کاربرد کنسرسیوم باکتریایی مولد بیوسورفکتانت و تجزیه‌کننده نفت در افزایش ضریب آبگذری خاک آلوده به TPH

نوع مقاله : مقاله پژوهشی

نویسندگان

1 گروه علوم و مهندسی خاک، دانشکدگان کشاورزی و منابع طبیعی، دانشگاه تهران، کرج، ایران

2 گروه مهندسی محیط زیست، دانشکده محیط زیست، دانشگاه تهران، تهران، ایران.

3 گروه مهندسی علوم خاک، دانشکدگان کشاورزی و منابع طبیعی دانشگاه تهران، کرج ، ایران

چکیده

آلودگی نفتی به عنوان یکی از تهدیدات مهم حوزه حاصلخیزی خاک و تولیدات گیاهی شناخته شده است.  آلودگی ناشی  از هیدروکربنهای نفتی،  با کاهش هدایت هیدرولیکی خا‌ک‌ها، منجر به افزایش فرسایش و رواناب و کاهش رشد گیاه می‌شود. یکی از راه‌های اصلاح خاک‌های آلوده به هیدروکربن‌های نفتی، استفاده از میکروارگانیسم‌های مولد بیوسورفکتانت با قابلیت تجزیه هیدروکربن‌های نفتی است. در این مطالعه توانایی سویه‌های باکتریایی موثر در تجزیه نفت خام شامل: Dietzia aerolata PS14B1، Kocuria salina PS12B2 و Mesobacillus harenae PS9D12 در قالب یک کنسرسیوم میکروبی در تغییرات ضریب آبگذری یک خاک آلوده به نفت با آلودگی زیاد بررسی شدند. در آزمون توانایی رشد سویه‌ها و تجزیه هیدروکربن‌های نفتی در محیط پایه معدنی بعد از 7 روز گرماگذاری، نتایج نشان داد که سویه‌های PS14B1، PS12B2 و PS9D12 به ترتیب موفق به کاهش هیدروکربن‌های نفتی کل (TPH) به میزان 63/25 %، 11/24 % و 83/22 % شدند که تفاوت معنی‌داری با شاهد داشتند (P<0.05). نتایج آزمایشات تلقیح سویه‌ها در محیط خاک و بعد از 30 روز انکوباسیون نشان داد، کنسرسیوم فوق موفق به افزایش هدایت هیدرولیکی خاک از 18/1 به 12/9 سانتی‌متر بر ساعت شده است که نسبت به تیمار شاهد (24/3 سانتی‌متر بر ساعت) معنی‌دار بود. بنابراین، می‌توان از این سویه‌ها در اصلاح پایدار محل‌های آلوده به ترکیبات نفتی و تعدیل وضعیت آبگذری خاک‌های آلوده استفاده کرد.

کلیدواژه‌ها

موضوعات


عنوان مقاله [English]

The application of biosurfactant producing bacterial consortium as a petroleum degrader in increasing the hydraulic conductivity coefficient of TPH-contaminated soil

نویسندگان [English]

  • Komeil Zeynali 1
  • Shayan Shariati 2
  • Ahmad Ali pourbabaei 3
  • MEDI SHORAFA 3
1 Department of Soil Science Engineering, College of Agriculture &amp;amp; Natural Resources, University of Tehran, Karaj, Iran
2 Department of Environmental Engineering, Faculty of Environment, University of Tehran, Tehran, Iran.
3 Department of Soil Science Engineering, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran
چکیده [English]

Oil pollution is recognized as one of the significant threat to soil fertility and plant production. Pollution caused by petroleum hydrocarbons, reduces the hydraulic conductivity of soils, leading to increased erosion and runoff, and decreased plant growth. One practical approach for remediating soils contaminated with petroleum hydrocarbons is using biosurfactant-producing microorganisms that can degrade these compounds. This study examined the efficacy of a microbial consortium comprising the bacterial strains Dietzia aerolata PS14B1, Kocuria salina PS12B2, and Mesobacillus harenae PS9D12 in altering the permeability coefficient of soil contaminated with high pollution (TPH). In the hydrocarbon growth and degradation test in the mineral base medium after seven days of incubation, the results showed that strains PS14B1, PS12B2, and PS9D12 were successful in reducing Total Petroleum Hydrocarbons (TPH) by 25.63%, 24.11%, and 22.83%, respectively, which was significantly different from the control (P<0.05).  The inoculation of the bacterial strains into the soil and subsequent 30-day incubation demonstrated a significant increase in soil hydraulic conductivity, from 1.18 cm h-1 to 9.12 cm h-1, compared to the control treatment (3.24 cm h-1). These findings suggest that the bacterial consortium holds potential for the sustainable remediation of oil-contaminated sites and the enhancement of soil permeability in polluted areas.

