The potential of organic wastes in eliminating old-aged petroleum pollution in saline soils: A case study in Khuzestan province

Document Type : Original Research Paper

Authors

1 Department of Soil Science and Engineering, University of Tehran, Iran

2 Iranian Institute of R&D in Chemical Industries, Tehran, Iran (ACECR)

3 Department of Agricultural Machinery Engineering, University of Tehran, Iran

Abstract

Petroleum contains carcinogens and toxic substances that can have an unfavorable impact on environmental quality and human health when the soil becomes contaminated with crude oil.  BBiostimulation and bioaugmentation are the main strategies in the bioremediation of oil-contaminated soils. To decompose old-aged petroleum pollution in saline soil, a full factorial experiment was utilized. The experiment was designed using a completely randomized design with four factors: bacterial inoculum, sugarcane bagasse, chemical fertilizer, and molasses. The application of these factors was conducted in four separate experiments: pretreatment of agricultural soil and spent mushroom compost, pretreatment of spent mushroom compost, pretreatment of agricultural soil, and no pretreatment. After a 60-day incubation period at 28 ˚C, the results showed that the organic wastes of molasses and spent mushroom compost in combination with bacterial inoculum reduced total petroleum hydrocarbons 38 and 33.3%, respectively. Molasses had a considerable impact on increasing the efficiency of bacterial inoculum 1 and bacterial inoculum 3. Similarly, spent mushroom compost was found to significantly affect bacterial inoculum 1. In addition, bagasse was observed to accelerate the bioremediation process by improving the physical conditions of the soil. In the pretreatment of agricultural soil, bagasse in combination with bacterial inoculum 1 and chemical fertilizer reduced the total petroleum hydrocarbons significantly (38%) compared to the control treatment. These results highlight the effectiveness of organic wastes as biostimulation agents in promoting the growth and reproduction of the soil microbial community, as well as establishing the bacterial inoculum.

