Sains Malaysiana 51(9)(2022): 3069-3079

http://doi.org/10.17576/jsm-2022-5109-26

Perbandingan Penghasilan Siderofor daripada Bacillus aryabhattai, Bacillus megaterium dan Bacillus cereus

(Comparison of Siderophore Production by Bacillus aryabhattai, Bacillus megaterium, and Bacillus cereus)

LEE SHIN YIN¹, YONG SHIH NEE², KUAN SENG HOW^2,3 & SYLVIA CHIENG^1,*  

¹Department of Biological Sciences and Biotechnology, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor Darul Ehsan, Malaysia

²Department of Mechanical and Material Engineering, Lee Kong Chian Faculty of Engineering and Science, Universiti Tunku Abdul Rahman, Sg Long Campus, 43000 Kajang, Selangor Darul Ehsan, Malaysia

³Centre for Photonics and Advanced Materials Research, Universiti Tunku Abdul Rahman, Sg Long Campus, 43000 Kajang, Selangor Darul Ehsan, Malaysia

Received: 14 March 2022/Accepted: 10 May 2022

Abstrak

Besi merupakan unsur yang penting bagi proses metabolisme organisma seperti kitar asid trikarboksilik, pengangkutan elektron dan fosforilasi oksidatif. Walau bagaimanapun, sumber besi di persekitaran luar sentiasa berada dalam bentuk kompleks yang tidak tersedia untuk pengambilan terus. Bagi mengatasi pengehadan besi, mikroorganisma berupaya untuk menghasilkan siderofor, sejenis pengkelat Fe(III) yang berafinan tinggi. Salah satu genus bakteria yang dapat menghasilkan siderofor adalah Bacillus. Dalam kajian ini, penghasilan dan keupayaan pengkompleksan siderofor Bacillus cereus, Bacillus megaterium dan Bacillus aryabhattai ditentukan melalui asai piring agar dan cecair krom azurol S (CAS). Kesan sumber karbon (glukosa, maltosa dan gliserol) ke atas penghasilan siderofor oleh Bacillus turut dikaji. Hasil kajian telah menunjukkan bahawa B. cereus yang dikulturkan dalam kaldu LB berupaya untuk menghasilkan siderofor yang tertinggi berbanding B. aryabhattai dan B. megaterium. Siderofor yang dihasilkan oleh ketiga-tiga spesies berupaya untuk berkompleks dengan Mn(II), Zn(II) dan Cu(II). Hasil kajian turut menunjukkan pengkulturan dengan maltosa telah memberikan penghasilan siderofor yang paling tinggi bagi B. aryabhattai dan B. megaterium.

Kata kunci: Bacillus aryabhattai; Bacillus cereus; Bacillus megaterium; siderofor

Abstract

Iron is an essential element for metabolic processes of organisms such as the tricarboxylic acid cycle, electron transport, and oxidative phophorylation. However, iron resources in the environment are always in complex forms that are not readily available for direct intake. To overcome iron limitation, microorganisms are able to produce a high affinity Fe(III) chelator, known as siderophore. One of the bacterial genus that can produced siderophore is Bacillus. In this study, the production and complexing ability of siderophore from Bacillus cereus, Bacillus megaterium, and Bacillus aryabhattai were determined through chrome azurol S (CAS) agar plate and liquid assay. The effect of carbon sources (glucose, maltose and glycerol) on siderophore production by the bacteria were also studied. The results demonstrated the ability of B. cereus to produce the most siderophore in LB broth in comparison to B. aryabhattai and B. megaterium. Siderophores produced by all three species were capable of complexing with Mn(II), Zn(II) and Cu(II). The results also showed that production of siderophore was the most effective with maltose as carbon source for B. aryabhattai and B. megaterium.

Keywords: Bacillus aryabhattai; Bacillus cereus; Bacillus megaterium; siderophore

REFERENCES

Alexander, D.B. & Zuberer, D.A. 1991. Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biology and Fertility of Soils 12(1): 39-45.

Bhattacharyya, C., Bakshi, U., Mallick, I., Mukherji, S., Bera, B. & Ghosh, A. 2017. Genome-guided insights into the plant growth promotion capabilities of the physiologically versatile Bacillus aryabhattai strain AB211. Frontiers in Microbiology 8(MAR): 1-16.

