed  Google Scholar 

  80. Tyurin, A., Alferova, V., and Korshun, V., Microorganisms, 2018, vol. 6, Article ID: 52. https://doi.org/10.3390/microorganisms6020052

  81. Björkroth, K.J., Schillinger, U., Geisen, R., Weiss, N., Hoste, B., Holzapfel, W.H., Korkeala, H.J., and Vandamme, P., Int. J. Syst. Evol. Microbiol., 2002, vol. 52, pp. 141–148. https://doi.org/10.1099/00207713-52-1-141

    Article  PubMed  Google Scholar 

  82. Fortina, M.G., Ricci, G., Mora, D., and Manachini, P.L., Int. J. Syst. Evol. Microbiol., 2004, vol. 54, pp. 1717–1721. https://doi.org/10.1099/ijs.0.63190-0

    Article  CAS  PubMed  Google Scholar 

  83. Jančič, U. and Gorgieva, S., Pharmaceutics, 2021, vol. 14, Article ID: 76. https://doi.org/10.3390/pharmaceutics14010076

  84. Muthukrishnan, P., Chithra Devi, D., Mostafa, A.A., Alsamhary, K.I., Abdel-Raouf, N., and Nageh Sholkamy, E., J. Infect. Publ. Health., 2020, vol. 13, pp. 1522–1532. https://doi.org/10.1016/j.jiph.2020.06.025

    Article  Google Scholar 

  85. Baranova, A.A., Chistov, A.A., Tyurin, A.P., Prokhorenko, I.A., Korshun, V.A., Biryukov, M.V., Alferova, V.A., and Zakalyukina, Y.V., Microorganisms, 2020, vol. 8, Article ID: 1948. https://doi.org/10.3390/microorganisms8121948

  86. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically, 11th Ed., Clinical and Laboratory Standards Institute (CLSI): Wayne, USA, 2015. https://clsi.org/standards/products/microbiology/documents/m07/

  87. Performance Standards for Antimicrobial Susceptibility Testing: 25th Informational Supplement, Clinical and Laboratory Standards Institute (CLSI): Wayne, USA, 2015. https://clsi.org/media/1631/m02a12_sample.pdf

  88. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts, 3rd Ed., Clinical and Laboratory Standards Institute (CLSI): Wayne, USA, 2008. https://clsi.org/media/1461/m27a3_sample.pdf

  89. Smith, A.C. and Hussey, M.A., Gram Stain Protocols, 2005. https://asm.org/getattachment/5c95a063-326b-4b2f-98ce-001de9a5ece3/gram-stain-protocol-2886.pdf

  90. Glass, N.L. and Donaldson, G.C., Appl. Environment. Microbiol., 1995, vol. 61, pp. 1323–1330. https://doi.org/10.1128/aem.61.4.1323-1330.1995

    Article  CAS  Google Scholar 

  91. White, T.J., Bruns, T., Lee, S., and Taylor, J., PCR Protocols. A Guide to Methods and Applications, Academic Press, Cambridge, Massachusetts, U.S., 1990, pp. 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1

  92. Lane, D.J., Stackebrandt, E., and Goodfellow, M., Nucleic Acid Techniques in Bacterial Systematic, Wiley, Hoboken, New Jersey, U.S., 1991.

