Using urease-producing bacteria Enterobacter cloacae and Corynebacterium glutamicum for stabilizing sandy soil and reducing wind erosion

Document Type : Complete scientific research article

Authors

1 PhD student, Department of Soil Science, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran.

2 Professor, Department of Soil Science, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran.

3 Department of Soil Sciecne, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran.

Abstract

Background and Objectives: Soil is a reservoir of millions of microorganisms, most of which have beneficial effects on agriculture, soil health, and soil protection against erosive forces. Some soil bacteria have the ability to produce the enzyme urease, which, by altering the concentration of hydrogen ions and producing bicarbonate ions in the presence of calcium, leads to the precipitation of calcium carbonate. It is possible to increase soil resistance against wind forces using biotechnological methods. In this study, the ability of two bacteria, Enterobacter cloacae and Corynebacterium glutamicum, to produce urease and their efficiency in increasing soil resistance and reducing wind erosion was investigated.

Materials and Methods: Sandy soil was collected from a critical wind erosion area in southeast Ahvaz and placed in trays with dimensions of 50×30×3 cm. Fresh cultures of each of bacteria, E. cloacae and C. glutamicum, were separately centrifuged, and the microbial cells were formed into pellets. The supernatant was discarded, and the microbial cells were re-suspended in physiological serum. The bacterial suspension was sprayed onto the trays containing the treated soil to achieve a bacterial population of 5 ×106 CFU/g. The different molar ratios of the chemical solution (urea: calcium chloride, including 1:1, 1:2, and 1:2) were sprayed to the soil surface. The experiment was conducted in a factorial design within a completely randomized design. The factors included different levels of urea: calcium chloride (no urea and calcium chloride, 1:1 ratio, 1:2 ratio, and 1:3 ratio of urea and calcium chloride) and bacterial inoculation (no bacteria, a mixture of the two bacteria, E. cloacae, and C. glutamicum). The samples were maintained under environmental conditions with moisture content 70-75% of field capacity for 60 days. Before measurements, the soil samples were dried at room temperature; then, some soil properties, including soil loss in a wind tunnel, erodible fraction, mean weight diameter of soil aggregates, penetration resistance, and shear strength of the soil, were measured.

Results: The two bacteria used had the ability to produce urease. The results showed that the interaction effect of bacteria and the ratio of urea:calcium chloride on the measured characteristics was significant. The lowest soil loss in the wind tunnel was related to the treatment with a mixture of the two bacteria, followed by E. cloacae with the application of a urea to calcium chloride ratio of 1:2. The highest amount was measured in the treatment without bacterial inoculation and without adding urea and calcium chloride. The mean weight diameter of soil aggregates in the treatment without bacteria, with C. glutamicum, E. cloacae, and a mixture of the two bacteria at a 2:1 urea to calcium chloride ratio was 1.04, 3.79, 3.34, and 3.90 mm, respectively. The lowest amount of the erosion-sensitive fraction in the treatment without bacteria, with C. glutamicum, E. cloacae, and a mixture of the two bacteria at a 2:1 urea to calcium chloride ratio was measured at 98.7%, 82.68%, 86.92%, and 81.47%, respectively.
Conclusion: The results showed that using a mixture of the two bacteria or using E. cloacae and a 1:2 ratio of urea: calcium chloride cement solution helped increase soil resistance against wind erosion forces. The increase in soil penetration resistance and shear strength with the treatments is likely due to the lower amount of the erosion-sensitive fraction and the larger MWD in the soil.

Keywords

Main Subjects


  1.  1.Maleki, M., Ebrahimi, S., Asadzadeh, F. & Emami Tabrizi, M. (2016). Performance of microbial-induced carbonate precipitation on wind erosion control of sandy soil. International Journal of Environmental Science and Technology, 13, 937-944. doi: 10.1007/s13762-015-0921-z