کلیدواژه‌ها [English]

  • Biodegradation
  • Biosurfactant
  • Crude oil
  • Hydraulic conductivity
  • Oil pollution

EXTENDED ABSTRACT

Introduction:

 The surge in petroleum product demand poses a significant risk of oil pollution. Crude oil, a mixture of diverse hydrocarbons, is susceptible to degradation by microorganisms. Exposure to petroleum compounds not only disrupts soil structure but also endangers human health due to their carcinogenic and mutagenic properties. Such compounds impede water flow mechanisms in contaminated soils, leading to reduced hydraulic conductivity, erosion, and surface runoff. Bioremediation emerges as a promising approach to address oil-contaminated soils, mainly through the secretion of biosurfactants by proficient microbes, enhancing the compounds' biodegradation by augmenting their bioavailability. This study aims to explore the biodegradation capability and biosurfactant secretion of hydrocarbonoclastic bacteria, along with improving hydraulic conductivity in oil-contaminated soil using potent strains.

Materials and Methods:

Twelve bacterial strains isolated from oil-contaminated soil were obtained from the microbial collection of the Soil Science and Engineering Department, Faculty of Agriculture, University of Tehran. Initial testing involved assessing the growth ability of strains in MSM-agar medium containing crude oil as the sole source of carbon and energy. The Total Petroleum Hydrocarbon (TPH) reduction ability was evaluated by inoculating bacteria into a MSM medium containing 1% crude oil (at a concentration of 5% v/v) and determining the remaining TPH gravimetrically after seven days. Furthermore, biosurfactant production capacity was assessed through oil spreading, surface tension reduction, and emulsification index (%E24) tests. Based on the results, three strain: Dietzia aerolata PS14B1, Kocuria salina PS12B2, and Mesobacillus harenae PS9D12 were selected and applied as a microbial consortium to contaminated soil to evaluate their impact on hydraulic conductivity.

Results and Discussion:

The growth ability test indicated that strain PS12B2 exhibited the highest growth compared to others in the presence of oil. In the oil spread test, strains PS12B2, PS2C3, and PS20B1 exhibited the most expansive halos, measuring 2.43, 2, and 2 cm, respectively, which was statistically significant (P<0.05). It's noteworthy that researchers established a minimum halo diameter of 0.5 cm as indicative of positive biosurfactant secretion. Moving on to the surface tension test, strains PS12E1, PS20B1, and PS12B2 demonstrated remarkable efficacy in reducing the surface tension of distilled water from 72.36 mN m-1 to 32.37, 31.39, and 30.43 mN m-1, respectively. Furthermore, in the E24 test utilizing n-hexane as a water-repellent medium, strains PS20B1, PS7D1, and PS12E1 exhibited the highest emulsifying capacity among all strains, with E24 values of 54.93%, 42.58%, and 40.5%, respectively. Notably, strains PS14B1, PS12B2, and PS9D12 demonstrated substantial TPH reduction capacities by 25.63%, 24.11%, and 22.83%, respectively, which was significantly different from the control treatment (1% reduction). Monitoring soil hydraulic conductivity showed a significant increase from 1.18 to 9.12 cm h-1 after 30 days with the PSZ treatment compared to the control treatment (3.24 cm h-1) (P<0.05).