  93. Glauert, A.M., Practical Methods in Electron Microscopy, North-Holland Publishing Company, Amsterdam, London, 1974.

  94. Wang, M., Carver, J.J., Phelan, V.V., Sanchez, L.M., Garg, N., Peng, Y., Nguyen, D.D., Watrous, J., Kapono, C.A., Luzzatto-Knaan, T., Porto, C., Bouslimani, A., Melnik, A.V., Meehan, M.J., Liu, W.-T., Crüsemann, M., Boudreau, P.D., Esquenazi, E., Sandoval-Calderón, M., Kersten, R.D., Pace, L.A., Quinn, R.A., Duncan, K.R., Hsu, C.-C., Floros, D.J., Gavilan, R.G., Kleigrewe, K., Northen, T., Dutton, R.J., Parrot, D., Carlson, E.E., Aigle, B., Michelsen, C.F., Jelsbak, L., Sohlenkamp, C., Pevzner, P., Edlund, A., McLean, J., Piel, J., Murphy, B.T., Gerwick, L., Liaw, C.-C., Yang, Y.-L., Humpf, H.-U., Maansson, M., Keyzers, R.A., Sims, A.C., Johnson, A.R., Sidebottom, A.M., Sedio, B.E., Klitgaard, A., Larson, C.B., Boya P, C.A., Torres-Mendoza, D., Gonzalez, D.J., Silva, D.B., Marques, L.M., Demarque, D.P., Pociute, E., O’Neill, E.C., Briand, E., Helfrich, E.J.N., Granatosky, E.A., Glukhov, E., Ryffel, F., Houson, H., Mohimani, H., Kharbush, J.J., Zeng, Y., Vorholt, J.A., Kurita, K.L., Charusanti, P., McPhail, K.L., Nielsen, K.F., Vuong, L., Elfeki, M., Traxler, M.F., Engene, N., Koyama, N., Vining, O.B., Baric, R., Silva, R.R., Mascuch, S.J., Tomasi, S., Jenkins, S., Macherla, V., Hoffman, T., Agarwal, V., Williams, P.G., Dai, J., Neupane, R., Gurr, J., Rodríguez, A.M.C., Lamsa, A., Zhang, C., Dorrestein, K., Duggan, B.M., Almaliti, J., Allard, P.-M., Phapale, P., Nothias, L.-F., Alexandrov, T., Litaudon, M., Wolfender, J.-L., Kyle, J.E., Metz, T.O., Peryea, T., Nguyen, D.-T., VanLeer, D., Shinn, P., Jadhav, A., Müller, R., Waters, K.M., Shi, W., Liu, X., Zhang, L., Knight, R., Jensen, P.R., Palsson, B.Ø., Pogliano, K., Linington, R.G., Gutiérrez, M., Lopes, N.P., Gerwick, W.H., Moore, B.S., Dorrestein, P.C., and Bandeira, N., Nat. Biotechnol., 2016, vol. 34, pp. 828–837. https://doi.org/10.1038/nbt.3597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

ACKNOWLEDGMENTS

SEM studies were carried out at the “Electron microscopy in life sciences” Shared Research Facility at Moscow State University (Unique equipment setup “Three-dimensional electron microscopy and spectroscopy”).

We thank A.V. Korshun for helpful advice on publication design.

Funding

The work was supported by the Russian Science Foundation (project no. 23-24-00409). https://rscf.ru/en/project/23-24-00409/

Author information

Authors and Affiliations

  1. Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, 117997, Moscow, Russia

    A. A. Baranova, A. P. Tyurin, V. A. Korshun, O. A. Belozerova, A. V. Moiseenko, S. S. Terekhov & V. A. Alferova

  2. Department of Soil Science, Lomonosov Moscow State University, 119991, Moscow, Russia

    Y. V. Zakalyukina

  3. Department of Biology, Lomonosov Moscow State University, 119991, Moscow, Russia

    M. V. Biryukov & A. V. Moiseenko

Authors
  1. A. A. Baranova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Y. V. Zakalyukina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. P. Tyurin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. V. A. Korshun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. O. A. Belozerova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. V. Biryukov
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. V. Moiseenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. S. S. Terekhov
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. V. A. Alferova
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors made equal contributions to the writing of the article.

Corresponding author

Correspondence to V. A. Alferova.

Ethics declarations

Harm to animals during all sampling procedures was minimized in accordance with the principles of good veterinary practice and the Federal Law “On the Responsible Treatment of Animals and on Amendments to Certain Legislative Acts of the Russian Federation” dated December 27, 2018 (no. 498-FZ). All procedures were carried out with the informed consent of the animal owner and under his supervision. No conflict of interest was declared by the authors.

Additional information

Publisher's Note. Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baranova, A.A., Zakalyukina, Y.V., Tyurin, A.P. et al. Antimicrobial Metabolites from Pig Nasal Microbiota. Russ J Bioorg Chem 50, 354–374 (2024). https://doi.org/10.1134/S1068162024020237

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1068162024020237

Keywords:

Search

Navigation