Keywords

Main Subjects


Abdollahinejad, B., Pasalari, H., Jafari, A. J., Esrafili, A., & Farzadkia, M. (2020). Bioremediation of diesel & gasoline-contaminated soil by co-vermicomposting amended with activated sludge: diesel & gasoline degradation & kinetics. Environ. Pollut., 263 (Part A); 114584.
Adesodun, J. K., & Mbagwu, J. S. C. (2008). Biodegradation of waste-lubricating petroleum oil in a tropical tlfisol as mediated by animal droppings. Bioresource Technol., 99(13); 5659–5665.
Alvim, G. M., & Pontes, P. P. (2018). Aeration & sawdust application effects as structural material in the bioremediation of clayey acid soils contaminated with diesel oil. Int. Soil Water Conserv. Res., 6(3); 253–260.
Ani, K. A., Agu, C. M., Esonye, C., & Menkiti, M. C. (2021). Investigations on the characterizations, optimization & effectiveness of goat manure compost in crude oil biodegradation. Curr. Res. Green Sustain. Chem., 4; 100120. 
Antón-Herrero, R., García-Delgado, C., Baena, N., Mayans, B., Delgado-Moreno, L., & Eymar, E. (2022). Assessment of different spent mushroom substrates to bioremediate soils contaminated with petroleum hydrocarbons. Appl. Sci., 12(15); 7720. 
Aona, D., Yaning, L., & Jun, Q. (2017). Life cycle assessment of edible fungi residue compost-a case study of Beijing.Nature Environ. Pollut. Technol., 16(2); 643-646.
Asemoloye, M. D., Chukwuka, K. S., & Jonathan, S. G. (2020). Spent mushroom compost enhances plant response & phytoremediation of heavy metal polluted soil. J. Plant Nutrition Soil Sci., 183(4); 492–499. 
Azadi, N., & Raiesi, F. (2021). Sugarcane bagasse biochar modulates metal & salinity stresses on microbial functions & enzyme activities in saline co-contaminated soils. Appl. Soil Ecol., 167; 104043.
Babaei, A. A., Safdari, F., Alavi, N., Bakhshoodeh, R., Motamedi, H., & Paydary, P. (2020). Co-composting of oil-based drilling cuttings by bagasse. Bioproc. biosyst. eng., 43(1); 1-12. 
Biswas, B., Sarkar, B., Rusmin, R., & Naidu, R. (2017). Mild acid & alkali treated clay minerals enhance bioremediation of polycyclic aromatic hydrocarbons in long-term contaminated soil: A 14 C-tracer study. Environ. Pollut., 223; 255–265. 
Bodor, A., Petrovszki, P., Kis, Á. E., Vincze, G. E., Laczi, K., Bounedjoum, N., Szilágyi, Á., Szalontai, B., Feigl, G., Kovács, K. L., Rákhely, G., & Perei, K. (2020). Intensification of ex situ bioremediation of soils polluted with used lubricant oils: a comparison of biostimulation & bioaugmentation with a special focus on the type & size of the inoculum. Int. J. Env. Res. Pub. Heal., 17(11); 4106. 
Bremner, J.M. (1996). Nitrogen total, 1085–1122, in: Methods of soil analysis Part 3: Chemical methods. Madison, WI: Soil Science Society of American & American Society of Agronomy.
Bridson, E. Y., & Brecker, A. (1970). Design & formulation of microbial culture media. Meth. Microbiol., 3: 229–295.
Dadrasnia, A., & Ismail, S. B. (2015). Bio-enrichment of waste crude oil polluted soil: amended with Bacillus 139SI & organic waste. Int. J. Environ. Sci. Dev., 6(4); 241–245.
Estefan, G. (2013). Methods of soil, plant, & water analysis: A manual for the west Asia & North Africa region: Third Edition. International Center for Agricultural Research in the Dry Areas. 
Etesami, H., & Beattie, G. A. (2018). Mining halophytes for plant growth-promoting halotolerant bacteria to enhance the salinity tolerance of non-halophytic crops. Front. Microbiol., 9; 148.
Feng, L., Jiang, X., Huang, Y., Wen, D., Fu, T., & Fu, R. (2021). Petroleum hydrocarbon-contaminated soil bioremediation assisted by isolated bacterial consortium & sophorolipid. Environ. Pollut., 273; 116476.
Garousin, H., Pourbabaee, A. A., Alikhani, H. A., & Yazdanfar, N. (2021). A combinational strategy mitigated old-aged petroleum contaminants: ineffectiveness of biostimulation as a bioremediation technique. Front. Microbiol., 12; 642215.
Gee, G.W., & Bauder, J.W. (1986). Particle-size analysis, 383–411, in: Klute, A. (Ed.), Method of soil analysis, part 1. Madison, WI: American Society of Agronomy/Soil Science Society of America.
Gharibzadeh, F., Rezaei Kalantary, R., Nasseri, S., Esrafili, A., & Azari, A. (2016). Reuse of polycyclic aromatic hydrocarbons (PAHs) contaminated soil washing effluent by bioaugmentation/biostimulation process. Separ. Purif. Tec., 168; 248–256.