    1. Nikseresht, F., Landi, A., Sayyad, G., Ghezelbash, G.R. & Schulin, R. (2020). Sugarecane molasse and vinasse added as microbial growth substrates increase calcium carbonate content, surface stability and resistance against wind erosion of desert soils. Journal of Environmental Management, 268, p.110639. doi: 10.1016/j.jenvman.2020.110639
    2. Keramat, A., Marivani, B., & Samsami, M. (2011). Climatic change, drought and dust crisis in Iran. WASET 6, 3–10.
    3. Broomandi, P., Dabir, B., Bonakdarpour, B., & Rashidi, Y. (2017). Identification of the sources of dust storms in the City of Ahvaz by HYSPLIT. Pollution, 3(2), 341–348. doi: 10.7508/PJ.2017.02. 015
    4. Anderson, J., Bang, S., Bang, S.S., Lee, S.J., Choi, S.R. & Dho, N.Y. (2014). Reduction of wind erosion potential using microbial calcite and soil fibers. In Geo-Congress 2014: Geo-characterization and Modeling for Sustainability(pp. 1664-1673). Doi: 10.1061/9780784413272.163
    5. Goudie, A.S., & Middleton, N.J. 2006. Desert dust in the global system. Springer, NewYork, USA.
    6. Gadi, V.K., Bordoloi, S., Garg, A., Kobayashi, Y., & Sahoo, L., (2016). Improving and correcting unsaturated soil hydraulic properties with plant parameters for agriculture and bioengineered slopes. Rhizosphere, 1, 58-78. doi:10.1016/j.rhisph.2016.07.003
    7. Karol, R.H., (2003). Chemical grouting and soil stabilization. Marcel Dekker, New York, USA.
    8. Deléglise, C., Loucougaray, G., & Alard, D. (2011). Effects of grazing exclusion on the spatial variability of subalpine plant communities: a multiscale approach. Basic and Applied Ecology, 12(7), pp.609-619. doi.org/10.1016/j.baae.2011.08.006
    9. Verdoodt, A., Mureithi, S.M., Ye, L., & Van Ranst, E. (2009). Chronosequence analysis of two enclosure management strategies in degraded rangeland of semi-arid Kenya. Agriculture, ecosystems & environment, 129(1-3), 332-339. doi: 10.1016/j.agee.2008.10.006.
    10. Zomorodian, S.M.A., Ghaffari, H., & O'Kelly, B.C. (2019). Stabilisation of crustal sand layer using biocementation technique for wind erosion control. Aeolian Research, 40, 34-41. doi: 10.1016/j.aeolia.2019.06.001.
    11. Meyer, F.D., Bang, S., Min, S., Stetler, L.D., & Bang, S.S. (2011). Microbiologically-induced soil stabilization: application of Sporosarcina pasteurii for fugitive dust control. In Geo-frontiers 2011: Advances in Geotechnical Engineering(pp. 4002-4011). doi: 10.1061/41165(397)409.
    12. Sharma, M., Satyam, N., & Reddy, K.R. (2021a). Rock-like behavior of biocemented sand treated under non-sterile environment and various treatment conditions. Journal of Rock Mechanics and Geotechnical Engineering, 13(3), 705-716. doi: 10.1016/j.jrmge.2020.11.006
    13. Sun, X., Miao, L., Tong, T., & Wang, C. (2019). Study of the effect of temperature on microbially induced carbonate precipitation. Acta Geotechnica, 14, 627-638. doi: 10.1007/s11440-018-0758-y
    14. Chou, C.W., Seagren, E.A., Aydilek, A.H., & Lai, M. (2011). Biocalcification of sand through ureolysis. Journal of Geotechnical and Geoenvironmental Engineering, 137(12), 1179-1189. doi: 10.1061/(ASCE)GT.1943-5606.0000532.
    15. Tiwari, N., Satyam, N., & Sharma, M. (2021). Micro-mechanical performance evaluation of expansive soil biotreated with indigenous bacteria using MICP method. Scientific Reports, 11(1), p.10324. doi: 10.1038/s41598-021-89687-2
    16. Whiffin, V.S., Van Paassen, L.A., & Harkes, M.P. (2007). Microbial carbonate precipitation as a soil improvement technique. Geomicrobiology Journal, 24(5), 417-423.doi: 10.1080/01490450701436505
    17. Al-Thawadi, S., (2008). High strength in-situ biocementation of soil by calcite precipitating locally isolated ureolytic bacteria (Doctoral dissertation, Murdoch University).
    18. Sharma, M., Satyam, N., and Reddy, K.R., (2021b). Hybrid bacteria mediated cemented sand: Microcharacterization, permeability, strength, shear wave velocity, stress-strain, and durability. International Journal of Damage Mechanics, 30(4), 618-645. doi: 10.1177/1056789521991196
