Evaluation of effects of selenium nanoparticles on Bacillus subtilis

Keywords: TEM analysis; nifS (nitrogenfixation) like gene; system of selenite detoxification; uptake of Nano-Se; probiotic.

Abstract

The present study was performed to characterize of selenium nanoparticles (Nano-Se) which were synthesized by pulsed laser ablation in liquids to obtain the aqueous selenium citrate solution. The study was conducted using bacteriological and electronic-microscopic methods. Transmission electron microscopy (TEM) and spectroscopy analyses demonstrated that nano-selenium particles obtained by the method of selenium ablation had the size of 4–8 nm. UV-Visible Spectrum colloidal solution Nano-Se exhibited absorption maxima at 210 nm. To clarify some effects of the action of Nano-Se on Bacillus subtilis, we investigated the interaction of Nano-Se with B. subtilis IMV B-7392 before and after incubation with Nano-Se, examining TEM images. It has been shown that exposure to B. subtilis IMV B-7392 in the presence of Nano-Se is accompanied by the rapid uptake of Nano-Se by bacterial culture. TEM analysis found that the electron-dense Nano-Se particles were located in the intracellular spaces of B. subtilis IMV B-7392. That does not lead to changes in cultural and morphological characteristics of B. subtilis IMV B-7392. Using TEM, it has been shown that penetration of nanoparticles in the internal compartments is accompanied with transient porosity of the cell membrane of B. subtilis IMV B-7392 without rupturing it. The effective concentration of Nano-Se 0.2 × 10–3 mg/mL was found to increase the yield of biologically active substances of B. subtilis. In order to create probiotic nano-selenium containing products, the nutrient medium of B. subtilis IMV B-7392 was enriched with Nano-Se at 0.2 × 10–3 mg/mL. It was found that particles Nano-Se are non-toxic to the culture and did not exhibit bactericidal or bacteriostatic effects. The experimentally demonstrated ability of B. subtilis to absorb selenium nanoparticles has opened up the possibility of using Nano-Se as suitable drug carriers.

References

Ayala-Castro, C., Saini, A., & Outten, F. W. (2008). Fe-S cluster assembly pathways in bacteria. Microbiology and Molecular Biology Reviews, 72(1), 110–125.

Banerjee, S., & Hansen, J. N. (1988). Structure and expression of a gene encoding the precursor of subtilin, a small protein antibiotic. Journal of Biological Chemistry, 263(19), 9508–9514.

Bérdy, J. (2005). Bioactive microbial metabolites. The Journal of Antibiotics (Tokyo), 58(1), 1–26.

Bityutskyy, V. S., Tsekhmistrenko, О. S., Tsekhmistrenko, S. I., Spyvack, M. Y., & Shadura, U. M. (2017). Perspectives of cerium nanoparticles use in agriculture. The Animal Biology, 19(3), 9–17.

Böck, A. (2001). Selenium metabolism in bacteria. In: Selenium. Springer, Boston. Pp. 7–22.

Böck, A., Forchhammer, K., Heider, J., Leinfelder, W., Sawers, G., Veprek, B., & Zinoni, F. (1991). Selenocysteine: The 21st amino acid. Molecular Microbiology, 5(3), 515–520.

Burdett, I. D., Kirkwood, T. B., & Whalley, J. B. (1986). Growth kinetics of individual Bacillus subtilis cells and correlation with nucleoid extension. Journal of Bacteriology, 167(1), 219–230.

Burk, R. F. (1983). Biological activity of selenium. Annual Review of Nutrition, 3(1), 53–70.

Calomme, M. R., Van den Branden, K., & VandenBerghe, D. A. (1995). Selenium and Lactobacillus species. Journal of Applied Bacteriology, 79(3), 331–340.

Carotenuto, G., Pepe, G. P., & Nicolais, L. (2000). Preparation and characterization of nano-sized Ag/PVP composites for optical applications. The European Physical Journal B – Condensed Matter and Complex Systems, 16(1), 11–17.

Chandramohan, S., Sundar, K., & Muthukumaran, A. (2018). Monodispersed spherical shaped selenium nanoparticles (SeNPs) synthesized by Bacillus subtilis and its toxicity evaluation in zebrafish embryos. Materials Research Express, 5(2), 025020.