Gielnik, A., Pechaud, Y., Huguenot, D., Cébron, A., Esposito, G., & van Hullebusch, E. D. (2021). Functional potential of sewage sludge digestate microbes to degrade aliphatic hydrocarbons during bioremediation of a petroleum hydrocarbons contaminated soil. J. Environ. Manage., 280; 1-8. 
Gitipour, S., Hedayati, M., & Madadian, E. (2015). Soil washing for reduction of aromatic & aliphatic contaminants in soil. CLEAN – Soil, Air, Water, 43(10); 1419–1425. 
Guzmán-López, O., Cuevas-Díaz, M. del C., Martínez Toledo, A., Contreras-Morales, M. E., Ruiz-Reyes, C. I., & Ortega Martínez, A. del C. (2021). Fenton-biostimulation sequential treatment of a petroleum-contaminated soil amended with oil palm bagasse (Elaeis Guineensis). Chem. Ecol., 37(6); 573–588. 
Hamzah, A., Phan, C., Yong, P., & Mohd Ridzuan, N. H. (2014). Oil palm empty fruit bunch & sugarcane bagasse enhance the bioremediation of soil artificially polluted by crude oil. Soil Sediment Contam., 23(7); 751–762. 
Hewelke, E., Szatyłowicz, J., Hewelke, P., Gnatowski, T., & Aghalarov, R. (2018). The impact of diesel oil pollution on the hydrophobicity & CO2 efflux of forest soils. Water, Air, & Soil Pollut., 229(2); 1–11. 
Hoang, S. A., Sarkar, B., Seshadri, B., Lamb, D., Wijesekara, H., Vithanage, M., Liyanage, C., Kolivabandara, Pabasari A., Rinklebe, J., Lam, S. S, Vinu, A., Wang, H., Kirkham, M. B., & Bolan, N. S. (2021). Mitigation of petroleum-hydrocarbon-contaminated hazardous soils using organic amendments: a review. J. Hazard. Mater., 416; 125702.
Horel, A., Mortazavi, B., & Sobecky, P. A. (2015). Input of organic matter enhances degradation of weathered diesel fuel in sub-tropical sediments. Sci. Total Environ, 533; 82–90.
Huang, L., Ye, J., Jiang, K., Wang, Y., & Li, Y. (2021). Oil contamination drives the transformation of soil microbial communities: co-occurrence pattern, metabolic enzymes & culturable hydrocarbon-degrading bacteria. Ecotox. Environ. safe., 225; 112740.
Hussain, F., Hussain, I., Khan, A. H. A., Muhammad, Y. S., Iqbal, Mazhar, S., Gerhard, R., Thomas Gerhard, Z., & Yousaf, S. (2018). Combined application of biochar, compost, & bacterial consortia with Italian Ryegrass enhanced phytoremediation of petroleum hydrocarbon contaminated soil. Environ., & Exp. Bot., 153; 80–88.
Kalami, R & Pourbabaee, A. A. (2021). Investigating the potential of bioremediation in aged oil-polluted hypersaline soils in the south oilfields of Iran. Environ. monit. assess., 193(8); 517-537. 
Korouzhdehi, B., Abbasi, A. R., Bahreini, M., Pourbabaee, A. A., & Moghadam, M. R. S. (2018). Isolation & recognition of keratinolytic bacteria strains based on their biochemical & molecular properties. J. Genet., 12(4); 525.
Kuyukina, M. S., & Ivshina, I. B. (2019). Bioremediation of contaminated environments using Rhodococcus. 231–270.
Levy-Booth, D. J., Fetherolf, M. M., Stewart, G. R., Liu, J., Eltis, L. D., & Mohn, W. W. (2019). Catabolism of alkylphenols in Rhodococcus via a meta-cleavage pathway associated with genomic Islands. Front. Microbiol., 1(AUG); 1862.
Lim, M. W., Lau, Ee V., & Poh, P. E. (2016). A comprehensive guide of remediation technologies for oil contaminated soil — present works & future directions. Mar. Pollut. Bull., 109(1); 14–45.
Liu, J., Chen, S., Ding, J., Xiao, Y., Han, H., & Zhong, G. (2015). Sugarcane bagasse as support for immobilization of Bacillus Pumilus HZ-2 & its use in bioremediation of mesotrione-contaminated soils. Appl. Microbiol. Biotec., 99(24); 10839–10851. 
Liu, X., Ge, W., Zhang, X., Chai, C., Wu, J., Xiang, D., & Chen, X. (2019). Biodegradation of aged polycyclic aromatic hydrocarbons in agricultural soil by Paracoccus Sp. LXC combined with humic acid & spent mushroom substrate. J. Hazard. Mater., 379; 120820.
Liu, Y., Lai, Q., Du, J., & Shao, Z. (2016). Bacillus Zhangzhouensis sp. Nov., & Bacillus Australimaris sp. Nov. Int. J. Syst. Evol. Microbiol., 66(3); 1193–1199. 
Lladó, S., Covino, S., Solanas, A. M., Viñas, M., Petruccioli, M., & D’annibale, A. (2013). Comparative assessment of bioremediation approaches to highly recalcitrant PAH degradation in a real industrial polluted soil. J. hazard. mater., 248–249(1); 407–414. 
Lu, C., Hong, Y., Liu, J., Gao, Y., Ma, Z., Yang, B., Ling, W., & Waigi, M. G. (2019). A PAH-degrading bacterial community enriched with contaminated agricultural soil & its utility for microbial bioremediation. Environ. Pollut., 251; 773–782.