    19. Moravej, S., Habibagahi, G., Nikooee, E. and Niazi, A., (2018). Stabilization of dispersive soils by means of biological calcite precipitation. Geoderma, 315, 130-137. doi:10.1016/j.geoderma.2017.11.037.
    20. Bu, C., Wen, K., Liu, S., Ogbonnaya, U., & Li, L., (2018). Development of bio-cemented constructional materials through microbial induced calcite precipitation. Materials and Structures, 51, 1-11. doi: 10.1617/s11527-018-1157-4.
    21. Poulsen, T.G., Cai, W., & Garg, A. (2020). Water evaporation from cracked soil under moist conditions as related to crack properties and near‐surface wind speed. European Journal of Soil Science, 71(4), 627-640. doi:10.1111/ejss.12926
    22. Mujah, D., Shahin, M.A., & Cheng, L. (2017). State-of-the-art review of biocementation by microbially induced calcite precipitation (MICP) for soil stabilization. Geomicrobiology Journal, 34(6), 524-537. doi: 10.1080/01490451.2016.1225866.
    23. Liang, S., Chen, J., Niu, J., Gong, X., & Feng, D. (2020). Using recycled calcium sources to solidify sandy soil through microbial induced carbonate precipitation. Marine Georesources & Geotechnology, 38(4), 393-399. doi:10.1080/1064119X.2019.1575939
    24. Choi, S.G., Chu, J., Brown, R.C., Wang, K., & Wen, Z. (2017). Sustainable biocement production via microbially induced calcium carbonate precipitation: Use of limestone and acetic acid derived from pyrolysis of lignocellulosic biomass. ACS Sustainable Chemistry & Engineering, 5(6), 5183-5190. doi:10.1021/acssuschemeng.7b00521
    25. Gowthaman, S., Nawarathna, T.H.K., Nayanthara, P.G.N., Nakashima, K., & Kawasaki, S. (2021). The amendments in typical microbial induced soil stabilization by low-grade chemicals, biopolymers and other additives: A review. Building Materials for Sustainable and Ecological Environment, 49-72.doi: 10.1007/978-981-16-1706-5_4
    26. Dargahian, F., Loftinasabasl, S., & Khosroshahi, M. 2018. Analysis of the role of internal dust sources in creating critical conditions in Ahvaz with an emphasis on the southeastern area. Iranian Journal of Forest and Range Protection Research, 16(32): 157-170. doi:10.22092/ijfrpr.2018.110809.1277
    27. Rajasekar, A., Zhao, C., Wu, S., Murava, R.T., & Wilkinson, S. 2024. Synergistic biocementation: harnessing Comamonas and Bacillus ureolytic bacteria for enhanced sand stabilization. World Journal of Microbiology and Biotechnology40(7), p.229.doi:10.1007/s11274-024-04038-3
    28. Harkes, M.P., Van Paassen, L.A., Booster, J.L., Whiffin, V.S., & van Loosdrecht, M.C., (2010). Fixation and distribution of bacterial activity in sand to induce carbonate precipitation for ground reinforcement. Ecological Engineering36(2), 112-117. doi:10.1016/j.ecoleng.2009.01.004
    29. Whiffin, V.S., (2004). Microbial CaCO3 precipitation for the production of biocement (Doctoral dissertation, Murdoch University).
    30. Sarikhani, M.R., & Moradi, Sh. (2015). Measurement of urease activity of several microbial species by electrical conductivity and Nessler's method. 14th Iranian Soil Science Congress. Rafsanjan.
    31. Katra, I. (2020). Soil erosion by wind and dust emission in semi-arid soils due to agricultural activities. Agronomy, 10(1): 89. doi:10.3390/agronomy10010089
    32. Lapierre, F.M. and Huber, R., 2024. Revisiting the urease production of MICP-relevant bacterium Sporosarcina pasteurii during cultivation. Biocatalysis and Agricultural Biotechnology55, p.102981. doi:10.1016/j.bcab.2023.102981
    33. 34. Mazzei, L., Musiani, F. and Ciurli, S., 2020. The structure-based reaction mechanism of urease, a nickel dependent enzyme: tale of a long debate. JBIC Journal of Biological Inorganic Chemistry25(6), 829-845. doi:1007/s00775-020-01808-w