Costa, O.Y.A., Oguejiofor, C., Zühlke, D., Barreto, C.C., Wünsche, C., Riedel, K. & Kuramae, E.E. 2020. Impact of different trace elements on the growth and proteome of two strains of Granulicella, Class “Acidobacteriia.” Frontiers in Microbiology 11(June): 1-16.

Cornelis, P. 2010. Iron uptake and metabolism in pseudomonads. Applied Microbiology and Biotechnology 86(6): 1637-1645.

Crowle, A.J. 1973. Immunodiffusion. 2nd ed. Massachusetts: Academic Press. pp. 65-206.

Dahmani, M.A., Desrut, A., Moumen, B., Verdon, J., Mermouri, L., Kacem, M., Coutos-Thévenot, P., Kaid-Harche, M., Bergès, T. & Vriet, C. 2020. Unearthing the plant growth-promoting traits of Bacillus megaterium RmBm31, an endophytic bacterium isolated from root nodules of Retama monosperma. Frontiers in Plant Science 11(February): 1-15.

Danial, E.N. & Al-Bishri, W.M. 2020. Optimization of medium composition for increased production of tyrosinase enzyme in recombinant Bacillus megaterium. Research Journal of Pharmaceutical, Biological and Chemical Sciences 9(1): 480-486.

Dias, M.P., Bastos, M.S., Xavier, V.B., Cassel, E., Astarita, L.V. & Santarém, E.R. 2017. Plant growth and resistance promoted by Streptomyces spp. in tomato. Plant Physiology and Biochemistry 118: 479-493.

Duport, C., Jobin, M. & Schmitt, P. 2016. Adaptation in Bacillus cereus: From stress to disease. Frontiers in Microbiology 7(OCT): 1-18.

Ferreira, C.M.H., Boas, Â.V., Sousa, C.A., Soares, H.M.V.M. & Soares, E.V. 2019. Comparison of five bacterial strains producing siderophores with ability to chelate iron under alkaline conditions. AMB Express 9: 78.

Hayrapetyan, H., Siezen, R., Abee, T. & Groot, M.N. 2016. Comparative genomics of iron-transporting systems in Bacillus cereus strains and impact of iron sources on growth and biofilm formation. Frontiers in Microbiology 7(JUN): 1-13.

Hider, R.C. & Kong, X. 2010. Chemistry and biology of siderophores. Natural Product Reports 27(5): 637-657.

Huang, Y., Jiang, Y., Wang, H., Wang, J., Shin, M.C., Byun, Y., He, H., Liang, Y. & Yang, V.C. 2011. Curb challenges of the “Trojan horse” approach: Smart strategies in achieving effective yet safe cell-penetrating peptide-based drug delivery. Bone 23(1): 1-7.

Ijaz, A., Mumtaz, M.Z., Wang, X., Ahmad, M., Saqib, M., Maqbool, H., Zaheer, A., Wang, W. & Mustafa, A. 2021. Insights into manganese solubilizing Bacillus spp. for improving plant growth and manganese uptake in maize. Frontiers in Plant Science 12(November): 1-18.

Jun, Y.H., Nee, Y.S., Qi, C.W., Chieng, S. & How, K.S. 2020. Bioleaching of kaolin with Bacillus cereus: Effects of bacteria source and concentration on iron removal. Journal of Sustainability Science and Management 15(4): 91-99.

Kell, D.B., Heyden, E.L. & Pretorius, E. 2020. The biology of lactoferrin, an iron-binding protein that can help defend against viruses and bacteria. Frontiers in Immunology 11: 0-2.

Ladomersky, E. & Petris, M.J. 2015. Copper tolerance and virulence. Metallomics 7(6): 957-964.

Lakshmanan, V., Shantharaj, D., Li, G., Seyfferth, A.L., Janine Sherrier, D. & Bais, H.P. 2015. A natural rice rhizospheric bacterium abates arsenic accumulation in rice (Oryza sativa L.). Planta 242(4): 1037-1050.

Lewis, K., Epstein, S., D’Onofrio, A. & Ling, L.L. 2010. Uncultured microorganisms as a source of secondary metabolites. Journal of Antibiotics 63(8): 468-476.

Maleki, M., Norouzpour, S., Rezvannejad, E. & Shakeri, S. 2018. Novel strains of Bacillus cereus Wah1 and Enterobacter cloacae Wkh with high potential for production of siderophores. Biological Journal of Microorganism 6(24): 1-11.