Cone, J. E., Del Rio, R. M., Davis, J. N., & Stadtman, T. C. (1976). Chemical characterization of the selenoprotein component of clostridial glycine reductase: Identification of selenocysteine as the organoselenium moiety. Proceedings of the National Academy of Sciences, 73(8), 2659–2663.

Cui, D., Liang, T., Sun, L., Meng, L., Yang, C., Wang, L., Liang, T., & Li, Q. (2018). Green synthesis of selenium nanoparticles with extract of hawthorn fruit induced HepG2 cells apoptosis. Pharmaceutical Biology, 56(1), 528–534.

Dhevahi, B., & Gurusamy, R. (2014). Factors influencing production of lipase under metal supplementation by bacterial strain, Bacillus subtilis BDG-8. Journal of Environmental Biology, 35(6), 1151–1155.

Dobias, J., Suvorova, E. I., & Bernier-Latmani, R. (2011). Role of proteins in controlling selenium nanoparticle size. Nanotechnology, 22(19), 195605.

Eswayah, A. S., Smith, T. J., & Gardiner, P. H. (2016). Microbial transformations of selenium species of relevance to bioremediation. Applied Environmental Microbiology, 82(16), 4848–4859.

Etezad, S. M., Khajeh, K., Soudi, M., Ghazvini, P. T. M., & Dabirmanesh, B. (2009). Evidence on the presence of two distinct enzymes responsible for the reduction of selenate and tellurite in Bacillus sp. STG-83. Enzyme and Microbial Technology, 45(1), 1–6.

Forchhammer, K., & Böck, A. (1991). Selenocysteine synthase from Escherichia coli. Analysis of the reaction sequence. Journal of Biological Chemistry, 266(10), 6324–6328.

Forchhammer, K., Leinfelder, W., & Böck, A. (1989). Identification of a novel translation factor necessary for the incorporation of selenocysteine into protein. Nature, 342(6248), 453–456.

Garbisu, C., Carlson, D., Adamkiewicz, M., Yee, B. C., Wong, J. H., Resto, E., Leighton, T., & Buchanan, B. B. (1999). Morphological and biochemical responses of Bacillus subtilis to selenite stress. BioFactors, 10(4), 311–319.

Garbisu, C., Gonzalez, S., Yang, W. H., Yee, B. C., Carlson, D. L., Yee, A., Smith, N. R., Otero, R., Buchanan, B. B., & Leighton, T. (1995). Physiological mechanisms regulating the conversion of selenite to elemental selenium by Bacillus subtilis. BioFactors, 5(1), 29–37.

Garbisu, C., Ishii, T., Leighton, T., & Buchanan, B. B. (1996). Bacterial reduction of selenite to elemental selenium. Chemical Geology, 132, 199–204.

Glass, R. S., Singh, W. P., Jung, W., Veres, Z., Scholz, T. D., & Stadtman, T. (1993). Monoselenophosphate: Synthesis, characterization, and identity with the prokaryotic biological selenium donor, compound SePX. Biochemistry, 32(47), 12555–12559.

Hartwig, A., Asmuss, M., Ehleben, I., Herzer, U., Kostelac, D., Pelzer, A., Schwerdtle, T., & Bürkle, A. (2002). Interference by toxic metal ions with DNA repair processes and cell cycle control: Molecular mechanisms. Environmental Health Perspectives, 110(suppl. 5), 797–799.

Javed, S., Sarwar, A., Tassawar, M., & Faisal, M. (2015). Conversion of selenite to elemental selenium by indigenous bacteria isolated from polluted areas. Chemical Speciation and Bioavailability, 27(4), 162–168.

Jin, W., Yoon, C., Johnston, T. V., Ku, S., & Ji, G. E. (2018). Production of selenomethionine-enriched Bifidobacterium bifidum BGN4 via sodium selenite biocatalysis. Molecules, 23(11), 2860.

Joardar, S., Ray, S., Samanta, S., & Bhattacharjee, P. (2016). Antibacterial activity of 3,6-di(pyridin-2-yl)-1,2,4,5-s-tetrazine capped Pd(0) nanoparticles against gram-positive Bacillus subtilis bacteria. Cogent Biology, 2(1), 1249232.

Kessi, J., & Hanselmann, K. W. (2004). Similarities between the abiotic reduction of selenite with glutathione and the dissimilatory reaction mediated by Rhodospirillum rubrum and Escherichia coli. Journal of Biological Chemistry, 279(49), 50662–50669.

