Functional diversity of bacteria in various saline soil plant vegetations around Sialang Buah Coast, North Sumatra, Indonesia

Mariani Sembiring, Juli M. Hutahuruk, Dwi Ningsih Susilowati, Erny Yuniarti, T. Sabrina, Luthfi A. Mahmud Siregar

Abstract

Environmental conditions profoundly influence microbial diversity and activity in soil. For optimal growth, soil microbes face limiting factors such as temperature, moisture, pH, and salinity levels in a given environment. This research aims to identify microorganisms capable of thriving in high-salinity (saline) soil conditions. The study was conducted in the Soil Biology Laboratory at Universitas Sumatera Utara (USU), Indonesia. Soil samples were collected around the Sialang Buah Coast, Serdang Bedagai Regency, North Sumatra, Indonesia. The method employed in this research was random composite sampling taken from three vegetation types: mangrove forests, grasslands, and oil palm plantations, with sample collection locations influenced by tidal fluctuations. Ten sampling points were taken at each location and then composited for each vegetation type. The research findings revealed that there are ten species of bacteria originating from saline soils, and all of them are able to grow on Pikovskaya, Alexandrov, and Jansen media. Among the ten bacteria found, seven species were capable of forming biofilms, namely Pseudomonas aeruginosa, Burkholderia gladioli, Enterobacter cloacae, Brucella ciceri, Achromobacter xylosoxidans, Priestia flexa and Enterobacter quasiroggenkampii.

Keywords

Biofilm; Microbial diversity; Nutrient availability; Salinity; Vegetation types

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References

Abrol, I. P., Yadav, J. S. P., & Massoud, F. I. (1988). Salt-affected soils and their management (Vol. 39). Food & Agriculture Organization (FAO). https://www.fao.org/4/x5871e/x5871e00.htm

Acosta-Motos, J. R., Ortuño, M. F., Bernal-Vicente, A., Diaz-Vivancos, P., Sanchez-Blanco, M. J., & Hernandez, J. A. (2017). Plant Responses to Salt Stress: Adaptive Mechanisms. Agronomy, 7(1), 18. https://doi.org/10.3390/agronomy7010018

Ahemad, M., & Kibret, M. (2014). Mechanisms and applications of plant growth promoting rhizobacteria: Current perspective. Journal of King Saud University - Science, 26(1), 1-20. https://doi.org/10.1016/j.jksus.2013.05.001

Ahmed, M. N., Abdelsamad, A., Wassermann, T., Porse, A., Becker, J., Sommer, M. O. A., . . . Ciofu, O. (2020). The evolutionary trajectories of P. aeruginosa in biofilm and planktonic growth modes exposed to ciprofloxacin: beyond selection of antibiotic resistance. npj Biofilms and Microbiomes, 6(1), 28. https://doi.org/10.1038/s41522-020-00138-8

Ali, S., Charles, T. C., & Glick, B. R. (2014). Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiology and Biochemistry, 80, 160-167. https://doi.org/10.1016/j.plaphy.2014.04.003

Amankwah, S., Abdella, K., & Kassa, T. (2021). Bacterial biofilm destruction: A focused review on the recent use of phage-based strategies with other antibiofilm agents. Nanotechnology, science and applications, 161-177. https://doi.org/10.2147/NSA.S325594

Barnawal, D., Bharti, N., Pandey, S. S., Pandey, A., Chanotiya, C. S., & Kalra, A. (2017). Plant growth-promoting rhizobacteria enhance wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression. Physiologia Plantarum, 161(4), 502-514. https://doi.org/10.1111/ppl.12614

Barraud, N., Kelso, M. J., Rice, S. A., & Kjelleberg, S. (2015). Nitric oxide: a key mediator of biofilm dispersal with applications in infectious diseases. Curr Pharm Des, 21(1), 31-42. https://doi.org/10.2174/1381612820666140905112822

