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Spore production and sporulation efficacy of Bacillus subtilis under different source of manganese supplementation
[Produksi Spora dan Efisiensi Sporulasi Bacillus subtilis dengan Suplementasi Mangan dari Sumber yang Berbeda]
Corresponding Author(s) : Ating Yuniarti
Jurnal Ilmiah Perikanan dan Kelautan,
Vol. 11 No. 2 (2019): JURNAL ILMIAH PERIKANAN DAN KELAUTAN
Abstract
Abstract
Bacillus is a species widely used as a probiotic in the aquaculture industry. The Bacillus spores have more advantages than their vegetative ones, and an addition of minerals such as calcium, magnesium, and manganese can improve the spore production. The purpose of this study was to determine the effect of different sources of manganese on the production and sporulation efficacy of B. subtilis SB3. The sources of manganese used in this study were manganese chloride (MnCl2) and manganese sulfate (MnSO4) at the concentration of 10 mM. Media without manganese supplementation was used as a control. The results showed that there was a significant effect of different manganese sources on the spore production of B. subtilis SB3. The highest spore production was found in media with MnCl2 supplementation with the total spore of 8.77 x 107 spores. mL-1. However, spore production with MnSO4 supplementation was still higher (22.7%) compared to that without manganese supplementation. The decrease in spore production with MnSO4 supplementation was possible due to the sulfate inhibition. The high spore production in media with MnCl2 supplementation was also preceded by the high production of vegetative cells from B. subtilis SB3 (2.54 x 108 cells. mL-1). The results indicated that manganese could stimulate both vegetative cell growth and its spores. The highest sporulation efficacy (35%) was also achieved in media with MnCl2 supplementation. On the other hand, the germination rate of B. subtilis SB3 spores was not influenced by manganese supplementation.
Abstrak
Bacillus adalah species yang banyak digunakan sebagai probiotik pada industri akuakultur. Dalam bentuk spora, species ini lebih banyak mempunyai kelebihan dibandingkan dalam bentuk vegetatifnya dan peningkatan produksi sporanya dapat dilakukan dengan penambahan mineral seperti kalsium, magnesium dan mangan. Tujuan penelitian ini adalah untuk mengetahui pengaruh sumber mangan yang berbeda terhadap produksi dan efisiensi sporulasi B. subtilis SB3 indigenous akuatik. Sumber mangan yang dipakai dalam penelitian ini adalah mangan klorida (MnCl2) dan mangan sulfat (MnSO4) sebanyak 10 mM dan sebagai kontrol digunakan media tanpa suplementasi mangan. Hasil penelitian menunjukkan bahwa terdapat pengaruh yang nyata penggunaan sumber mangan yang berbeda terhadap produksi spora. Produksi spora tertinggi didapatkan pada media dengan suplementasi MnCl2 sebanyak 8,77 x 107 spora. mL-1. Sedangkan produksi spora dengan suplementasi MnSO4 juga masih lebih tinggi (22,7%) dibandingkan tanpa suplementasi magan. Penurunan produksi spora pada media dengan penambahan mangan sulfat diduga karena adanya penghambatan oleh sulfat. Tingginya produksi spora pada media dengan suplementasi MnCl2 sebelumnya juga didahului dengan tingginya produksi sel vegetatif dari B. subtilis SB3 (2,54 x 108sel. mL-1). Hal ini menunjukkan bahwa mangan dapat menstimulasi baik pertumbuhan sel vegetatif dan sporanya. Efisiensi sporulasi tertinggi juga dicapai pada media dengan suplementasi MnCl2 sebesar 35%. Di sisi lain, kemampuan germinasi spora B. subtilis SB3 tercatat sama dan tidak dipengaruhi oleh suplementasi mangan.
Keywords
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- Boonthai, T., Vuthiphandchai, V., & Nimrat, S. (2011). Probiotic bacteria effects on growth and bacterial composition of black tiger shrimp (Penaeus monodon). Aquaculture Nutrition, 17(6), 634–644. https://doi.org/10.1111/j.1365-2095.2011.00865.x
- Buhr, T. L., Mcpherson, D. C., & Gutting, B. W. (2008). Analysis of broth-cultured Bacillus atrophaeus and Bacillus cereus spores. Journal of Applied Microbiology, 105(1965), 1604–1613. https://doi.org/10.1111/j.1365-2672.2008.03899.x
- Cauble, S. M., Grajeda, J., & Quinones, C. (1984). Chemically Defined Sporulation Medium for Bacillus subtilis: growth, sporulation and Extrace. Journal of Bacteriology, 160(1), 438–441.