    34. Dhami, N.K., Reddy, M.S., & Mukherjee, A. (2013) Biomineralization of calcium carbonate polymorphs by the bacterial strains isolated from calcareous sites. Journal of Microbiology & Biotechnology, 23:707–714.doi:10.4014/jmb.1212.11087
    35. Dhami, N.K., Reddy, M.S., & Mukherjee, A. (2014) Synergistic role of bacterial urease and carbonic anhydrase in carbonate mineralization. Applied Biochemistry & Biotechnology, 172:2552–2561.doi:10.1007/s12010-013-0694-0
    36. Achal, V. and Pan, X., 2014. Influence of calcium sources on microbially induced calcium carbonate precipitation by Bacillus sp. CR2. Applied biochemistry and biotechnology173, pp.307-317. doi:10.1007/s12010-014-0842-1
    37. Anbu, P., Kang, C.H., Shin, Y.J. and So, J.S., 2016. Formations of calcium carbonate minerals by bacteria and its multiple applications. Springerplus5, pp.1-26.
    38. McConnaughey, T.A., & Whelan, J.F. (1997). Calcification generates protons for nutrient and bicarbonate uptake. Earth-Science Reviews42(1-2), 95-117.
    39. Hammes, F., Boon, N., de Villiers, J., Verstraete, W., & Siciliano, S.D. (2003). Strain-specific ureolytic microbial calcium carbonate precipitation. Applied and environmental microbiology69(8), 4901-4909. doi: 10.1128/AEM.69.8.4901-4909.2003
    40. Warthmann, R., Van Lith, Y., Vasconcelos, C., McKenzie, J.A., & Karpoff, A.M. (2000). Bacterially induced dolomite precipitation in anoxic culture experiments. Geology28(12), 1091-1094. doi:10.1130/0091-7613(2000)28<1091:BIDPIA>2.0.CO;2
    41. Arias, J.L., & Fernández, M.S. (2008). Polysaccharides and proteoglycans in calcium carbonate-based biomineralization. Chemical reviews108(11), 4475-4482. doi:10.1021/cr078269p
    42. Datta, S., Manna, S., & Roy, D. (2022). Attachment of extracellular metabolic products of lysinibacillus sp. DRG3 on sand surface under variable flow velocities and bioprocesses. Journal of Environmental Engineering148(11), p.04022069.
    43. Xiao, Y., He, X., Zaman, M., Ma, G., & Zhao, C. (2022). Review of strength improvements of biocemented soils. International Journal of Geomechanics22(11), p.03122001. doi:10.1061/(ASCE)GM.1943-5622.0002565
    44. Achal, V., Mukherjee, A., Basu, P.C., & Reddy, M.S. (2009). Strain improvement of Sporosarcina pasteurii for enhanced urease and calcite production. Journal of industrial Microbiology and Biotechnology36(7), 981-988.doi:10.1007/s10295-009-0578-z
    45. DeJong, J.T., Fritzges, M.B., & Nüsslein, K. (2006). Microbially induced cementation to control sand response to undrained shear. Journal of geotechnical and geoenvironmental engineering132(11), 1381-1392. doi:10.1061/(ASCE)1090-0241(2006)132:11(1381)
    46. Lian, B., Hu, Q., Chen, J., Ji, J., & Teng, H.H. (2006). Carbonate biomineralization induced by soil bacterium Bacillus megateriumGeochimica et cosmochimica acta70(22), 5522-5535. doi:10.1016/j.gca.2006.08.044
    47. Dhami, N.K., Reddy, M.S., & Mukherjee, A. (2013) Biomineralization of calcium carbonate polymorphs by the bacterial strains isolated from calcareous sites. Journal of Microbiology & Biotechnology, 23:707–714.doi:10.4014/jmb.1212.11087
    48. Dhami, N.K., Reddy, M.S., & Mukherjee, A. (2014) Synergistic role of bacterial urease and carbonic anhydrase in carbonate mineralization. Applied Biochemistry & Biotechnology, 172:2552–2561. doi:10.1007/s12010-013-0694-0
    49. Zhang, C., Yin, L., Ou, Y., Yang, G., Huang, L., & Li, F. (2021). Contribution of selective bacterial extracellular polymeric substances to the polymorphism and morphologies of formed Ca/Mg carbonates. International Biodeterioration & Biodegradation160, p.105213.doi:10.1016/j.ibiod.2021.105213
    50. Okwadha, G.D., & Li, J. (2010). Optimum conditions for microbial carbonate precipitation. Chemosphere81(9), 1143-1148. doi:10.1016/j.chemosphere.2010.09.066
    51. De Muynck, W., De Belie, N., & Verstraete, W. (2010). Microbial carbonate precipitation in construction materials: a review. Ecological engineering36(2), 118-136. doi:10.1016/j.ecoleng.2009.02.006