Beauregard, P. B., Chai, Y., Vlamakis, H., Losick, R., & Kolter, R. (2013). <i>Bacillus subtilis</i> biofilm induction by plant polysaccharides. Proceedings of the National Academy of Sciences, 110(17), E1621-E1630. https://doi.org/10.1073/pnas.1218984110

Bharti, N., Barnawal, D., Awasthi, A., Yadav, A., & Kalra, A. (2014). Plant growth promoting rhizobacteria alleviate salinity induced negative effects on growth, oil content and physiological status in Mentha arvensis. Acta Physiologiae Plantarum, 36(1), 45-60. https://doi.org/10.1007/s11738-013-1385-8

Egamberdieva, D., Wirth, S. J., Shurigin, V. V., Hashem, A., & Abd Allah, E. F. (2017). Endophytic Bacteria Improve Plant Growth, Symbiotic Performance of Chickpea (Cicer arietinum L.) and Induce Suppression of Root Rot Caused by Fusarium solani under Salt Stress. Front Microbiol, 8, 1887. https://doi.org/10.3389/fmicb.2017.01887

Ehis-Eriakha, C., Willy-Vidona, C., & Akemu, S. (2022). Isolation and Molecular Characterization of Diazotrophic Bacteria in Arable Soils. International Journal of Innovative Science and Research Technology, 7(4), 1436-1443. https://doi.org/10.5281/zenodo.6596587

Glick, B. R. (2014). Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiological Research, 169(1), 30-39. https://doi.org/10.1016/j.micres.2013.09.009

Goodwine, J., Gil, J., Doiron, A., Valdes, J., Solis, M., Higa, A., . . . Sauer, K. (2019). Pyruvate-depleting conditions induce biofilm dispersion and enhance the efficacy of antibiotics in killing biofilms in vitro and in vivo. Scientific Reports, 9(1), 3763. https://doi.org/10.1038/s41598-019-40378-z

Jiao, Y., Zhu, Y., Zeng, S., Wang, S., Chen, J., Zhou, X., & Ma, G. (2023). Characterization of a novel marine microbial uricase from Priestia flexa and evaluation of the effects of CMCS conjugation on its enzymatic properties. Preparative Biochemistry & Biotechnology, 53(7), 816-826. https://doi.org/10.1080/10826068.2022.2145611

Kang, S.-M., Khan, A. L., Waqas, M., You, Y.-H., Kim, J.-H., Kim, J.-G., . . . Lee, I.-J. (2014). Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. Journal of Plant Interactions, 9(1), 673-682. https://doi.org/10.1080/17429145.2014.894587

Kaushal, M. (2020). Insights Into Microbially Induced Salt Tolerance and Endurance Mechanisms (STEM) in Plants [Review]. Frontiers in Microbiology, 11. https://doi.org/10.3389/fmicb.2020.01518

Khan, M. A., Asaf, S., Khan, A. L., Jan, R., Kang, S.-M., Kim, K.-M., & Lee, I.-J. (2019). Rhizobacteria AK1 remediates the toxic effects of salinity stress via regulation of endogenous phytohormones and gene expression in soybean. Biochemical Journal, 476(16), 2393-2409. https://doi.org/10.1042/bcj20190435

Kim, K., Samaddar, S., Chatterjee, P., Krishnamoorthy, R., Jeon, S., & Sa, T. (2019). Structural and functional responses of microbial community with respect to salinity levels in a coastal reclamation land. Applied Soil Ecology, 137, 96-105. https://doi.org/10.1016/j.apsoil.2019.02.011

Lade, H., Park, J. H., Chung, S. H., Kim, I. H., Kim, J.-M., Joo, H.-S., & Kim, J.-S. (2019). Biofilm Formation by Staphylococcus aureus Clinical Isolates is Differentially Affected by Glucose and Sodium Chloride Supplemented Culture Media. Journal of Clinical Medicine, 8(11), 1853. https://doi.org/10.3390/jcm8111853

Liu, F., Xing, S., Ma, H., Du, Z., & Ma, B. (2013). Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Applied Microbiology and Biotechnology, 97(20), 9155-9164. https://doi.org/10.1007/s00253-013-5193-2