Miethke, M. & Marahiel, M.A. 2007. Siderophore-based iron acquisition and pathogen control. Microbiology and Molecular Biology Reviews 71(3): 413-451.

Parker, D.L., Sposito, G. & Tebo, B.M. 2004. Manganese(III) binding to a pyoverdine siderophore produced by a manganese(II)-oxidizing bacterium. Geochimica et Cosmochimica Acta 68(23): 4809-4820.

Patel, P.R., Shaikh, S.S. & Sayyed, R.Z. 2018. Modified chrome azurol S method for detection and estimation of siderophores having affinity for metal ions other than iron. Environmental Sustainability 1(1): 81-87.

Payne, S.M. 1994. Detection, isolation, and characterization of siderophores. Methods in Enzymology 205(Ii): 205-213.

Pereira, D.G., Afonso, A. & Medeiros, F.M. 2015. Overview of Friedmans test and post-hoc analysis. Communications in Statistics: Simulation and Computation 44(10): 2636-2653.

Puig, S., Ramos-Alonso, L., Romero, A.M. & Martínez-Pastor, M.T. 2017. The elemental role of iron in DNA synthesis and repair. Metallomics 9(11): 1483-1500.

Rodríguez-Rojas, A., Makarova, O., Müller, U. & Rolff, J. 2015. Cationic peptides facilitate iron-induced mutagenesis in bacteria. PLoS Genetics 11(10): 1-16.

Rungin, S., Indananda, C., Suttiviriya, P., Kruasuwan, W., Jaemsaeng, R. & Thamchaipenet, A. 2012. Plant growth enhancing effects by a siderophore-producing endophytic streptomycete isolated from a Thai jasmine rice plant (Oryza sativa L. cv. KDML105). Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology 102(3): 463-472.

Santos, S., Neto, I.F.F., Machado, M.D., Soares, H.M.V.M. & Soares, E.V. 2014. Siderophore production by Bacillus megaterium: Effect of growth phase and cultural conditions. Applied Biochemistry and Biotechnology 172(1): 549-560.

Saravanan, V.S., Subramoniam, S.R. & Raj, S.A. 2004. Assessing in vitro solubilization potential of different zinc solubilizing bacterial (ZSB) isolates. Brazilian Journal of Microbiology 35(1-2): 121-125.

Shakeel, M., Rais, A., Hassan, M.N. & Hafeez, F.Y. 2015. Root associated Bacillus sp. improves growth, yield and zinc translocation for basmati rice (Oryza sativa) varieties. Frontiers in Microbiology 6(NOV): 1-12.

Sinha, A.K., Parli Venkateswaran, B., Tripathy, S.C., Sarkar, A. & Prabhakaran, S. 2018. Effects of growth conditions on siderophore producing bacteria and siderophore production from Indian Ocean sector of Southern Ocean. Journal of Basic Microbiology 59(4): 412-424.

Smith, A.D., Modi, A.R., Sun, S., Dawson, J.H. & Wilks, A. 2015. Spectroscopic determination of distinct heme ligands in outer-membrane receptors PhuR and HasR of Pseudomonas aeruginosa. Biochemistry 54(16): 2601-2612.

Srimathi, K. & Suji, H.A. 2018. Siderophores detection by using blue agar CAS assay methods. International Journal of Scientific Research in Biological Sciences 5(6): 180-185.

Wang, F., Xu, Z., Wang, C., Guo, Z., Yuan, Z., Kang, H., Li, J., Lu, F. & Liu, Y. 2021. Biochemical characterization of a tyrosinase from Bacillus aryabhattai and its application. International Journal of Biological Macromolecules 176: 37-46.

Yu, S., Teng, C., Bai, X., Liang, J., Song, T., Dong, L., Jin, Y. & Qu, J. 2017. Optimization of siderophore production by Bacillus sp. PZ-1 and its potential enhancement of phytoextration of PB from soil. Journal of Microbiology and Biotechnology 27(8): 1500.

 Zhang, J., Wang, H., Huang, Q., Zhang, Y., Zhao, L., Liu, F. & Wang, G. 2020. Four superoxide dismutases of Bacillus cereus 0–9 are non-redundant and perform different functions in diverse living conditions. World Journal of Microbiology and Biotechnology 36(1): 1-12.

^*Corresponding author; email: sylvia@ukm.edu.my