- Charney, J., Fisher, W. P., & Hegarty, C. P. (1951). Manganese as an essential elements for sporulation in the genus Bacillus. J . Bacteriol., 62, 145–148.
- Dawes, I. W., & Mandelstam, J. (1970). Sporulation of Bacillus subtilis in continuous culture. Journal of Bacteriology, 103(3), 529–535.
- Errington, J. (2003). Regulation of endospore formation in Bacillus subtilis. Nature Reviews Microbiology, 1(2), 117–126. https://doi.org/10.1038/nrmicro750
- Ghosh, S., Ramirez-Peralta, A., Gaidamakova, E., Zhang, P., Li, Y.-Q., Daly, M. J., & Setlow, P. (2011). Effects of Mn levels on resistance of Bacillus megaterium spores to heat , radiation and hydrogen peroxide. Journal of Applied Microbiology, 111, 663–670. https://doi.org/10.1111/j.1365-2672.2011.05095.x
- Granger, A. C., Gaidamakova, E. K., Matrosova, V. Y., Daly, M. J., & Setlow, P. (2011). Effects of levels of Mn and Fe on Bacillus subtilis spore resistance, and effects of Mn2+, other divalent cations, orthophosphate, and dipicolinic acid on resistance of a protein to ionizing radiation. Appl Environ Microbiol, 77, 32–40.
- Hong, H. A., Duc, L. H., & Cutting, S. (2005). The use of bacterial spore formers as probiotics. FEMS Microbiology Reviews, 29(4), 813–835. https://doi.org/10.1016/j.femsre.2004.12.001
- Lara-Flores, M. (2011). The use of probiotic in aquaculture : an overview. International Research Journal of Microbiology, 2(12), 471–478.
- Levinson, H. S., & Hyatt, M. T. (1964). Effect of sporulation medium on heat resistance, chemical composition, and germination of Bacillus megaterium spores. Journal of Bacteriology, 4(4), 876–886.
- Monteiro, S. M., Clemente, J., Henriques, A. O., Gomes, R. J., Carrondo, M. J., & Cunha, A. E. (2005). A Procedure for High-Yield Spore Production by Bacillus subtilis. Biotechnol. Prog., 21, 1026–1031.
- Monteiro, S. M. S., Clemente, J. J., Carrondo, M. J. T., & Cunha, A. E. (2014). Enhanced Spore Production of Bacillus subtilis Grown in a Chemically Defined Medium. Advances in Microbiology, 4, 444–454. https://doi.org/10.4236/aim.2014.48049
- Moriarty, D. J. W. (1999). Disease Control in Shrimp Aquaculture with Probiotic Bacteria. In Microbial Biosystem: New Frontiers.
- Nicholson, W.L., & Setlow, P. (1990). Sporulation, germination and outgrowth. In Molecular Biological Methods for Bacillus (pp. 391–450). Chichester UK: John Wiley and Sons Ltd.
- Nicholson, Wayne L, Munakata, N., Horneck, G., Melosh, H. J., & Setlow, P. (2000). Resistance of Bacillus Endospores to Extreme Terrestrial and Extraterrestrial Environments, 64(3), 548–572.
- Omer, A. M. (2010). Bioformulations of bacillus spores for using as Biofertilizer. Life Science Journal, 7(4), 124–131.
- Posada-Uribe, L. F., Romero-Tabarez, M., & Villegas-Escobar, V. (2015). Effect of medium components and culture conditions in Bacillus subtilis EA-CB0575 spore production. Bioprocess and Biosystems Engineering, 38(10), 1879–1888. https://doi.org/10.1007/s00449-015-1428-1
- Ryu, J.-H., Kim, H., & Beuchat, L. R. (2016). Spore Formation by Bacillus cereus in Broth as Affected by Temperature, Nutrient Availability, and Manganese. Journal of Food Protection, 68(8), 1734–1738. https://doi.org/10.4315/0362-028x-68.8.1734
- Setlow, P. (2013). Summer meeting 2013 - when the sleepers wake: The germination of spores of Bacillus species. Journal of Applied Microbiology, 115(6), 1251–1268. https://doi.org/10.1111/jam.12343
- Setlow, Peter. (2014). Germination of Spores of Bacillus Species : What We Know and Do Not Know. Journal of Bacteriology, 196(7), 1297–1305. https://doi.org/10.1128/JB.01455-13
- Sinnelä, M. T., Park, Y. K., Lee, J. H., Jeong, K. C., Kim, Y., Hwang, H., & Mah, J. (2019). Effects of Calcium and Manganese on Sporulation of and Spoilage. Foods, 8, 119. https://doi.org/10.3390/foods8040119
- Ugoji, E., & Hunter, C. (2006). An investigation of the shelf-life (storage) of Bacillus isolates on seeds. South African Journal of Botany, 72, 28–33. https://doi.org/10.1016/j.sajb.2005.04.001
- Villamil, L., & Reyes, C. (2012). In vivo and in vitro assessment of Lactobacillus acidophilus as probiotic for tilapia ( Oreochromis niloticus , Perciformes : Cichlidae ) culture improvement. Aquaculture Research, 1–10. https://doi.org/10.1111/are.12051
- Weinberg, E. D. (1964). Manganese Requirement for Sporulation and Other Secondary Biosynthetic Processes of Bacillus ’. Appl. Microbiol., 12(5), 436–441.
