Journal of fish pathology (한국어병학회지)

The Korean Society of Fish Pathology (한국어병학회)
권호 표지
DOI QR코드

DOI QR Code

In vitro antimicrobial properties of Bacillus subtilis KCTC 1326 for fish bacterial disease management

  • Ji-Yoon Park (Department of Aquatic Life Medical Sciences, Summon University) ;
  • In-Joo Shin (Department of Aquatic Life Medical Sciences, Summon University) ;
  • So-Ri Han (Fishcare laboratory) ;
  • Sung-Hyun Kim (Fishcare laboratory) ;
  • Youhee Kim (Department of Smart Aquaculture, Gangwon State University) ;
  • Se Ryun Kwon (Department of Aquatic Life Medical Sciences, Summon University)
  • Received : 2024.05.24
  • Accepted : 2024.06.12
  • Published : 2024.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

This study evaluated in vitro antimicrobial properties of Bacillus subtilis KCTC 1326 as an environmentally friendly alternative to antibiotics. B. subtilis KCTC 1326 was characterized on biochemical properties and antibiotics susceptibility. It exhibited antimicrobial effects against all 12 species of fish bacteria used in this experiment. Among them, the largest antibacterial zone was observed for Streptococcus parauberis (34 mm), while the smallest antibacterial zone was observed for Citrobacter freundii (8 mm). Additionally, in the co-culture inhibitory assay of B. subtilis and Edwardsiella piscicida, the growth of E. piscicida was suppressed with increasing concentrations of B. subtilis KCTC 1326, with complete inhibition observed at 107 and 108 CFU/mL of B. subtilis KCTC 1326 after 24 hours of incubation. Moreover, at 48 hours of incubation, the growth of E. piscicida was inhibited across all concentration ranges of B. subtilis KCTC 1326. Therefore, this study indicated the utilizing of B. subtilis KCTC 1326 as an antimicrobial for controlling fish bacterial diseases.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea grant (NRF-2023R1A2C1008182) and the Korea Innovation Foundation grant (2023-DD-UP-0007) funded by the Ministry of Science and ICT (MSIT).