Conclusion:

Petroleum hydrocarbons have adverse effects on human health and soil physical properties such as hydraulic conductivity. Bioremediation is one of the best methods for restoring soils contaminated with oil. The results of this study showed that strains Dietzia aerolata PS14B1, Kocuria salina PS12B2, and Mesobacillus harenae PS9D12 have good growth capability in MSM agar oily medium, biosurfactant secretion, and petroleum hydrocarbon degradation. Additionally, the consortium composed of these strains increased soil hydraulic conductivity from 1.18 to 9.12 cm h-1 (P<0.05). Therefore, these strains can be used in the bioremediation of oil-contaminated areas to promote environmental cleanliness and stability.

Author Contributions

K.Z wrote the original draft and, investigation, writing—review, A.A.P; supervision, Conceptualization, funding acquisition and project administration, S.S; methodology, formal analysis, data curation, M.S.; validation, resources, editing, and visualization. All authors have read and agreed to the published version of the manuscript.

Acknowledgements

Authors sincerely acknowledge University College of Agriculture (UCA), South Oilfields Company for providing funding to carry out this research work. The authors also would like to thank Dr. Moradi from Gachsaran oil company for providing of soil sample for the present study.

Conflict of interest

The authors declare no competing interests.

Adieze, I. E., Orji, J. C., Nwabueze, R. N., & Onyeze, G. O. C. (2012). Hydrocarbon stress response of four tropical plants in weathered crude oil contaminated soil in microcosms. International Journal of Environmental Studies, 69(3), 490-500.
Akinwumi, I. I., Adeyeri, J. B., & Ejohwomu, O. A. (2013). Effects of steel slag addition on the plasticity, strength, and permeability of lateritic soil. In ICSDEC 2012: Developing the Frontier of Sustainable Design, Engineering, and Construction (pp. 457-464).
Alexander, M. (1983). Most probable number method for microbial populations. Methods of Soil Analysis: Part 2 Chemical and Microbiological Properties, 9, 815-820.
Almansoory, A. F., Hasan, H. A., Abdullah, S. R. S., Idris, M., Anuar, N., & Al-Adiwish, W. M. (2019). Biosurfactant produced by the hydrocarbon-degrading bacteria: Characterization, activity and applications in removing TPH from contaminated soil. Environmental technology & innovation14, 100347.
Al-Marri, S., Eldos, H. I., Ashfaq, M. Y., Saeed, S., Skariah, S., Varghese, L., ... & Raja, M. M. (2023). Isolation, identification, and screening of biosurfactant-producing and hydrocarbon-degrading bacteria from oil and gas industrial waste. Biotechnology Reports39, e00804.
Athar, H. U. R., Ambreen, S., Javed, M., Hina, M., Rasul, S., Zafar, Z. U., ... & Ashraf, M. (2016). Influence of sub-lethal crude oil concentration on growth, water relations and photosynthetic capacity of maize (Zea mays L.) plants. Environmental Science and Pollution Research, 23, 18320-18331.
Avizhgan, A., Asadi, H., Mohammadi, M. H., & Gorji, M. (2021). Assessment of Surface Sealing Formation and Its Relationship with Soil Quality Indices. Iranian Journal of Soil and Water Research, 52(6), 1501-1514.
Baoune, H., Aparicio, J. D., Pucci, G., Ould El Hadj-Khelil, A., & Polti, M. A. (2019). Bioremediation of petroleum-contaminated soils using Streptomyces sp. Hlh1. Journal of Soils and Sediments19, 2222-2230.
Black, C. A. (1965). Method of soil analysis part 2. Chemical and microbiological properties, 9, 1387-1388.
Bouyoucos, G. J. (1962). Hydrometer method improved for making particle size analyses of soils 1. Agronomy Journal, 54(5), 464-465.
Bremner, J. M. (1965). Total nitrogen. Methods of soil analysis: part 2 chemical and microbiological properties, 9, 1149-1178.