- Wolken, W. A. M., Tramper, J., & Werf, M. J. van der. (2003). What can spores do for us ? Trends in Biotechnology, 21(8), 338–345. https://doi.org/10.1016/S0167-7799(03)00170-7
- Yuniarti, A., Guntoro, D. A., & Hariati, A. M. (2013). Response of Indigenous Bacillus megaterium Supplementation on the Growth of Litopenaeus vannamei ( Boone ), a New Target Species for Shrimp Culture in East Java of Indonesia. J. Basic. Appl. Sci. Res., 3(1), 747–754.
- Yuniarti, A., Maftuch, Soemarno, & Aulanni’am. (2015a). In vitro and in vivo study of acyl homoserine lactone degrading Bacillus against Vibrio harveyi. International Journal of Biosciences, 6(2), 338–348.
- Yuniarti, A., Maftuch, Soemarno, & Aulanni’am. (2015b). In vitro assessments of Bacillus as a potential probiotic in shrimp culture of East Java Indonesia. Asian Jr. of Microbiol. Biotech. Env. Science, 17(1), 27–34.
References
Boonthai, T., Vuthiphandchai, V., & Nimrat, S. (2011). Probiotic bacteria effects on growth and bacterial composition of black tiger shrimp (Penaeus monodon). Aquaculture Nutrition, 17(6), 634–644. https://doi.org/10.1111/j.1365-2095.2011.00865.x
Buhr, T. L., Mcpherson, D. C., & Gutting, B. W. (2008). Analysis of broth-cultured Bacillus atrophaeus and Bacillus cereus spores. Journal of Applied Microbiology, 105(1965), 1604–1613. https://doi.org/10.1111/j.1365-2672.2008.03899.x
Cauble, S. M., Grajeda, J., & Quinones, C. (1984). Chemically Defined Sporulation Medium for Bacillus subtilis: growth, sporulation and Extrace. Journal of Bacteriology, 160(1), 438–441.
Charney, J., Fisher, W. P., & Hegarty, C. P. (1951). Manganese as an essential elements for sporulation in the genus Bacillus. J . Bacteriol., 62, 145–148.
Dawes, I. W., & Mandelstam, J. (1970). Sporulation of Bacillus subtilis in continuous culture. Journal of Bacteriology, 103(3), 529–535.
Errington, J. (2003). Regulation of endospore formation in Bacillus subtilis. Nature Reviews Microbiology, 1(2), 117–126. https://doi.org/10.1038/nrmicro750
Ghosh, S., Ramirez-Peralta, A., Gaidamakova, E., Zhang, P., Li, Y.-Q., Daly, M. J., & Setlow, P. (2011). Effects of Mn levels on resistance of Bacillus megaterium spores to heat , radiation and hydrogen peroxide. Journal of Applied Microbiology, 111, 663–670. https://doi.org/10.1111/j.1365-2672.2011.05095.x
Granger, A. C., Gaidamakova, E. K., Matrosova, V. Y., Daly, M. J., & Setlow, P. (2011). Effects of levels of Mn and Fe on Bacillus subtilis spore resistance, and effects of Mn2+, other divalent cations, orthophosphate, and dipicolinic acid on resistance of a protein to ionizing radiation. Appl Environ Microbiol, 77, 32–40.
Hong, H. A., Duc, L. H., & Cutting, S. (2005). The use of bacterial spore formers as probiotics. FEMS Microbiology Reviews, 29(4), 813–835. https://doi.org/10.1016/j.femsre.2004.12.001
Lara-Flores, M. (2011). The use of probiotic in aquaculture : an overview. International Research Journal of Microbiology, 2(12), 471–478.
Levinson, H. S., & Hyatt, M. T. (1964). Effect of sporulation medium on heat resistance, chemical composition, and germination of Bacillus megaterium spores. Journal of Bacteriology, 4(4), 876–886.
