Antimicrobial and plant growth-promoting activity of Bacillus subtilis isolated from mangrove soil.
Article Sidebar
Main Article Content
Abstract
Bacillus subtilis strain was isolated from mangrove soil and evaluated for its biocontrol and plant growth-promoting potential. The strain exhibited key traits including indole-3-acetic acid (IAA) production, biofilm formation, and tolerance to high salinity (up to 10% NaCl). It showed broad-spectrum antimicrobial activity, inhibiting the growth of both fungal and bacterial pathogens. Antifungal activity was demonstrated using well-diffusion and dual-overlay assays, effectively suppressing Aspergillus niger, Rhizopus arrhizus, and Mucor mucedo. Antibacterial effects were observed against Escherichia coli, Bacillus albus, and Xanthomonas sp. The cell-free supernatant of the isolate significantly inhibited fungal spore germination, as confirmed by turbidity assays. LC-MS analysis of the supernatant revealed the presence of antimicrobial compounds, including palmitic acid derivatives, fatty acid amides, and pyridine-based molecules. Bio-priming wheat seeds with this Bacillus sp. led to enhanced seed germination and increased shoot and root lengths, especially under saline soil conditions. These findings highlight the potential of this mangrove-derived B. subtilis strain as a promising bioinoculant for sustainable agriculture, particularly in salt-affected environments.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
Abuhena, M., Al-Rashid, J., Azim, M. F., Khan, M. N. M., Kabir, M. G., Barman, N. C., Rasul, N. M., Akter, S. and Huq, M. A. (2022) Optimization of industrial (3000 L) production of Bacillus subtilis CW-S and its novel application for minituber and industrial-grade potato cultivation. Scientific Reports, 12:11153.
Afsharmanesh, H., Ahmadzadeh, M., Javan-Nikkhah, M. and Behboudi, K. (2014). Improvement in biocontrol activity of Bacillus subtilis UTB1 against Aspergillus flavus using gamma-irradiation. Crop Protection, 60:83-92.
Aktar, Md.W., Sengupta, D. and Chowdhury, A. (2009) Impact of pesticides use in agriculture: their benefits and hazards. Interdisciplinary Toxicology, 2:1-12.
Amri, M., Rjeibi, M. R., Gatrouni, M., Mateus, D. M. R., Asses, N., Pinho, H. J. O. and Abbes, C. (2023) Isolation, Identification, and Characterization of Phosphate-Solubilizing Bacteria from Tunisian Soils. Microorganisms, 11:783.
Aryani, A., Suprayitno, E., Sasmito, B. B. and Hardoko, H. (2020). Characterization and identification of charcoal of inedible Kerandang fish (Channa pleurophthalmus Blkr) body parts and potential antiallergenic properties. Veterinary World, 13:1480-1486.
Bai, J-R., Wu, Y-P., Elena, G., Zhong, K. and Gao, H. (2019). Insight into the effect of quinic acid on biofilm formed by Staphylococcus aureus. RSC Advances, 9:3938-3945.
Bashan, Y. and Holguin, G. (2002). Plant growth-promoting bacteria: a potential tool for arid mangrove reforestation. Trees, 16:159-166.
Bin Rahman, A. N. M. R. and Zhang, J. (2023). Trends in rice research: 2030 and beyond. Food and Energy Security, 12:390.
Boedeker, W., Watts, M., Clausing, P. and Marquez, E. (2020). The global distribution of acute unintentional pesticide poisoning: estimations based on a systematic review. BMC Public Health, 20:1875.
Boubekri, K., Soumare, A., Mardad, I., Lyamlouli, K., Hafidi, M., Ouhdouch, Y. and Kouisni, L. (2021). The Screening of Potassium- and Phosphate-Solubilizing Actinobacteria and the Assessment of Their Ability to Promote Wheat Growth Parameters. Microorganisms, 9:470.
Cemaloğlu, Ö. Ş., Ogutcu, H. and Hayvalı, Z. (2021). Synthesis, characterization, and antimicrobial activities of novel double-armed benzo-15-crown-5 and their sodium and potassium complexes. Journal of Chemical Research, 45:116-124.