Martínez Álvarez, L. M., Lo Balbo, A., Mac Cormack, W. P., & Ruberto, L. A.M. (2015). Bioremediation of a petroleum hydrocarbon-contaminated antarctic soil: optimization of a biostimulation strategy using response-surface methodology (RSM). Cold Reg. Sci. Technol., 119; 61–67.
Mohammadi, F., Roedl, A., Abdoli, M. A., Amidpour, M., & Vahidi, H. (2020). Life cycle assessment (LCA) of the energetic use of bagasse in iranian sugar industry. Renew. Energ., 145; 1870–1882.
Nelson, D.W., & Sommers, L.E. (1996). Total carbon, organic carbon & organic matter, 961–1010, in: Sparks, D. L. (Ed.), Methods of soil analysis Part 3: Chemical methods. Madison, WI: Soil Science Society of American & American Society of Agronomy.
Nikkhah, M., Pourbabaee, A. A., Shariati, S., & Shakiba, M. (2023). The saline rhizospheric soil of Sparganium Erectum L. plant: a new source of efficient bacteria for azo dye decolorization. Pollut., 9(1); 107-125. 
Nwankwegu, A. S., & Onwosi, C. O. (2017). Bioremediation of gasoline contaminated agricultural soil by bioaugmentation. Environ. Technol. Innov., 7: 1–11.
Obieze, C. C., Chikere, C. B., Selvarajan, R., Adeleke, R., Ntushelo, K., & Akaranta, O. (2020). Functional attributes & response of bacterial communities to nature-based fertilization during hydrocarbon remediation. Int. Biodeterior. Biodegrad., 154: 105084.
Okerentugba, P.O., Orji, F.A., Ibiene, A.A., & Elemo, G.N. (2015). Spent mushroom compost for bioremediation of petroleum hydrocarbon polluted soil: a review. Global Adv. Res. J. Environ. Sci. Toxicol., 4(1); 001–007. 
Olsen, S. R., & Sommers, L. E. (1982). Phosphorus, 403–430, in: Page, A. L. (Ed.), Methods of soil analysis Part 2: Chemical & microbiological properties. Madison, WI: Soil Science Society of American & American Society of Agronomy.
Ossai, I. C., Ahmed, A., Hassan, A., & Hamid, F. S. (2020). Remediation of soil & water contaminated with petroleum hydrocarbon: a review. Environ. Technol. Innov., 17: 100526.
Poi, G., Aburto-Medina, A., Mok, P. C., Ball, A. S., & Shahsavari, E. (2017). Large scale bioaugmentation of soil contaminated with petroleum hydrocarbons using a mixed microbial consortium. Ecol. Eng., 102; 64–71.
Pourbabaee, A. A., Shahriari, M. H., & Garousin, H. (2019). Biodegradation of phenanthrene as a model hydrocarbon: power display of a super-hydrophobic halotolerant enriched culture derived from a saline-sodic soil. Biotechnol. Rep., 24; e00388.
Ravanipour, M., Kalantary, R. R., Mohseni-Bandpi, A., Esrafili, A., Farzadkia, M., & Hashemi-Najafabadi, S. (2015). Experimental design approach to the optimization of PAHs bioremediation from artificially contaminated soil: application of variables screening development. J. Environ. Heal. Sci. Eng., 13(1); 1-10.
Rhoads, J.D. (1996). Electrical conductivity & total dissolved solids, 417–435, in: Sparks, D. L., Page, A. L., Helmke, P. A., Loeppert, R. H., Soltanpour, P. N., Tabatabai, M. A., Johnston, C. T., & Sumner, M. . (Eds.), Methods of soil analysis Part 3. Madison, WI: Soil Science Society of American & American Society of Agronomy.
Sadañoski, M. A., Tatarin, A. S., Barchuk, M. L., Gonzalez, M., Pegoraro, C. N., Fonseca, M. I., Levin, Laura N., & Villalba, L. L. (2020). Evaluation of bioremediation strategies for treating recalcitrant halo-organic pollutants in soil environments. Ecotox. Environ. Safe., 202; 110929.
Sarkar, J., Roy, A., Sar, P., & Kazy, S. K. (2020). Accelerated bioremediation of petroleum refinery sludge through biostimulation & bioaugmentation of native microbiome. Emerg. Technol. Environ. Biorem., 23–65.
Song, Y. F., Jing, X., Fleischmann, S., & Wilke, B. M. (2002). Comparative study of extraction methods for the determination of PAHs from contaminated soils & sediments. Chemosphere, 48(9); 993–1001.
Sparks, D. L. (1996). Methods of soil analysis: Part 3 Chemical methods (D. L. Sparks, A. L. Page, P. A. Helmke, R. H. Loeppert, P. N. Soltanpour, M. A. Tabatabai, C. T. Johnston, & M. E. Sumner, Eds.). Madison: the Soil Science Society of America, Inc., American Society of Agronomy, Inc.
Speight, J. G., & Arjoon, K. K. (2012). Bioremediation of petroleum & petroleum products. Hoboken, NJ, USA: John Wiley & Sons, Inc. 