Chen, W., Kong, Y., Li, J., Sun, Y., Min, J., & Hu, X. (2020). Enhanced biodegradation of crude oil by constructed bacterial consortium comprising salt-tolerant petroleum degraders and biosurfactant producers. International Biodeterioration & Biodegradation, 154, 105047.
Clark, F. E. (1965). Agar-plate method for total microbial count. In: C. A. Black, D. D. Evans, L. E. Ensminger, J. L.White, & F. E. Clark (Eds.), Methods for soil analysis. Part 2 chemical and microbiological properties (pp. 1461–1465).
Concepta Goveas, L., Alva, M., Menezes, J., Krishna, A., Salian, A., & Sajankila, S. P. (2022). Optimization of degradation of petroleum crude oil by Lysinibacillus sp. SS1 in seawater by response surface methodology. Journal of Applied Biotechnology Reports9(1), 494-503.
Dastgheib, S. M. M., Tirandaz, H., Moshtaghi Nikou, M., Ramezani, M., Shavandi, M., Amoozegar, M. A., & Ventosa, A. (2017). Prauserella oleivorans sp. nov., a halophilic and thermotolerant crude-oil-degrading actinobacterium isolated from an oil-contaminated mud pit. International Journal of Systematic and Evolutionary Microbiology67(9), 3381-3386.
Devatha, C. P., Vishnu Vishal, A., & Purna Chandra Rao, J. (2019). Investigation of physical and chemical characteristics on soil due to crude oil contamination and its remediation. Applied Water Science, 9, 1-10.
Devatha, C. P., Vishnu Vishal, A., & Purna Chandra Rao, J. (2019). Investigation of physical and chemical characteristics on soil due to crude oil contamination and its remediation. Applied Water Science9, 1-10.
Gyasi, S. F., Sarfo, M. K., Kabo-Bah, A. T., Adu, B., Appiah, A. S., & Serfor-Armah, Y. (2024). In vitro assessment of crude oil degradation by Acinetobacter junii and Alcanivorax xenomutans isolated from the coast of Ghana. Heliyon10(3).
Hamidi, Y., Ataei, S. A., & Sarrafi, A. (2021). Biodegradation of total petroleum hydrocarbons in oily sludge: a comparative study of biostimulation, bioaugmentation, and combination of methods. Journal of Chemical Technology & Biotechnology96(5), 1302-1307.
Hewelke, E., & Gozdowski, D. (2020). Hydrophysical properties of sandy clay contaminated by petroleum hydrocarbon. Environmental Science and Pollution Research27(9), 9697-9706.
Hossain, M. F., Akter, M. A., Sohan, M. S. R., Sultana, N., Reza, M. A., & Hoque, K. M. F. (2022). Bioremediation potential of hydrocarbon degrading bacteria: isolation, characterization, and assessment. Saudi Journal of Biological Sciences29(1), 211-216.
Karlapudi, A. P., Venkateswarulu, T. C., Tammineedi, J., Kanumuri, L., Ravuru, B. K., Ramu Dirisala, V., & Kodali, V. P. (2018). Role of biosurfactants in bioremediation of oil pollution-a review. Petroleum4(3), 241-249.
Khalifa, A. Y. (2017). Degradation of diesel-oil by a newly isolated Kocuria sediminis DDK6. African Journal of Microbiology Research11(10), 400-407.
Khobragade, V. B., & Kulkarni, S. D. (2019). Isolation and biochemical characterization of bacteria from petroleum hydrocarbon contaminated soils from Maharashtra, India.
Kim, K. H., Jahan, S. A., Kabir, E., & Brown, R. J. (2013). A review of airborne polycyclic aromatic hydrocarbons (PAHs) and their human health effects. Environment international, 60, 71-80.
Lee, D. W., Lee, H., Kwon, B. O., Khim, J. S., Yim, U. H., Kim, B. S., & Kim, J. J. (2018). Biosurfactant-assisted bioremediation of crude oil by indigenous bacteria isolated from Taean beach sediment. Environmental pollution241, 254-264.
Li, Z., Rosenzweig, R., Chen, F., Qin, J., Li, T., Han, J., ... & Ronen, Z. (2022). Bioremediation of Petroleum-Contaminated Soils with Biosurfactant-Producing Degraders Isolated from the Native Desert Soils. Microorganisms10(11), 2267.