Kessi, J., Ramuz, M., Wehrli, E., Spycher, M., & Bachofen, R. (1999). Reduction of selenite and detoxification of elemental selenium by the phototrophic bacterium Rhodospirillum rubrum. Applied Environmental Microbiology, 65(11), 4734–4740.

Klein, C., Kaletta, C., Schnell, N., & Entian, K. D. (1992). Analysis of genes involved in biosynthesis of the lantibioticsubtilin. Applied Environmental Microbiology, 58(1), 132–142.

Kloepfer, J. A., Mielke, R. E., & Nadeau, J. L. (2005). Uptake of CdSe and CdSe/ZnS quantum dots into bacteria via purine-dependent mechanisms. Applied Environmental Microbiology, 71(5), 2548–2557.

Kumar, A., Pandey, A. K., Singh, S. S., Shanker, R., & Dhawan, A. (2011a). A flow cytometric method to assess nanoparticle uptake in bacteria. Cytometry A, 79(9), 707–712.

Kumar, A., Pandey, A. K., Singh, S. S., Shanker, R., & Dhawan, A. (2011b). Cellular uptake and mutagenic potential of metal oxide nanoparticles in bacterial cells. Chemosphere, 83(8), 1124–1132.

Kurek, E., Ruszczyńska, A., Wojciechowski, M., Łuciuk, A., Michalska-Kacymirow, M., Motyl, I., & Bulska, E. (2016). Bio-transformation of selenium in Se-enriched bacterial strains of Lactobacillus casei. Roczniki Panstwowego Zakladu Higieny, 67(3), 253–262.

Lacourciere, G. M., & Stadtman, T. C. (1998). The NIFS protein can function as a selenide delivery protein in the biosynthesis of selenophosphate. Journal of Biological Chemistry, 273(47), 30921–30926.

Lacourciere, G. M., Mihara, H., Kurihara, T., Esaki, N., & Stadtman, T. C. (2000). Escherichia coli NifS-like proteins provide selenium in the pathway for the biosynthesis of selenophosphate. Journal of Biological Chemistry, 275(31), 23769–23773.

Lampis, S., Zonaro, E., Bertolini, C., Cecconi, D., Monti, F., Micaroni, M., Turner, R. J., Butler, C. S., & Vallini, G. (2017). Selenite biotransformation and detoxification by Stenotrophomonas maltophilia SeITE02: Novel clues on the route to bacterial biogenesis of selenium nanoparticles. Journal of Hazardous Materials, 324, 3–14.

Lee, B. J., Worland, P. J., Davis, J. N., Stadtman, T. C., & Hatfield, D. L. (1989). Identification of a selenocysteyl-tRNA (Ser) in mammalian cells that recognizes the nonsense codon, UGA. Journal of Biological Chemistry, 264(17), 9724–9727.

Leong-Morgenthaler, P., Oliver, S. G., Hottinger, H., & Söll, D. (1994). A Lactobacillus nifS-like gene suppresses an Escherichia coli transaminase B mutation. Biochimie, 76(1), 45–49.

Li, X. Z., & Nikaido, H. (2004). Efflux-mediated drug resistance in bacteria. Drugs, 64(2), 159–204.

Mehdi, Y., Hornick, J. L., Istasse, L., & Dufrasne, I. (2013). Selenium in the environment, metabolism and involvement in body functions. Molecules, 18(3), 3292–3311.

Mullins, L. S., Hong, S. B., Gibson, G. E., Walker, H., Stadtman, T. C., & Raushel, F. M. (1997). Identification of a phosphorylated enzyme intermediate in the catalytic mechanism for selenophosphatesynthetase. Journal of the American Chemical Society, 119(28), 6684–6685.

Naito, M., Yokoyama, T., Hosokawa, K., & Nogi, K. (Eds.). (2018). Nanoparticle Technology Handbook. Elsevier.

Nancharaiah, Y. V., & Lens, P. N. L. (2015). Ecology and biotechnology of selenium-respiring bacteria. Microbiology and Molecular Biology Reviews, 79(1), 61–80.

Nelersa, C. M., Schmier, B. J., & Malhotra, A. (2011). Purification and crystallization of Bacillus subtilis NrnA, a novel enzyme involved in nanoRNA degradation. Acta Crystallographica Section F: Structural Biology and Crystallization Communications, 67(10), 1235–1238.