Desbois, A. P. and Smith, V. J. (2010). Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. Applied Microbiology and Biotechnology, 85:1629-1642.
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32:1792-1797.
Elbagory, M., El-Nahrawy, S. and Omara, A. E. D. (2022). Synergistic Interaction between Symbiotic N2 Fixing Bacteria and Bacillus strains to Improve Growth, Physiological Parameters, Antioxidant Enzymes and Ni Accumulation in Faba Bean Plants (Vicia faba) under Nickel Stress. Plants, 11:1812.
Fira, D., Dimkić, I., Berić, T., Lozo, J. and Stanković, S. (2018). Biological control of plant pathogens by Bacillus species. Journal of Biotechnology, 285:44-55.
Guarin, J. R., Martre, P., Ewert, F., Webber, H., Dueri, S., Calderini, D., Reynolds, M., Molero, G., Miralles, D., Garcia, G., Slafer, G., Giunta, F., Pequeno, D. N. L., Stella, T., Ahmed, M., Alderman, P. D., Basso, B., Berger, A. G., Bindi, M., Bracho-Mujica, G., Cammarano, D., Chen, Y., Dumont, B., Rezaei, E. E., Fereres, E., Ferrise, R., Gaiser, T., Gao, Y., Garcia-Vila, M., Gayler, S., Hochman, Z., Hoogenboom, G., Hunt, L. A., Kersebaum, K. C., Nendel, C., Olesen, J. E., Palosuo, T., Priesack, E., Pullens, J. W. M., Rodríguez, A., Rötter, R. P., Ruiz Ramos, M., Semenov, M. A., Senapati, N., Siebert, S., Srivastava, A. K., Stöckle, C., Supit, I., Tao, F., Thorburn, P., Wang, E., Weber, T. K. D., Xiao, L., Zhang, Z., Zhao, C., Zhao, J., Zhao, Z., Zhao, Y., Zhu, Y. and Asseng, S. (2022). Evidence for increasing global wheat yield potential. Environmental Research Letters, 17:124045.
Gul, S., Javed, S., Azeem, M., Aftab, A., Anwaar, N., Mehmood, T. and Zeshan, B. (2023). Application of Bacillus subtilis for the Alleviation of Salinity Stress in Different Cultivars of Wheat (Tritium aestivum L.). Agronomy, 13:437.
Hashem, A., Tabassum, B. and Abd Allah, E. F. (2019). Bacillus subtilis: A plant-growth promoting rhizobacterium that also impacts biotic stress. Saudi Journal of Biological Sciences, 26:1291-1297.
Islam, S., Mahmud, M. L., Almalki, W. H., Biswas, S., Islam, M. A., Mortuza, M. G., Hossain, M. A., Ekram, M. A.-E., Uddin, M. S., Zaman, S. and Saleh, M. A. (2022). Cell-Free Supernatants (CFSs) from the Culture of Bacillus subtilis Inhibit Pseudomonas sp. Biofilm Formation. Microorganisms, 10:2105.
Jan, F., Arshad, H., Ahad, M., Jamal, A. and Smith, D. L. (2023). In vitro assessment of Bacillus subtilis FJ3 affirms its biocontrol and plant growth promoting potential. Frontiers in Plant Science, 14.
Ji, C., Tian, H., Wang, X., Song, X., Ju, R., Li, H., Gao, Q., Li, C., Zhang, P., Li, J., Hao, L., Wang, C., Zhou, Y., Xu, R., Liu, Y., Du, J. and Liu, X. (2022). Bacillus subtilis HG-15, a Halotolerant Rhizoplane Bacterium, Promotes Growth and Salinity Tolerance in Wheat (Triticum aestivum). BioMed Research International, 2022:9506227.
Jiménez, D. J., Montaña, J. S. and Martínez, M. M. (2011). Characterization of free nitrogen fixing bacteria of the genus Azotobacter in organic vegetable-grown Colombian soils. Brazilian Journal of Microbiology, 42:846-858.
