Abstract
To date, studies for bioremediation of oil-polluted hypersaline soils have been neglected or limited to specific spots. Hence, in this study, ten samples of oil field soils in the Khuzestan province of Iran were collected to evaluate bioremediation’s feasibility. These samples were analyzed for their physicochemical properties as well as the most probable number of total and hydrocarbon-degrading bacteria. Thirty-nine hydrocarbon-degrading bacteria were isolated from these soils over a 1-month incubation in an MSM medium enriched with diesel oil as the sole source of carbon. As revealed by 16S-rRNA analysis, the identified strains belonged to the genera Ochrobactrum, Microbacterium, and Bacillus with a high frequency of Ochrobactrum species. Additionally, by using degenerate primers, the third group of alkB gene was detected in Ochrobactrum and Microbacterium isolates through the touchdown nested PCR method for the first time. Ochrobactrum species possessing the alkB gene showed the highest population, and therefore, the highest adaptation to harsh environmental conditions. Most isolates showed outstanding results in the ability to grow with crude and diesel oil and tolerate high salt percentages, biosurfactant production, and emulsification activity, which are considered the most effective factors in bioremediation of such environments. Considering the soil analysis, limiting factors in bioremediation like available phosphorous, and the abundance of bacteria with remediation traits in these soils, these extremely polluted environments can be refined.
This is a preview of subscription content, log in via an institution to check access.
© 2015 Google Inc
Similar content being viewed by others
Data availability statement
The supplement data that support the findings of this study are available and was represented in supplementary materials.
References
Abou-Shanab, R. A. I., Eraky, M., Haddad, A. M., Abdel-Gaffar, A. R. B., & Salem, A. M. (2016). Characterization of crude oil degrading bacteria isolated from contaminated soils surrounding gas stations. Bulletin of Environmental Contamination and Toxicology, 97(5), 684–688. https://doi.org/10.1007/s00128-016-1924-2
Aislabie, J. M., Balks, M. R., Foght, J. M., & Waterhouse, E. J. (2004). Hydrocarbon spills on Antarctic soils: Effects and management. Environmental science & technology, 38(5), 1265–74. http://www.ncbi.nlm.nih.gov/pubmed/15046325. Accessed 17 January 2019
Al-Mailem, D., Eliyas, M., Khanafer, M., & Radwan, S. (2014). Culture-dependent and culture-independent analysis of hydrocarbonoclastic microorganisms indigenous to hypersaline environments in Kuwait. Microbial Ecology, 67(4), 857–865. https://doi.org/10.1007/s00248-014-0386-5
Al-Mailem, D. M., Eliyas, M., & Radwan, S. S. (2013). Oil-bioremediation potential of two hydrocarbonoclastic, diazotrophic Marinobacter strains from hypersaline areas along the Arabian Gulf coasts. Extremophiles, 17(3), 463–470. https://doi.org/10.1007/s00792-013-0530-z
Al-Mailem, D. M., Sorkhoh, N. A., Marafie, M., Al-Awadhi, H., Eliyas, M., & Radwan, S. S. (2010). Oil phytoremediation potential of hypersaline coasts of the Arabian Gulf using rhizosphere technology. Bioresource Technology, 101(15), 5786–5792. https://doi.org/10.1016/j.biortech.2010.02.082
Al-Mailem, D. M., Al-Deieg, M., Eliyas, M., & Radwan, S. S. (2017). Biostimulation of indigenous microorganisms for bioremediation of oily hypersaline microcosms from the Arabian Gulf Kuwaiti coasts. Journal of Environmental Management, 193, 576–583. https://doi.org/10.1016/j.jenvman.2017.02.054
Ali Khan, A. H., Tanveer, S., Alia, S., Anees, M., Sultan, A., Iqbal, M., & Yousaf, S. (2017). Role of nutrients in bacterial biosurfactant production and effect of biosurfactant production on petroleum hydrocarbon biodegradation. Ecological Engineering, 104, 158–164. https://doi.org/10.1016/j.ecoleng.2017.04.023
Ali, N., Dashti, N., Khanafer, M., Al-Awadhi, H., & Radwan, S. (2020). Bioremediation of soils saturated with spilled crude oil. Scientific Reports, 10(1), 1–9. https://doi.org/10.1038/s41598-019-57224-x