Newton, G. L., & Fahey, R. C. (1989). Glutathione in prokaryotes. Glutathione: Metabolism and physiological functions. CRC Press, Boca Raton, Florida, 69–77.

Newton, G. L., Rawat, M., La Clair, J. J., Jothivasan, V. K., Budiarto, T., Hamilton, C. J., Claiborne, A., Helmann, J. D., & Fahey, R. C. (2009). Bacillithiol is an antioxidant thiol produced in Bacilli. Nature Chemical Biology, 5(9), 625–627.

Oremland, R. S., Herbel, M. J., Blum, J. S., Langley, S., Beveridge, T. J., Ajayan, P. M., Sutto, T., Ellis, A. V., & Curran, S. (2004). Structural and spectral features of selenium nanospheres produced by Se-respiring bacteria. Applied Environmental Microbiology, 70(1), 52–60.

Oudhia, A. (2012). UV-VIS spectroscopy as a nondestructive and effective characterization tool for II–VI compounds. Recent Research in Science and Technology, 4(8), 109–111.

Overschelde, O. V., Guisbiers, G., & Snyders, R. (2013). Green synthesis of selenium nanoparticles by excimer pulsed laser ablation in water. APL Materials, 1, 042114.

Paige, A. J., Mccracken, V. J., Theodorakis, C., & Lin, Z.-Q. (2015). Microbial accumulation and transformation of nanoscale elemental selenium particles. Journal of Environmental Indicators, 9, 23–24.

Palomo-Siguero, M., & Madrid, Y. (2017). Exploring the behavior and metabolic transformations of SeNPs in exposed lactic acid bacteria. Effect of nanoparticles coating agent. International Journal of Molecular Sciences, 18(8), 1712.

Pantidos, N., & Horsfall, L. E. (2014). Biological synthesis of metallic nanoparticles by bacteria, fungi and plants. Journal of Nanomedicine and Nanotechnology, 5(5), 233–242.

Pouri, S., Motamedi, H., Honary, S., & Kazeminezhad, I. (2017). Biological synthesis of selenium nanoparticles and evaluation of their bioavailability. Brazilian Archives of Biology and Technology, 60, e17160452.

Rayman, M. P. (2004). The use of high-selenium yeast to raise selenium status: How does it measure up? British Journal of Nutrition, 92(4), 557–573.

Sargent, M. G. (1975). Control of cell length in Bacillus subtilis. Journal of Bacteriology, 123(1), 7–19.

Schrauzer, G. N. (2003). The nutritional significance, metabolism and toxicology of selenomethionine. Advances in Food and Nutrition Research, 47, 73–112.

Selim, N. A., Radwan, N. L., Youssef, S. F., Eldin, T. S., & Elwafa, S. A. (2015). Effect of inclusion inorganic, organic or nano selenium forms in broiler diets on: Physiological, immunological and toxicity statuses of broiler chicks. International Journal of Poultry Science, 14(3), 144–155.

Shirsat, S., Kadam, A., Naushad, M., & Mane, R. S. (2015). Selenium nanostructures: Microbial synthesis and applications. Royal Society of Chemistry Advances, 5(112), 92799–92811.

Singh, R., & Whitesides, G. M. (1991). Selenols catalyze the interchange reactions of dithiols and disulfides in water. The Journal of Organic Chemistry, 56(24), 6931–6933.

Sohm, B., Immel, F., Bauda, P., & Pagnout, C. (2015). Insight into the primary mode of action of TiO2 nanoparticles on Escherichia coli in the dark. Proteomics, 15(1), 98–113.

Stadtman, T. C. (1974). Selenium biochemistry: Proteins containing selenium are essential components of certain bacterial and mammalian enzyme systems. Science, 183(4128), 915–922.

Stolz, J. F., & Oremland, R. S. (1999). Bacterial respiration of arsenic and selenium. FEMS Microbiology Reviews, 23(5), 615–627.

Stolz, J. F., Basu, P., Santini, J. M., & Oremland, R. S. (2006). Arsenic and selenium in microbial metabolism. Annual Review of Microbiology, 60, 107–130.

Stolz, J., Basu, P., & Oremland, R. (2002). Microbial transformation of elements: The case of arsenic and selenium. International Microbiology, 5(4), 201–207.