Sundberg, C., Smårs, S., & Jönsson, H. (2004). Low PH as an inhibiting factor in the transition from mesophilic to thermophilic phase in composting. Bioresource Technol., 95(2); 145–150.
Sutigoolabud, P., Senoo, K., Ongprasert, S., Mizuno, T., Mishima, T., Hisamatsu, M., & Obata, H. (2005). Decontamination of chlorate in longan plantation soils by bio-stimulation with molasses amendment. Soil Sci. Plant Nutrition, 51(4); 583–588.
Tabachnick, B. G., & Fidell, L. S. (2012). Using multivariate statistics (6th Ed.). Courier Companies, Inc. 
Tandon, H. L. S. (2005). Methods of analysis of soils, plants, waters, fertilisers & organic manures. Fertiliser Development & Consultation Organisation.
Tao, K., Zhang, X., Chen, X., Liu, X., Hu, X., & Yuan, X. (2019). Response of soil bacterial community to bioaugmentation with a plant residue-immobilized bacterial consortium for crude oil removal. Chemosphere, 222; 831–838.
Thomas, G.W. (1996). Soil pH & soil acidity, 475–490, in: Sparks, D. L. (Ed.), Methods of soil analysis Part 3: Chemical methods. Madison, WI: Soil Science Society of American & American Society of Agronomy.
Tremblay, J., Yergeau, E., Fortin, N., Cobanli, S., Elias, M., King, T. L., Lee, K., & Greer, C. W. (2017). Chemical dispersants enhance the activity of oil- & gas condensate-degrading marine bacteria. ISME J., 11(12); 2793–2808. 
Udume, O. A., Abu, G. O., Stanley, H. O., Vincent-Akpu, I. F., Momoh, Y., & Eze, M. O. (2023). Biostimulation of petroleum-contaminated soil using organic & inorganic amendments. Plants, 12(3); 1-14. 
Umor, N. A., Ismail, S., Abdullah, S., Huzaifah, M. H.R., Huzir, N. M., Mahmood, N. A.N., & Zahrim, A. Y. (2021). Zero waste management of spent mushroom compost. J. Mater. Cycles Waste Manag., 23(5); 1726–1736. 
USDA (2019), FoodData Central. available at https://fdc.nal.usda.gov/fdc-app.html#/food-details/168820/nutrients [31 May 2021].
Visentin, C., DaSilvaTrentin, A., Braun, A., & Thomé, A. (2019). Application of life cycle assessment as a tool for evaluating the sustainability of contaminated sites remediation: a systematic & bibliographic analysis. Sci. Total Environ., 672; 893-905.
Wei, Y., Chen, J., Wang, Y., Meng, T., & Li, M. (2021). Bioremediation of the petroleum contaminated desert steppe soil with Rhodococcus Erythropolis KB1 & its effect on the bacterial communities of the soils. Geomicrobiol. J., 38(10); 842–849. 
Wu, M., Ye, X., Chen, K., Li, W., Yuan, J., & Jiang, X. (2017). Bacterial community shift & hydrocarbon transformation during bioremediation of short-term petroleum-contaminated soil. Environ. Pollut., 223; 657–664. 
Wu, M., Wu, J., Zhang, X., & Ye, X. (2019). Effect of bioaugmentation & biostimulation on hydrocarbon degradation & microbial community composition in petroleum-contaminated loessal soil. Chemosphere, 237; 124456.
Wu, T., Xie, W. J., Yi, Y. L., Li, X. B., Yang, H. J., & Wang, J. (2012). Surface activity of salt-tolerant Serratia Spp., & crude oil biodegradation in saline soil. Plant, Soil Environ., 58(9); 412–416.
Xu, X., Liu, W., Tian, S., Wang, W., Qi, Q., Jiang, P., Gao, X., Li, F., Li, H., & Yu, H. (2018). Petroleum hydrocarbon-degrading bacteria for the remediation of oil pollution under aerobic conditions: a perspective analysis. Front. Microbiol., 9; 2885.
Yam, K. C., Geize, R. van der & Eltis, L. D. (2010). Catabolism of aromatic compounds & steroids by Rhodococcus: 133–169. 
Yousefi, K., Mohebbi, A., & Pichtel, J. (2021). Biodegradation of weathered petroleum hydrocarbons using organic waste amendments. Appl. Environ. Soil Sci., 2021; 1-12.
Zeneli, A., Kastanaki, E., Simantiraki, F., & Gidarakos, E. (2019). Monitoring the biodegradation of TPH & PAHs in refinery solid waste by biostimulation & bioaugmentation. J. Environ. Chem. Eng., 7(3); 103054.
Zhang, C., Wu, D., & Ren, H. (2020). Bioremediation of oil contaminated soil using agricultural wastes via microbial consortium. Sci. Rep., 10(1); 1–8. 
Zhang, J., Lin, X., Liu, W., Wang, Y., Zeng, J., & Chen, H. (2012). Effect of organic wastes on the plant-microbe remediation for removal of aged PAHs in soils. J. Environ. Sci., 24(8); 1476–1482.
Zhang, K., Wang, S., Guo, P., & Guo, S. (2021). Characteristics of organic carbon metabolism & bioremediation of petroleum-contaminated soil by a mesophilic aerobic biopile system. Chemosphere, 264(Part 2); 128521.