Jumina, J., Nurmala, A., Fitria, A., Pranowo, D., Sholikhah, E. N., Kurniawan, Y. S. and Kuswandi, B. (2018). Monomyristin and Monopalmitin derivatives: synthesis and evaluation as potential antibacterial and antifungal agents. Molecules (Basel, Switzerland), 23:3141.
Kerr, J. R. (1999). Bacterial inhibition of fungal growth and pathogenicity. Microbial Ecology in Health and Disease, 11:129-142.
Khan, M. A., Sahile, A. A., Jan, R., Asaf, S., Hamayun, M., Imran, M., Adhikari, A., Kang, S. M., Kim, K. M. and Lee, I. J. (2021). Halotolerant bacteria mitigate the effects of salinity stress on soybean growth by regulating secondary metabolites and molecular responses. BMC Plant Biology, 21:176.
Khan, S. R., Mahmood, A., Korai, M. A., Ikram, R., Amin, M., Hidayatullah, H., Aslam, M. Z., Afzal, M., Kalhoro, A. A., Khan, A. S., Nabi, G. and Ullah, I. (2021). Effect of different growing media on germination and growth of Terminalia mantaly L. under lath house conditions. (2022). Effect of different growing media on germination and growth of Terminalia mantaly L. under lath house conditions. Bioscience Research, 18:3310-3315.
Lastochkina, O., Garshina, D., Ivanov, S., Yuldashev, R., Khafizova, R., Allagulova, C., Fedorova, K., Avalbaev, A., Maslennikova, D. and Bosacchi, M. (2020). Seed priming with endophytic Bacillus subtilis modulates physiological responses of two different Triticum aestivum L. Cultivars under Drought Stress. Plants, 9:1810.
Lotfy, W. A., Mostafa, S. W., Adel, A. A. and Ghanem, K. M. (2018). Production of di-(2-ethylhexyl) phthalate by Bacillus subtilis AD35: Isolation, purification, characterization and biological activities. Microbial Pathogenesis, 124:89-100.
Louden, B. C., Haarmann, D. and Lynne, A. M. (2011). Use of Blue Agar CAS Assay for Siderophore Detection. Journal of Microbiology & Biology Education: JMBE, 12:51-53.
Menendez, E. and Garcia-Fraile, P. (2017). Plant probiotic bacteria: solutions to feed the world. AIMS Microbiology, 3:502-524.
Metzler, A. (2016). Developing a crystal violet assay to quantify biofilm production capabilities of Staphylococcus aureus. Agricultural and Food Sciences.
Monteiro, S. M., Clemente, J. J., Henriques, A. O., Gomes, R. J., Carrondo, M. J. and Cunha, A. E. (2005). A procedure for high-yield spore production by Bacillus subtilis. Biotechnology Progress, 21:1026-1031.
Olanrewaju, O.S., Glick, B.R. and Babalola, O.O. (2017) Mechanisms of action of plant growth promoting bacteria. World Journal of Microbiology & Biotechnology, 33:197.
Pallavi, P., Mishra, R. K., Sahu, P. K., Mishra, V., Jamal, H., Varma, A. and Tripathi, S. (2023). Isolation and characterization of halotolerant plant growth promoting rhizobacteria from mangrove region of Sundarbans, India for enhanced crop productivity. Frontiers in Plant Science, 14.
Panigrahi, S., Mohanty, S. and Rath, C. C. (2020). Characterization of endophytic bacteria Enterobacter cloacae MG00145 isolated from Ocimum sanctum with Indole Acetic Acid (IAA) production and plant growth promoting capabilities against selected crops. South African Journal of Botany, 134:17-26.
Peng, Q., Yang, J., Wang, Q., Suo, H., Hamdy, A. M. and Song, J. (2023). Antifungal Effect of Metabolites from a New Strain Lactiplantibacillus Plantarum LPP703 Isolated from Naturally Fermented Yak Yogurt. Foods, 12:181.
Sarker, A. and Al-Rashid, J. (2013). Analytical Protocol for determination of Indole 3 acetic acid (IAA) production by Plant Growth Promoting Bacteria (PGPB). Technical Report No. 012.