Sun, D., & Setlow, P. (1993). Cloning, nucleotide sequence, and regulation of the Bacillus subtilis nadB gene and a nifS-like gene, both of which are essential for NAD biosynthesis. Journal of Bacteriology, 175(5), 1423–1432.

Tan, Y., Yao, R., Wang, R., Wang, D., Wang, G., & Zheng, S. (2016). Reduction of selenite to Se(0) nanoparticles by filamentous bacterium Streptomyces sp. ES2-5 isolated from a selenium mining soil. Microbial Cell Factories, 15(1), 157–166.

Thill, A., Zeyons, O., Spalla, O., Chauvat, F., Rose, J., Auffan, M., & Flank, A. M. (2006). Cytotoxicity of CeO2 nanoparticles for Escherichia coli. Physico-chemical insight of the cytotoxicity mechanism. Environmental Science and Technology, 40(19), 6151–6156.

Tsekhmistrenko, O. S., Tsekhmistrenko, S. I., Bityutskyy, V. S., Melnichenko, O. M., & Oleshko, O. A. (2018). Biomimetic and antioxidant activity of nanocrystalline cerium dioxide. World of Medicine and Biology, 14(63), 196–201.

Tsekhmistrenko, S. I., Bityutskyy, V. S., Tsekhmistrenko, O. S., Polishchuk, V. M., Polishchuk, S. A., Ponomarenko, N. V., Melnychenko, Y. O., & Spivak, M. Y. (2018). Enzyme-like activity of nanomaterials. Regulatory Mechanisms in Biosystems, 9(3), 469–476.

Veres, Z., Kim, I. Y., Scholz, T. D., & Stadtman, T. C. (1994). Selenophosphatesynthetase. Enzyme properties and catalytic reaction. Journal of Biological Chemistry, 269(14), 10597–10603.

Verma, A., Uzun, O., Hu, Y., Hu, Y., Han, H. S., Watson, N., Chen, S., & Stellacci, F. (2008). Surface-structure-regulated cell-membrane penetration by monolayer-protected nanoparticles. Nature Materials, 7(7), 588–595.

Wadhwani, S. A., Shedbalkar, U. U., Singh, R., & Chopade, B. A. (2016). Biogenic selenium nanoparticles: Current status and future prospects. Applied Microbiology and Biotechnology, 100(6), 2555–2566.

Wang, T., Yang, L., Zhang, B., & Liu, J. (2010). Extracellular biosynthesis and transformation of selenium nanoparticles and application in H2O2 biosensor. Colloids and Surfaces B: Biointerfaces, 80(1), 94–102.

Yu, Q., Boyanov, M. I., Liu, J., Kemner, K. M., & Fein, J. B. (2018). Adsorption of selenite onto Bacillus subtilis: The overlooked role of cell envelope sulfhydryl sites in the microbial conversion of Se (IV). Environmental Science and Technology, 52(18), 10400–10407.

Yuan, J., Palioura, S., Salazar, J. C., Su, D., O’Donoghue, P., Hohn, M. J., Cardoso, A. M., Whitman, W. B., & Söll, D. (2006). RNA-dependent conversion of phosphoserine forms selenocysteine in eukaryotes and archaea. Proceedings of the National Academy of Sciences, 103(50), 18923–18927.

Zee, J., Patterson, S., Wiseman, S., & Hecker, M. (2016). Is hepatic oxidative stress a main driver of dietary selenium toxicity in white sturgeon (Acipenser transmontanus)? Ecotoxicology and Environmental Safety, 133, 334–340.

Zinoni, F., Birkmann, A., Stadtman, T. C., & Böck, A. (1986). Nucleotide sequence and expression of the selenocysteine-containing polypeptide of formate dehydrogenase (formate-hydrogen-lyase-linked) from Escherichia coli. Proceedings of the National Academy of Sciences, 83(13), 4650–4654.

Published
2019-11-07
How to Cite
Tymoshok, N. O., Kharchuk, M. S., Kaplunenko, V. G., Bityutskyy, V. S., Tsekhmistrenko, S. I., Tsekhmistrenko, O. S., Spivak, M. Y., & MelnichenkoО. М. (2019). Evaluation of effects of selenium nanoparticles on Bacillus subtilis . Regulatory Mechanisms in Biosystems, 10(4), 544-552. https://doi.org/10.15421/021980

Most read articles by the same author(s)