Mehetre, G. T., Dastager, S. G., & Dharne, M. S. (2019). Biodegradation of mixed polycyclic aromatic hydrocarbons by pure and mixed cultures of biosurfactant producing thermophilic and thermo-tolerant bacteria. Science of the total environment679, 52-60.
Michel, B. E., & Kaufmann, M. R. (1973). The osmotic potential of polyethylene glycol 6000. Plant Physiology, 51(5), 914-916.
Mishra, A., Saxena, A., & Singh, S. P. (2019). Isolation and characterization of microbial strains from refinery effluent to screen their bioremediation potential. J Pure Appl Microbiol13(4), 2325-2332.
Nayarisseri, A., Singh, P., & Singh, S. K. (2018). Screening, isolation and characterization of biosurfactant producing Bacillus subtilis strain ANSKLAB03. Bioinformation14(6), 304.
Nazina, T. N., Shumkova, E. S., Sokolova, D. S., Babich, T. L., Zhurina, M. V., Xue, Y. F., ... & Tourova, T. P. (2015). Identification of hydrocarbon-oxidizing Dietzia bacteria from petroleum reservoirs based on phenotypic properties and analysis of the 16S rRNA and gyr B genes. Microbiology84, 377-388.
Nazir, A. K. (2011). Effect of motor oil contamination on geotechnical properties of over consolidated clay. Alexandria Engineering Journal, 50(4), 331-335.
Nelson, D. A., & Sommers, L. (1983). Total carbon, organic carbon, and organic matter. Methods of soil analysis: Part 2 chemical and microbiological properties, 9, 539-579.
Nikitha, T., Satyaprakash, M., Vani, S. S., Sadhana, B., & Padal, S. B. (2017). A review on polycyclic aromatic hydrocarbons: their transport, fate and biodegradation in the environment. Int. J. Curr. Microbiol. Appl. Sci, 6(4), 1627-1639.
Olsen, S. R. (1954). Estimation of available phosphorus in soils by extraction with sodium bicarbonate (No. 939). US Department of Agriculture.
Othman, A. R., Ismail, N. S., Abdullah, S. R. S., Hasan, H. A., Kurniawan, S. B., Sharuddin, S. S. N., & Ismail, N. I. (2022). Potential of indigenous biosurfactant-producing fungi from real crude oil sludge in total petroleum hydrocarbon degradation and its future research prospects. Journal of Environmental Chemical Engineering10(3), 107621.
Phulpoto, I. A., Yu, Z., Li, J., Ndayisenga, F., Hu, B., Qazi, M. A., & Yang, X. (2022). Evaluation of di-rhamnolipid biosurfactants production by a novel Pseudomonas sp. S1WB: Optimization, characterization and effect on petroleum-hydrocarbon degradation. Ecotoxicology and Environmental Safety242, 113892.
Rayment, G. E., & Higginson, F. R. (1992). Australian laboratory handbook of soil and water chemical methods. Inkata Press Pty Ltd.
Sattar, S., Siddiqui, S., Shahzad, A., Bano, A., Naeem, M., Hussain, R., ... & Yasmin, H. (2022). Comparative Analysis of Microbial Consortiums and Nanoparticles for Rehabilitating Petroleum Waste Contaminated Soils. Molecules, 27(6), 1945.
Shah, G., & Soni, V. (2024). Comprehensive Insights into the Impact of Oil Pollution on the Environment. Regional Studies in Marine Science, 103516.
Shariati, S., Ebenau-Jehle, C., Pourbabaee, A. A., Alikhani, H. A., Rodriguez-Franco, M., Agne, M., ... & Boll, M. (2021). Degradation of dibutyl phthalate by Paenarthrobacter sp. Shss isolated from Saravan landfill, Hyrcanian Forests, Iran. Biodegradation, 1-12.
Sharuddin, S. S. N., Abdullah, S. R. S., Hasan, H. A., Othman, A. R., & Ismail, N. I. (2021). Potential bifunctional rhizobacteria from crude oil sludge for hydrocarbon degradation and biosurfactant production. Process Safety and Environmental Protection155, 108-121.
Silva, R. D. C. F., Almeida, D. G., Rufino, R. D., Luna, J. M., Santos, V. A., & Sarubbo, L. A. (2014). Applications of biosurfactants in the petroleum industry and the remediation of oil spills. International journal of molecular sciences15(7), 12523-12542.
Sobri, I. M., Halim, M., Lai, O. M., Lajis, A. F., Yusof, M. T., Halmi, M. I. E., ... & Wasoh, H. (2018). Emulsification characteristics of rhamnolipids by Pseudomonas aeruginosa using coconut oil as carbon source. Journal of Environmental Microbiology and Toxicology6(1), 7-12.