Monteiro, S. M., Clemente, J., Henriques, A. O., Gomes, R. J., Carrondo, M. J., & Cunha, A. E. (2005). A Procedure for High-Yield Spore Production by Bacillus subtilis. Biotechnol. Prog., 21, 1026–1031.
Monteiro, S. M. S., Clemente, J. J., Carrondo, M. J. T., & Cunha, A. E. (2014). Enhanced Spore Production of Bacillus subtilis Grown in a Chemically Defined Medium. Advances in Microbiology, 4, 444–454. https://doi.org/10.4236/aim.2014.48049
Moriarty, D. J. W. (1999). Disease Control in Shrimp Aquaculture with Probiotic Bacteria. In Microbial Biosystem: New Frontiers.
Nicholson, W.L., & Setlow, P. (1990). Sporulation, germination and outgrowth. In Molecular Biological Methods for Bacillus (pp. 391–450). Chichester UK: John Wiley and Sons Ltd.
Nicholson, Wayne L, Munakata, N., Horneck, G., Melosh, H. J., & Setlow, P. (2000). Resistance of Bacillus Endospores to Extreme Terrestrial and Extraterrestrial Environments, 64(3), 548–572.
Omer, A. M. (2010). Bioformulations of bacillus spores for using as Biofertilizer. Life Science Journal, 7(4), 124–131.
Posada-Uribe, L. F., Romero-Tabarez, M., & Villegas-Escobar, V. (2015). Effect of medium components and culture conditions in Bacillus subtilis EA-CB0575 spore production. Bioprocess and Biosystems Engineering, 38(10), 1879–1888. https://doi.org/10.1007/s00449-015-1428-1
Ryu, J.-H., Kim, H., & Beuchat, L. R. (2016). Spore Formation by Bacillus cereus in Broth as Affected by Temperature, Nutrient Availability, and Manganese. Journal of Food Protection, 68(8), 1734–1738. https://doi.org/10.4315/0362-028x-68.8.1734
Setlow, P. (2013). Summer meeting 2013 - when the sleepers wake: The germination of spores of Bacillus species. Journal of Applied Microbiology, 115(6), 1251–1268. https://doi.org/10.1111/jam.12343
Setlow, Peter. (2014). Germination of Spores of Bacillus Species : What We Know and Do Not Know. Journal of Bacteriology, 196(7), 1297–1305. https://doi.org/10.1128/JB.01455-13
Sinnelä, M. T., Park, Y. K., Lee, J. H., Jeong, K. C., Kim, Y., Hwang, H., & Mah, J. (2019). Effects of Calcium and Manganese on Sporulation of and Spoilage. Foods, 8, 119. https://doi.org/10.3390/foods8040119
Ugoji, E., & Hunter, C. (2006). An investigation of the shelf-life (storage) of Bacillus isolates on seeds. South African Journal of Botany, 72, 28–33. https://doi.org/10.1016/j.sajb.2005.04.001
Villamil, L., & Reyes, C. (2012). In vivo and in vitro assessment of Lactobacillus acidophilus as probiotic for tilapia ( Oreochromis niloticus , Perciformes : Cichlidae ) culture improvement. Aquaculture Research, 1–10. https://doi.org/10.1111/are.12051
Weinberg, E. D. (1964). Manganese Requirement for Sporulation and Other Secondary Biosynthetic Processes of Bacillus ’. Appl. Microbiol., 12(5), 436–441.
Wolken, W. A. M., Tramper, J., & Werf, M. J. van der. (2003). What can spores do for us ? Trends in Biotechnology, 21(8), 338–345. https://doi.org/10.1016/S0167-7799(03)00170-7
Yuniarti, A., Guntoro, D. A., & Hariati, A. M. (2013). Response of Indigenous Bacillus megaterium Supplementation on the Growth of Litopenaeus vannamei ( Boone ), a New Target Species for Shrimp Culture in East Java of Indonesia. J. Basic. Appl. Sci. Res., 3(1), 747–754.
Yuniarti, A., Maftuch, Soemarno, & Aulanni’am. (2015a). In vitro and in vivo study of acyl homoserine lactone degrading Bacillus against Vibrio harveyi. International Journal of Biosciences, 6(2), 338–348.
Yuniarti, A., Maftuch, Soemarno, & Aulanni’am. (2015b). In vitro assessments of Bacillus as a potential probiotic in shrimp culture of East Java Indonesia. Asian Jr. of Microbiol. Biotech. Env. Science, 17(1), 27–34.