Machado, R. M. A., & Serralheiro, R. P. (2017). Soil Salinity: Effect on Vegetable Crop Growth. Management Practices to Prevent and Mitigate Soil Salinization. Horticulturae, 3(2), 30. https://doi.org/10.3390/horticulturae3020030

Merritt, J. H., Kadouri, D. E., & O'Toole, G. A. (2006). Growing and Analyzing Static Biofilms. Current Protocols in Microbiology, 00(1), 1B.1.1-1B.1.17. https://doi.org/10.1002/9780471729259.mc01b01s00

Misra, S., Dixit, V. K., Khan, M. H., Kumar Mishra, S., Dviwedi, G., Yadav, S., . . . Singh Chauhan, P. (2017). Exploitation of agro-climatic environment for selection of 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase producing salt tolerant indigenous plant growth promoting rhizobacteria. Microbiological Research, 205, 25-34. https://doi.org/10.1016/j.micres.2017.08.007

Mohamed, D. J., & Martiny, J. B. H. (2011). Patterns of fungal diversity and composition along a salinity gradient. The ISME Journal, 5(3), 379-388. https://doi.org/10.1038/ismej.2010.137

Muhammad, M. H., Idris, A. L., Fan, X., Guo, Y., Yu, Y., Jin, X., . . . Huang, T. (2020). Beyond Risk: Bacterial Biofilms and Their Regulating Approaches [Review]. Frontiers in Microbiology, 11. https://doi.org/10.3389/fmicb.2020.00928

Naher, U. A., Othman, R., & Panhwar, Q. A. (2013). Beneficial effects of mycorrhizal association for crop production in the tropics - a review. International Journal of Agriculture and Biology, 15, 1021-1028. https://www.fspublishers.org/published_papers/625_..pdf

Naher, U. A., Panhwar, Q. A., Othman, R., Ismail, M. R., & Berahim, Z. (2016). Biofertilizer as a supplement of chemical fertilizer for yield maximization of rice. Journal of Agriculture Food and Development, 2(0), 16-22.

Navarro-Torre, S., Barcia-Piedras, J. M., Mateos-Naranjo, E., Redondo-Gómez, S., Camacho, M., Caviedes, M. A., . . . Rodríguez-Llorente, I. D. (2017). Assessing the role of endophytic bacteria in the halophyte Arthrocnemum macrostachyum salt tolerance. Plant Biology, 19(2), 249-256. https://doi.org/10.1111/plb.12521

Olanrewaju, O. S., Glick, B. R., & Babalola, O. O. (2017). Mechanisms of action of plant growth promoting bacteria. World Journal of Microbiology and Biotechnology, 33(11), 197. https://doi.org/10.1007/s11274-017-2364-9

Panhwar, Q. A., Naher, U. A., Radziah, O., Shamshuddin, J., & Razi, I. M. (2014). Bio-Fertilizer, Ground Magnesium Limestone and Basalt Applications May Improve Chemical Properties of Malaysian Acid Sulfate Soils and Rice Growth. Pedosphere, 24(6), 827-835. https://doi.org/10.1016/S1002-0160(14)60070-9

Paul, D. (2013). Osmotic stress adaptations in rhizobacteria. Journal of Basic Microbiology, 53(2), 101-110. https://doi.org/10.1002/jobm.201100288

Ponomareva, A. L., Buzoleva, L. S., & Bogatyrenko, E. A. (2018). Abiotic Environmental Factors Affecting the Formation of Microbial Biofilms. Biology Bulletin, 45(5), 490-496. https://doi.org/10.1134/S106235901805014X

Rath, K. M., Fierer, N., Murphy, D. V., & Rousk, J. (2019). Linking bacterial community composition to soil salinity along environmental gradients. The ISME Journal, 13(3), 836-846. https://doi.org/10.1038/s41396-018-0313-8