Almeida, C. M. R., Reis, I., Couto, M. N., Bordalo, A. A., & Mucha, A. P. (2013). Potential of the microbial community present in an unimpacted beach sediment to remediate petroleum hydrocarbons. Environmental Science and Pollution Research, 20(5), 3176–3184. https://doi.org/10.1007/s11356-012-1240-2
Atlas, R. M. (1981). Microbial degradation of petroleum hydrocarbons: an environmental perspective. Microbiological reviews, 45(1), 180–209. http://www.ncbi.nlm.nih.gov/pubmed/7012571. Accessed 27 September 2018
Baboshin, M. A., & Golovleva, L. A. (2012). Aerobic bacterial degradation of polycyclic aromatic hydrocarbons (PAHs) and its kinetic aspects. Microbiology, 81(6), 639–650. https://doi.org/10.1134/S0026261712060021
Bachoon, D. S., Hodson, R. E., & Araujo, R. (2001). Microbial community assessment in oil-impacted salt marsh sediment microcosms by traditional and nucleic acid-based indices. Journal of Microbiological Methods, 46(1), 37–49. https://doi.org/10.1016/S0167-7012(01)00260-3
Bahrami, S., Moore, F., & Keshavarzi, B. (2019). Evaluation, source apportionment and health risk assessment of heavy metal and polycyclic aromatic hydrocarbons in soil and vegetable of Ahvaz metropolis. Human and Ecological Risk Assessment. https://doi.org/10.1080/10807039.2019.1692300
Banerjee, A., Sarkar, S., Cuadros-Orellana, S., & Bandopadhyay, R. (2019). Exopolysaccharides and biofilms in mitigating salinity stress: The biotechnological potential of halophilic and soil-inhabiting PGPR microorganisms. In Microorganisms in Saline Environments: Strategies and Functions (pp. 133–153). https://doi.org/10.1007/978-3-030-18975-4_6
Batista, S. B., Mounteer, A. H., Amorim, F. R., & Tótola, M. R. (2006). Isolation and characterization of biosurfactant/bioemulsifier-producing bacteria from petroleum contaminated sites. Bioresource Technology, 97(6), 868–875. https://doi.org/10.1016/j.biortech.2005.04.020
Bayat, Z., Hassanshahian, M., & Askari Hesni, M. (2015). Enrichment and isolation of crude oil degrading bacteria from some mussels collected from the Persian Gulf. Marine Pollution Bulletin, 101(1), 85–91. https://doi.org/10.1016/j.marpolbul.2015.11.021
Bonfá, M. R. L., Grossman, M. J., Mellado, E., & Durrant, L. R. (2011). Biodegradation of aromatic hydrocarbons by Haloarchaea and their use for the reduction of the chemical oxygen demand of hypersaline petroleum produced water. Chemosphere, 84(11), 1671–1676. https://doi.org/10.1016/j.chemosphere.2011.05.005
Bossert I., and Bartha, R. (1984). The fate of petroleum in soil ecosystem. Atlas, R.M. (Ed.) Petroleum microbiology, Macmillan Publishing Company, New York, 435–473. http://www.sciepub.com/reference/146572. Accessed 18 January 2019
Bouyoucos, G. J. (1962). Hydrometer method improved for making particle size analyses of soils1. Agronomy Journal, 54(5), 464. https://doi.org/10.2134/agronj1962.00021962005400050028x
Bremner, J. M. (1996). Nitrogen-Total. In D.L. Sparks A.L. Page P.A. Helmke R.H. Loeppert P. N. Soltanpour M. A. Tabatabai C. T. Johnston M. E. Sumner (Ed.), Methods of soil analysis. Part 3: Chemical methods (pp. 1085–1123). Soil Science Society of America and American Society of Agronomy, Madison. https://doi.org/10.2136/sssabookser5.3.c37
Cai, P., Ning, Z., Liu, Y., He, Z., Shi, J., & Niu, M. (2020). Diagnosing bioremediation of crude oil-contaminated soil and related geochemical processes at the field scale through microbial community and functional genes. Annals of Microbiology, 70(1), 36. https://doi.org/10.1186/s13213-020-01580-x
da Cerozi, B., & S., & Fitzsimmons, K. (2016). The effect of pH on phosphorus availability and speciation in an aquaponics nutrient solution. Bioresource Technology, 219, 778–781. https://doi.org/10.1016/j.biortech.2016.08.079
Chen, K. F., Kao, C. M., Chen, C. W., Surampalli, R. Y., & Lee, M. S. (2010). Control of petroleum-hydrocarbon contaminated groundwater by intrinsic and enhanced bioremediation. Journal of Environmental Sciences, 22(6), 864–871. https://doi.org/10.1016/S1001-0742(09)60190-X
Comey, C. T., Koons, B. W., Presley, K. W., Smerick, J. B., Sobieralski, C. A., Stanley, D. M., & Baechtel, F. S. (1994). DNA extraction strategies for amplified fragment length polymorphism analysis. Journal of Forensic Sciences, 39(5), 13711J. https://doi.org/10.1520/jfs13711j