    53.Rao, M.S., Reddy, V.S., & Sasikala, C. (2017). Performance of microbial concrete developed using bacillus subtilus JC3. Journal of The Institution of Engineers (India): Series A98, 501-510.

    54.Lee, C., Lee, H., & Kim, O.B. (2018). Biocement fabrication and design application for a sustainable urban area. Sustainability10(11), p.4079. doi:10.3390/su10114079

    1. Zhao Y., Xiao, Z., Lv, J., Shen, W., & Xu, R. (2019). A novel approach to enhance the urease activity of Sporosarcina pasteurii and its application on microbial-induced calcium carbonate precipitation for sand. Geomicrobiology, 36, 819–825. doi:10.1080/01490451.2019.1631911

    56.Konstantinou, C., Wang, Y., Biscontin, G., & Soga, K. (2021). The role of bacterial urease activity on the uniformity of carbonate precipitation profiles of bio-treated coarse sand specimens. Science Report. 11, 6161.

    1. Pourjasem, L., Landi, A., Enayatizamir, N., & Hojati, S. (2020). The release of some elements from vermiculite during the short periods of incubation by heterotrophic bacteria. Eurasian Soil Science53, 223-229. doi:10.1134/S106422932002009X

    58.Gurbuz, A., Sari, Y.D., Yuksekdag, Z.N., & Cinar, B., (2011). Cementation in a matrix of loose sandy soil using biological treatment method. African Journal of Biotechnology10(38), 7432-7440.

    59.Li, M., Li, L., Ogbonnaya, U., Wen, K., Tian, A., & Amini, F. (2016). Influence of fiber addition on mechanical properties of MICP-treated sand. Journal of Materials in Civil Engineering28(4), p.04015166. doi:10.1061/(ASCE)MT.1943-5533.0001442

    60.Chahal, N., Siddique, R., & Rajor, A. (2012a). Influence of bacteria on the compressive strength, water absorption and rapid chloride permeability of fly ash concrete. Construction and Building Materials28(1), pp.351-356. doi:10.15224/978-1-63248-062-0-28

    61.Andalib, R., Abd Majid, M.Z., Hussin, M.W., Ponraj, M., Keyvanfar, A., Mirza, J., & Lee, H.S. (2016). Optimum concentration of Bacillus megaterium for strengthening structural concrete. Construction and Building Materials118, pp.180-193. doi:10.3221/IGF-ESIS.59.32

    62.Shukla, A., Gupta, N., Singh, K.R., Kumar Verma, P., Bajaj, M., Khan, A.A., & Ayalew, F. (2022). Performance evaluation of bio concrete by cluster and regression analysis for environment protection. Computational Intelligence and Neuroscience2022(1), p.4411876. doi:10.1155/2022/4411876

    63.Dubey, A.A., Devrani, R., Ravi, K., Dhami, N.K., Mukherjee, A., & Sahoo, L. (2021). Experimental investigation to mitigate aeolian erosion via biocementation employed with a novel ureolytic soil isolate. Aeolian Research52, p.100727. doi:10.1016/j.aeolia.2021.100727

    64.Wang, Z., Zhang, N., Ding, J., Lu, C., & Jin, Y. (2018). Experimental study on wind erosion resistance and strength of sands treated with microbial-induced calcium carbonate precipitation. Advances in Materials Science and Engineering, 2018. doi:10.1155/2018/3463298

    65.Gomez, M.G., Martinez, B.C., DeJong, J.T., Hunt, C.E., deVlaming, L.A., Major, D.W., & Dworatzek, S.M. (2015). Field-scale bio-cementation tests to improve sands. Proceedings of the Institution of Civil Engineers-Ground Improvement168(3), pp.206-216.

    66.Meng, H., Gao, Y., He, J., Qi, Y., & Hang, L. (2021). Microbially induced carbonate precipitation for wind erosion control of desert soil: Field-scale tests. Geoderma383, p.114723.doi: 10.1016/j.geoderma.2020.114723

    67.Coban, O., De Deyn, G.B., & van der Ploeg, M. (2022). Soil microbiota as game-changers in restoration of degraded lands. Science375(6584), p.abe0725. doi:10.1126/science.abe0725