References

  1. Abarike, E.D., Cai, J., Lu, Y., Yu, H., Chen, L., Jian, J., Tang, J., Jun, L. and Kuebutornye, F.K.A.: Effects of a commercial probiotic BS containing Bacillus subtilis and Bacillus licheniformis on growth, immune response and disease resistance in Nile tilapia, Oreochromis niloticus. Fish & shellfish immunology, 82:229-238, 2018. https://doi.org/10.1016/j.fsi.2018.08.037
  2. Abriouel, H., Franz, C.M.A.P., Omar, N.B. and Galvez, A.: Diversity and applications of Bacillus bacteriocins. FEMS microbiology reviews, 35(1):201-232, 2011. https://doi.org/10.1111/j.1574-6976.2010.00244.x
  3. Adesiyan, I.M., Bisi-Johnson, M.A., Ogunfowokan, A.O. and Okoh, A.I.: Incidence and antimicrobial susceptibility fingerprints of Plesiomonas shigelliodes isolates in water samples collected from some freshwater resources in Southwest Nigeria. Science of the total environment, 665:632-640, 2019. https://doi.org/10.1016/j.scitotenv.2019.02.062
  4. Anagnostopoulos, C. and Spizizen, J.: Requirements for transformation in Bacillus subtilis. Journal of Bacteriology, 81:741-746, 1961. https://doi.org/10.1128/jb.81.5.741-746.1961
  5. Blibech, M., Mouelhi, S., Farhat-Khemakhem, A., Boukhris, I., Ayeb, A.E. and Chouayekh, H.: Selection of Bacillus subtilis US191 as a mannanase-producing probiotic candidate. Biotechnology and Applied Biochemistry, 66(5):858-869, 2019. https://doi.org/10.1002/bab.1798
  6. Caulier, S., Nannan, C., Gillis, A., Licciardi, F., Bragard, C. and Mahillon, J.: Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group. Frontiers in microbiology, 10:435128, 2019. https://doi.org/10.3389/fmicb.2019.00302
  7. Costa, T.S., Copatti, C.E., da Silva, J.J., Marchao, R.S., da Silva, R.C., da Silva Rocha, A., Pereira, G.A., da Rocha, D.R., de Souza, A.M., da Costa, M.M., Martins, I.P.S., Moreira, J.F. and Melo, J.F.B.: Use of Bacillus subtilis multiplicate in the water used for biofloc formation: Growth, hemato-biochemistry, intestinal bacteria colonies, and bacterial resistance evaluations of Nile tilapia. Aquaculture, 590:741 039, 2024. https://doi.org/10.1016/j.aquaculture.2024.741039
  8. De Souza, D.M., Suita, S.M., Leite, F.P.L., Romano, L.A., Wasielesky, W. and Ballester, E.L.C.: The use of probiotics during the nursery rearing of the pink shrimp Farfantepenaeus brasiliensis (Latreille, 1817) in a zero exchange system. Aquaculture Research, 43(12):1828-1837, 2012. https://doi.org/10.1111/j.1365-2109.2011.02992.x
  9. El-Saadony, M.T., Alagawany, M., Patra, A.K., Kar, I., Tiwari, R., Dawood, M.A.O., Dhama, K. and AbdelLatif, H.M.R.: The functionality of probiotics in aquaculture: An overview. Fish & shellfish immunology, 117:36-52, 2021. https://doi.org/10.1016/j.fsi.2021.07.007
  10. Guo, X., Chen, D.D., Peng, K.S., Cui, Z.W., Zhang, X.J., Li, S. and Zhang, Y.A.: Identification and characterization of Bacillus subtilis from grass carp (Ctenopharynodon idellus) for use as probiotic additives in aquatic feed. Fish & shellfish immunology, 52:74-84, 2016. https://doi.org/10.1016/j.fsi.2016.03.017
  11. Hao, K., Wu, Z.Q., Li, D.L., Yu, X.B., Wang, G.X. and Ling, F.: Effects of dietary administration of Shewanella xiamenensis A-1, Aeromonas veronii A-7, and Bacillus subtilis, single or combined, on the grass carp (Ctenopharyngodon idella) intestinal microbiota. Probiotics and antimicrobial proteins, 9:386-396, 2017. https://doi.org/10.1007/s12602-017-9269-7
  12. Hashmi, S., Iqbal, S., Ahmed, I. and Janjua, H.A.: Production, optimization, and partial purification of alkali-thermotolerant proteases from newly isolated Bacillus subtilis S1 and Bacillus amyloliquefaciens KSM12. Processes, 10(6):1050, 2022. https://doi.org/10.3390/pr10061050
  13. Janda, J.M. and Abbott, S.L.: The changing face of the family Enterobacteriaceae (Order: "Enterobacterales"): New members, taxonomic issues, geographic expansion, and new diseases and disease syndromes. Clinical microbiology reviews, 34(2):10-1128, 2021. https://doi.org/10.1128/cmr.00174-20
  14. Kim, D.H. and Heo, M.S.: Dietary effect of Bacillus subtilis MD-02 on Innate Immune Response and Disease Resistance in Olive Flounder, Paralichthys olivaceus. Microbiol. Biotechnol. Lett., 47(1):132-138, 2019. https://doi.org/10.4014/mbl.1807.07003