Rodríguez-Blanco, A., Sicardi, M., & Frioni, L. (2015). Plant genotype and nitrogen fertilization effects on abundance and diversity of diazotrophic bacteria associated with maize (Zea mays L.). Biology and Fertility of Soils, 51(3), 391-402. https://doi.org/10.1007/s00374-014-0986-8

Rumbaugh, K. P., & Sauer, K. (2020). Biofilm dispersion. Nature Reviews Microbiology, 18(10), 571-586. https://doi.org/10.1038/s41579-020-0385-0

Sembiring, M., & Sabrina, T. (2022a). Diversity of phosphate solubilizing bacteria and fungi from andisol soil affected by the eruption of Mount Sinabung, North Sumatra, Indonesia. Biodiversitas Journal of Biological Diversity, 23(2). https://doi.org/10.13057/biodiv/d230216

Sembiring, M., & Sabrina, T. (2022b). Diversity of potassium solving microbes on andisol soil affected by the eruption of Mount Sinabung, North Sumatra, Indonesia. Biodiversitas Journal of Biological Diversity, 23(4). https://doi.org/10.13057/biodiv/d230406

Seshachala, U., & Tallapragada, P. (2012). Phosphate Solubilizers from the Rhizosphere of Piper nigrum L. in Karnataka, India. Chilean journal of agricultural research, 72, 397-403. https://doi.org/10.4067/S0718-58392012000300014

Setia, R., Gottschalk, P., Smith, P., Marschner, P., Baldock, J., Setia, D., & Smith, J. (2013). Soil salinity decreases global soil organic carbon stocks. Science of The Total Environment, 465, 267-272. https://doi.org/10.1016/j.scitotenv.2012.08.028

Setia, R., Marschner, P., Baldock, J., Chittleborough, D., Smith, P., & Smith, J. (2011). Salinity effects on carbon mineralization in soils of varying texture. Soil Biology and Biochemistry, 43(9), 1908-1916. https://doi.org/10.1016/j.soilbio.2011.05.013

Shahbaz, M., & Ashraf, M. (2013). Improving Salinity Tolerance in Cereals. Critical Reviews in Plant Sciences, 32(4), 237-249. https://doi.org/10.1080/07352689.2013.758544

Sharma, S., Kulkarni, J., & Jha, B. (2016). Halotolerant Rhizobacteria Promote Growth and Enhance Salinity Tolerance in Peanut [Original Research]. Frontiers in Microbiology, 7. https://doi.org/10.3389/fmicb.2016.01600

Sharma, S. B., Sayyed, R. Z., Trivedi, M. H., & Gobi, T. A. (2013). Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus, 2(1), 587. https://doi.org/10.1186/2193-1801-2-587

Shrivastava, P., & Kumar, R. (2015). Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi Journal of Biological Sciences, 22(2), 123-131. https://doi.org/10.1016/j.sjbs.2014.12.001

Sianturi, J. K., Sembiring, M., & Guchi, H. (2021). Isolation of potassium solubilizing bacteria in Andisol soil affected by the eruption of Sinabung. IOP Conference Series: Earth and Environmental Science, 782(4), 042070. https://doi.org/10.1088/1755-1315/782/4/042070

Singh, R. P., Shelke, G. M., Kumar, A., & Jha, P. N. (2015). Biochemistry and genetics of ACC deaminase: a weapon to "stress ethylene" produced in plants. Front Microbiol, 6, 937. https://doi.org/10.3389/fmicb.2015.00937

Soni, A., Rokad, S., & Sharma, P. (2013). Screening of efficient halotolerant phosphate solubilizing bacteria and their effect on seed germination under saline conditions. Journal of Scientific and Innovative Research, 2(5), 932-937. http://www.jsirjournal.com/Vol2Issue5013.pdf

Sorty, A. M., Meena, K. K., Choudhary, K., Bitla, U. M., Minhas, P. S., & Krishnani, K. K. (2016). Effect of Plant Growth Promoting Bacteria Associated with Halophytic Weed (Psoralea corylifolia L) on Germination and Seedling Growth of Wheat Under Saline Conditions. Applied Biochemistry and Biotechnology, 180(5), 872-882. https://doi.org/10.1007/s12010-016-2139-z