Su, H., Lin, J., & Wang, Q. (2021). A clean production process on oily sludge with a novel collaborative process via integrating multiple approaches. Journal of Cleaner Production322, 128983.
Sutton, N. B., Maphosa, F., Morillo, J. A., Abu Al-Soud, W., Langenhoff, A. A., Grotenhuis, T., ... & Smidt, H. (2013). Impact of long-term diesel contamination on soil microbial community structure. Applied and Environmental Microbiology, 79(2), 619-630.
Thavasi, R., Jayalakshmi, S., & Banat, I. M. (2011). Application of biosurfactant produced from peanut oil cake by Lactobacillus delbrueckii in biodegradation of crude oil. Bioresource technology102(3), 3366-3372.
Tripathi, V., Gaur, V. K., Thakur, R. S., Patel, D. K., & Manickam, N. (2023). Assessing the half-life and degradation kinetics of aliphatic and aromatic hydrocarbons by bacteria isolated from crude oil contaminated soil. Chemosphere337, 139264.
Ure, A. M., Quevauviller, P. H., Muntau, H., & Griepink, B. (1993). Speciation of heavy metals in soils and sediments. An account of the improvement and harmonization of extraction techniques undertaken under the auspices of the BCR of the Commission of the European Communities. International journal of environmental analytical chemistry51(1-4), 135-151.
Uyun, K., Darmayati, Y., & Mustafa, I. (2022). Perlite-immobilized bacterialconsortium enhanced degradation of crude oil-contaminated marine sediment. Journal of Sustainability Science and Management, 17(1), 194-203.
Varjani, S. J. (2017). Microbial degradation of petroleum hydrocarbons. Bioresource technology223, 277-286.
Varjani, S. J., & Upasani, V. N. (2016). Carbon spectrum utilization by an indigenous strain of Pseudomonas aeruginosa NCIM 5514: Production, characterization and surface active properties of biosurfactant. Bioresource technology221, 510-516.
Varjani, S. J., & Upasani, V. N. (2017). A new look on factors affecting microbial degradation of petroleum hydrocarbon pollutants. International Biodeterioration & Biodegradation, 120, 71-83.
Varjani, S. J., and V. K. Srivastava. "Green technology and sustainable development of environment." Renewable Resources Journal 3.1 (2015): 244-49.
Viramontes-Ramos, S., Portillo-Ruiz, M. C., Ballinas-Casarrubias, M. D. L., Torres-Muñoz, J. V., Rivera-Chavira, B. E., & Nevárez-Moorillón, G. V. (2010). Selection of biosurfactan/bioemulsifier-producing bacteria from hydrocarbon-contaminated soil. Brazilian Journal of Microbiology41, 668-675.
Wang, D., Lin, J., Lin, J., Wang, W., & Li, S. (2019). Biodegradation of petroleum hydrocarbons by Bacillus subtilis BL-27, a strain with weak hydrophobicity. Molecules, 24(17), 3021.
Xia, M., Liu, Y., Taylor, A. A., Fu, D., Khan, A. R., & Terry, N. (2017). Crude oil depletion by bacterial strains isolated from a petroleum hydrocarbon impacted solid waste management site in California. International Biodeterioration & Biodegradation123, 70-77.
Yan, Z., Jiang, H., Cai, H., Zhou, Y., & Krumholz, L. R. (2015). Complex interactions between the macrophyte Acorus calamus and microbial fuel cells during pyrene and benzo [a] pyrene degradation in sediments. Scientific reports, 5(1), 10709.
Zhang, Z., Sun, J., Gong, X., Yang, Z., Wang, C., & Wang, H. (2022). Anaerobic phenanthrene biodegradation by a new salt-tolerant/halophilic and nitrate-reducing Virgibacillus halodenitrificans strain PheN4 and metabolic processes exploration. Journal of Hazardous Materials, 435, 129085.
Ziwei, B., Hanning, W., Lusha, W., Zena, Z., & Yifei, W. (2023). Isolation and characterization of viscosity-reducing and biosurfactant-producing bacteria in low-permeability reservoir. International Journal of Energy Research2023.