Dastgheib, S. M. M., Amoozegar, M. A., Khajeh, K., Shavandi, M., & Ventosa, A. (2012). Biodegradation of polycyclic aromatic hydrocarbons by a halophilic microbial consortium. Applied Microbiology and Biotechnology, 95(3), 789–798. https://doi.org/10.1007/s00253-011-3706-4
Dastgheib, S. M. M., Amoozegar, M. A., Khajeh, K., & Ventosa, A. (2011). A halotolerant Alcanivorax sp. strain with potential application in saline soil remediation. Applied Microbiology and Biotechnology, 90(1), 305–312. https://doi.org/10.1007/s00253-010-3049-6
Ebadi, A., Khoshkholgh Sima, N. A., Olamaee, M., Hashemi, M., & Ghorbani Nasrabadi, R. (2017). Effective bioremediation of a petroleum-polluted saline soil by a surfactant-producing Pseudomonas aeruginosa consortium. Journal of Advanced Research, 8(6), 627–633. https://doi.org/10.1016/j.jare.2017.06.008
Eneje, R. C., & N. C. and U. I. E. (2012). Amelioration of chemical properties of crude oil contaminated soil using compost from Calapoigonium mucunoides and poultry manure. International Research Journal of Agricultural Science and Soil Science, 2(June), 246–251.
Fathepure, B. Z. (2014). Recent studies in microbial degradation of petroleum hydrocarbons in hypersaline environments Frontiers in Microbiology 5 https://doi.org/10.3389/fmicb.2014.00173
Frenzel, M., Scarlett, A., Rowland, S. J., Galloway, T. S., Burton, S. K., Lappin-Scott, H. M., & Booth, A. M. (2010). Complications with remediation strategies involving the biodegradation and detoxification of recalcitrant contaminant aromatic hydrocarbons. Science of the Total Environment, 408(19), 4093–4101. https://doi.org/10.1016/j.scitotenv.2010.04.042
Fuentes, S., Méndez, V., Aguila, P., & Seeger, M. (2014). Bioremediation of petroleum hydrocarbons: Catabolic genes, microbial communities, and applications. Applied Microbiology and Biotechnology, 98(11), 4781–4794. https://doi.org/10.1007/s00253-014-5684-9
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. Frontiers in Microbiology, 12, 363. https://doi.org/10.3389/fmicb.2021.642215
Giebler, J., Wick, L. Y., Chatzinotas, A., & Harms, H. (2013). Alkane-degrading bacteria at the soil-litter interface: Comparing isolates with T-RFLP-based community profiles. FEMS Microbiology Ecology, 86(1), 45–58. https://doi.org/10.1111/1574-6941.12097
Goswami, M., & Deka, S. (2019). Biosurfactant production by a rhizosphere bacteria Bacillus altitudinis MS16 and its promising emulsification and antifungal activity. Colloids and Surfaces B: Biointerfaces, 178(March), 285–296. https://doi.org/10.1016/j.colsurfb.2019.03.003
Hamdi, H., Benzarti, S., Manusadžianas, L., Aoyama, I., & Jedidi, N. (2007). Solid-phase bioassays and soil microbial activities to evaluate PAH-spiked soil ecotoxicity after a long-term bioremediation process simulating landfarming. Chemosphere, 70(1), 135–143. https://doi.org/10.1016/j.chemosphere.2007.06.043
Hassanshahian, M., Ahmadinejad, M., Tebyanian, H., & Kariminik, A. (2013). Isolation and characterization of alkane degrading bacteria from petroleum reservoir waste water in Iran (Kerman and Tehran provenances). Marine Pollution Bulletin, 73(1), 300–305. https://doi.org/10.1016/j.marpolbul.2013.05.002
Hassanshahian, M., Emtiazi, G., & Cappello, S. (2012). Isolation and characterization of crude-oil-degrading bacteria from the Persian Gulf and the Caspian Sea. Marine Pollution Bulletin, 64(1), 7–12. https://doi.org/10.1016/j.marpolbul.2011.11.006
Hassanshahian, M., Emtiazi, G., Kermanshahi, R. K., & Cappello, S. (2010). Comparison of oil degrading microbial communities in sediments from the Persian Gulf and Caspian Sea. Soil and Sediment Contamination, 19(3), 277–291. https://doi.org/10.1080/15320381003695215
Head, I. M., Jones, D. M., & Larter, S. R. (2003). Biological activity in the deep subsurface and the origin of heavy oil. Nature, 426(6964), 344–352. https://doi.org/10.1038/nature02134
Holt, S. G., Kriey, N. R., Sneath, P. H. A., Staley, J. T., Williams, S. T. (1998). Bergey’s manual of determinative bacteriology. American Journal of Public Health and the Nations Health. Williams and Wilkins, New York.