Satapute, P., Olekar, H. S., Shetti, A., Kulkarni, A. G., Hiremath, G., Patagundi, B. I., Shivsharan, C. T. and Kaliwal, B. B. (2012). Isolation and characterization of nitrogen fixing Bacillus subtilis strain as-4 from agricultural soil. International Journal of Recent Scientific Research, 3:762-765.
Savary, S., Willocquet, L., Pethybridge, S. J., Esker, P., McRoberts, N. and Nelson, A. (2019). The global burden of pathogens and pests on major food crops. Nature Ecology & Evolution, 3:430-439.
Shakhatreh, M. A. K., Al-Smadi, M. L., Khabour, O. F., Shuaibu, F. A., Hussein, E. I. and Alzoubi, K. H. (2016). Study of the antibacterial and antifungal activities of synthetic benzyl bromides, ketones, and corresponding chalcone derivatives. Drug Design, Development and Therapy, 10:3653-3660.
Sharma, A., Kumar, V., Shahzad, B., Tanveer, M., Sidhu, G. P. S., Handa, N., Kohli, S. K., Yadav, P., Bali, A. S., Parihar, R. D., Dar, O. I., Singh, K., Jasrotia, S., Bakshi, P., Ramakrishnan, M., Kumar, S., Bhardwaj, R. and Thukral, A. K. (2019). Worldwide pesticide usage and its impacts on ecosystem. SN Applied Sciences, 1:1446.
S Shoaib, A., Ali, H., Javaid, A. and Awan, Z. A. (2020). Contending charcoal rot disease of mungbean by employing biocontrol Ochrobactrum ciceri and zinc. Physiology and Molecular Biology of Plants, 26:1385-1397.
Somashekaraiah, R., Shruthi, B., Deepthi, B. V. and Sreenivasa, M. Y. (2019). Probiotic Properties of Lactic Acid Bacteria Isolated From Neera: A Naturally Fermenting Coconut Palm Nectar. Frontiers in Microbiology, 10.
Song, P., Zhao, B., Sun, X., Li, L., Wang, Z., Ma, C. and Zhang, J. (2023). Effects of Bacillus subtilis HS5B5 on Maize Seed Germination and Seedling Growth under NaCl Stress Conditions. Agronomy, 13:1874.
Su, Y., Liu, C., Fang, H. and Zhang, D. (2020). Bacillus subtilis: a universal cell factory for industry, agriculture, biomaterials and medicine. Microbial Cell Factories, 19:173.
Suyama, K., Suganuma, O. and Adachi, S. (1981). Quaternary pyridinium compounds formed by reaction of primary amines with alkanals and their antimicrobial activities. Agricultural and Biological Chemistry, 45:1535-1539.
Tamura, K., Stecher, G. and Kumar, S. (2021). MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38:3022-3027.
US EPA, O. (2015). Human health issues related to pesticides. US Environmental Protection Agency. Retrieved from https://www.epa.gov/pesticide-science-and-assessing-pesticide-risks/human-health-issues-related-pesticides
Wang, A., Guan, C., Wang, T., Mu, G. and Tuo, Y. (2023). Changes in intracellular and extracellular metabolites of mixed lactobacillus strains enhance inhibition of pathogenic bacterial growth and lipopolysaccharide-induced alleviation of RAW264.7 Cellular Inflammation. Probiotics and Antimicrobial Proteins, 17:175-192.
Zhao, S., Hao, X., Yang, F., Wang, Y., Fan, X. and Wang, Y. (2022). Antifungal activity of Lactobacillus plantarum ZZUA493 and its application to extend the shelf life of Chinese steamed buns. Foods, 11:195.
Zhou, Q., Xie, Z., Wu, D., Liu, L., Shi, Y., Li, P. and Gu, Q. (2022). The Effect of Indole-3-Lactic Acid from Lactiplantibacillus plantarum ZJ316 on Human Intestinal Microbiota In Vitro. Foods, 11:3302.
Ziklo, N., Bibi, M., and Salama, P. (2021). The antimicrobial mode of action of maltol and its synergistic efficacy with selected cationic surfactants. Cosmetics, 8:86.