Srinivasan, R., Santhakumari, S., Poonguzhali, P., Geetha, M., Dyavaiah, M., & Xiangmin, L. (2021). Bacterial Biofilm Inhibition: A Focused Review on Recent Therapeutic Strategies for Combating the Biofilm Mediated Infections [Review]. Frontiers in Microbiology, 12. https://doi.org/10.3389/fmicb.2021.676458

Tan, W., Wang, J., Bai, W., Qi, J., & Chen, W. (2020). Soil bacterial diversity correlates with precipitation and soil pH in long-term maize cropping systems. Scientific Reports, 10(1), 6012. https://doi.org/10.1038/s41598-020-62919-7

Toyofuku, M., Inaba, T., Kiyokawa, T., Obana, N., Yawata, Y., & Nomura, N. (2016). Environmental factors that shape biofilm formation. Bioscience, Biotechnology, and Biochemistry, 80(1), 7-12. https://doi.org/10.1080/09168451.2015.1058701

Wong, V. N. L., Greene, R. S. B., Dalal, R. C., & Murphy, B. W. (2010). Soil carbon dynamics in saline and sodic soils: a review. Soil Use and Management, 26(1), 2-11. https://doi.org/10.1111/j.1475-2743.2009.00251.x

Yang, C., & Sun, J. (2020). Soil Salinity Drives the Distribution Patterns and Ecological Functions of Fungi in Saline-Alkali Land in the Yellow River Delta, China [Original Research]. Frontiers in Microbiology, 11. https://doi.org/10.3389/fmicb.2020.594284

Yin, W., Wang, Y., Liu, L., & He, J. (2019). Biofilms: The Microbial “Protective Clothing” in Extreme Environments. International Journal of Molecular Sciences, 20(14), 3423. https://doi.org/10.3390/ijms20143423

Zea, L., McLean, R. J. C., Rook, T. A., Angle, G., Carter, D. L., Delegard, A., . . . Velez Justiniano, Y. A. (2020). Potential biofilm control strategies for extended spaceflight missions. Biofilm, 2, 100026. https://doi.org/10.1016/j.bioflm.2020.100026

Zebua, A. C., Guchi, H., & Sembiring, M. (2020). Isolation of non-symbiotic Nitrogen-fixing bacteria on andisol land affected by Sinabung eruption. IOP Conference Series: Earth and Environmental Science, 454(1), 012167. https://doi.org/10.1088/1755-1315/454/1/012167

Zhao, K., Penttinen, P., Zhang, X., Ao, X., Liu, M., Yu, X., & Chen, Q. (2014). Maize rhizosphere in Sichuan, China, hosts plant growth promoting Burkholderia cepacia with phosphate solubilizing and antifungal abilities. Microbiological Research, 169(1), 76-82. https://doi.org/10.1016/j.micres.2013.07.003

Zhao, Q., Bai, J., Gao, Y., Zhao, H., Zhang, G., & Cui, B. (2020). Shifts in the soil bacterial community along a salinity gradient in the Yellow River Delta. Land Degradation & Development, 31(16), 2255-2267. https://doi.org/10.1002/ldr.3594

Zhao, S., Liu, J.-J., Banerjee, S., Zhou, N., Zhao, Z.-Y., Zhang, K., & Tian, C.-Y. (2018). Soil pH is equally important as salinity in shaping bacterial communities in saline soils under halophytic vegetation. Scientific Reports, 8(1), 4550. https://doi.org/10.1038/s41598-018-22788-7

Zou, M., & Liu, D. (2020). Effects of carbon sources and temperature on the formation and structural characteristics of food-related Staphylococcus epidermidis biofilms. Food Science and Human Wellness, 9(4), 370-376. https://doi.org/10.1016/j.fshw.2020.05.007

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