  15. Kim, H.W., Lee, E.S., Lee, S.J., Han, S.R., Oh, T.J., Kim, M.S., Kim, S.J. and Kwon, S.R.: The antibiotic resistance of Lactococcus lactis isolated from the farmed Anguilla japonica. J. Fish Pathol., 36(1):107-116, 2023a. https://doi.org/10.7847/jfp.2023.36.1.107
  16. Kim, H.W., Lee, E.S., Lee, S.J., Kim, H.E., Han, S.R., Oh, T.J., Kim, M.S., Kim, S.J. and Kwon, S.R.: Characterization of Photobacterium sp. YW2207 isolated from rainbow trout (Oncorhynchus mykiss) raised in a fresh water farm in South Korea. J. Fish Pathol., 36(2):251-261, 2023b. https://doi.org/10.7847/jfp.2023.36.2.251
  17. Kuebutornye, F.K., Abarike, E.D. and Lu, Y.: A review on the application of Bacillus as probiotics in aquaculture. Fish & shellfish immunology, 87:820-828, 2019. https://doi.org/10.1016/j.fsi.2019.02.010
  18. Lee, S.H., Katya, K., Park, Y.J., Won, S.H., Seong, M.J., Hamidoghli, A. and Bai, S.C.: Comparative evaluation of dietary probiotics Bacillus subtilis WB60 and Lactobacillus plantarum KCTC3928 on the growth performance, immunological parameters, gut morphology and disease resistance in Japanese eel, Anguilla japonica. Fish & shellfish immunology, 61:201-210, 2017. https://doi.org/10.1016/j.fsi.2016.12.035
  19. Logan, N.A. and Berkeley, R.C.W.: Identification of Bacillus strains using the API system. Microbiology, 130(7):1871-1882, 1984. https://doi.org/10.1099/00221287-130-7-1871
  20. Mabrok, M., Algammal, A.M., El-Tarabili, R.M., Dessouki, A.A., ElBanna, N.I., Abd-Elnaby, M., ElLamie M.M.M. and Rodkhum, C.: Enterobacter cloacae as a re-emerging pathogen affecting mullets (Mugil spp.): Pathogenicity testing, LD50, antibiogram, and encoded antimicrobial resistance genes. Aquaculture, 583:740619, 2024. https://doi.org/10.1016/j.aquaculture.2024.740619
  21. Nair, A.V., Antony, M.L., Praveen, N.K., Sayooj, P., Swaminathan, T.R. and Vijayan, K.K.: Evaluation of in vitro and in vivo potential of Bacillus subtilis MBTDCMFRI Ba37 as a candidate probiont in fish health management. Microbial Pathogenesis, 152:104610, 2021. https://doi.org/10.1016/j.micpath.2020.104610
  22. Nayak, S.K.: Multifaceted applications of probiotic Bacillus species in aquaculture with special reference to Bacillus subtilis. Reviews in Aquaculture, 13(2):862-906, 2021. https://doi.org/10.1111/raq.12503
  23. Pereira, C., Duarte, J., Costa, P., Braz, M. and Almeida, A.: Bacteriophages in the control of Aeromonas sp. in aquaculture systems: an integrative view. Antibiotics, 11(2):163, 2022. https://doi.org/10.3390/antibiotics11020163
  24. Ren, X., Wu, B., Zhao, F., Qi, L., Qiu, X., Li, R., Yang, S., Yi, G., Ding, X., Xia, L. and Sun, Y.: Antagonistic activity and protective effect of a Bacillus subtilis isolate against fish pathogen Edwardsiella piscicida. Fisheries science, 85:1011-1018, 2019. https://doi.org/10.1007/s12562-019-01346-8
  25. Rohani, M.F., Islam, S.M.M., Hossain, M.K., Ferdous, Z., Siddik, M.A.B., Nuruzzaman, M., Padeniya, U., Brown, C. and Shahjahan, M.: Probiotics, prebiotics and synbiotics improved the functionality of aquafeed: Upgrading growth, reproduction, immunity and disease resistance in fish. Fish & shellfish immunology, 120:569-589, 2022. https://doi.org/10.1016/j.fsi.2021.12.037
  26. Zhao, C., Wen, H., Huang, S., Weng, S. and He, J.: A novel disease (water bubble disease) of the giant freshwater prawn Macrobrachium rosenbergii caused by Citrobacter freundii: antibiotic treatment and effects on the antioxidant enzyme activity and immune responses. Antioxidants, 11(8):1491, 2022. https://doi.org/10.3390/antiox11081491
  27. Zokaeifar, H., Babaei, N., Saad, C.R., Kamarudin, M.S., Sijam, K. and Balcazar, J.L.: Administration of Bacillus subtilis strains in the rearing water enhances the water quality, growth performance, immune response, and resistance against Vibrio harveyi infection in juvenile white shrimp, Litopenaeus vannamei. Fish & shellfish immunology, 36(1):68-74, 2014. https://doi.org/10.1016/j.fsi.2013.10.007
  28. Zuenko, V.A., Laktionov, K.S., Pravdin, I.V., Kravtsova, L.Z. and Ushakova, N.A.: Effect of Bacillus subtilis in feed probiotic on the digestion of fish cultured in cages. Journal of ichthyology, 57:152-157, 2017. https://doi.org/10.1134/S0032945217010143