Iturbe, R., Castro, A., Perez, G., Flores, C., & Torres, L. G. (2008). TPH and PAH concentrations in the subsoil of polyduct segments, oil pipeline pumping stations, and right-of-way pipelines from Central Mexico. Environmental Geology, 55(8), 1785–1795. https://doi.org/10.1007/s00254-007-1129-4
IUSS Working Group WRB. (2014). World Reference Base for Soil Resources 2014: International soil classification system for naming soils and creating legends for soil maps. (E. M. Peter Schad, Cornie van Huysteen, Ed.) World Reference Base for Soil Resources 2014, update 2015 (Vol. World Soil). FAO. https://doi.org/10.1017/S0014479706394902
Jackson, M. L. (1958). Soil chemical analysis. Wiley. https://doi.org/10.1002/jpln.19590850311
Jarvis, B., Wilrich, C., & Wilrich, P. T. (2010). Reconsideration of the derivation of most probable numbers, their standard deviations, confidence bounds and rarity values. Journal of Applied Microbiology, 109(5), 1660–1667. https://doi.org/10.1111/j.1365-2672.2010.04792.x
Khemili-Talbi, S., Kebbouche-Gana, S., Akmoussi-Toumi, S., Angar, Y., & Gana, M. L. (2015). Isolation of an extremely halophilic arhaeon Natrialba sp. C21 able to degrade aromatic compounds and to produce stable biosurfactant at high salinity. Extremophiles, 19(6), 1109–1120. https://doi.org/10.1007/s00792-015-0783-9
Kim, O. S., Cho, Y. J., Lee, K., Yoon, S. H., Kim, M., Na, H., et al. (2012). Introducing EzTaxon-e: A prokaryotic 16s rRNA gene sequence database with phylotypes that represent uncultured species. International Journal of Systematic and Evolutionary Microbiology, 62(PART 3), 716–721. https://doi.org/10.1099/ijs.0.038075-0
Kloos, K., Munch, J. C., & Schloter, M. (2006). A new method for the detection of alkane-monooxygenase homologous genes (alkB) in soils based on PCR-hybridization. Journal of Microbiological Methods, 66(3), 486–496. https://doi.org/10.1016/j.mimet.2006.01.014
Kohno, T., Sugimoto, Y., & Sei, K. (2002). Desing of PCR primers and gene probes for general detection of alkane-degrading bacteria. Japanese Society of Microbial Ecology, 17(3), 114–121. https://doi.org/10.1264/jsme2.17.114
Kumar, C. G., Sujitha, P., Mamidyala, S. K., Usharani, P., Das, B., & Reddy, C. R. (2014). Ochrosin, a new biosurfactant produced by halophilic Ochrobactrum sp. strain BS-206 (MTCC 5720): Purification, characterization and its biological evaluation. Process Biochemistry, 49(10), 1708–1717. https://doi.org/10.1016/j.procbio.2014.07.004
Kumari, B., Kriti, Singh, G., Sinam, G., & Singh, D. P. (2020). Microbial remediation of crude oil-contaminated sites. In Environmental concerns and sustainable development (pp. 333–351). Springer Singapore. https://doi.org/10.1007/978-981-13-5889-0_17
Kuyukina, M. S., & Ivshina, I. B. (2010). Application of Rhodococcus in Bioremediation of Contaminated Environments. https://doi.org/10.1007/978-3-642-12937-7_9
Lane, D. J. (1991). 16S/23S rRNA sequencing. In: Stackebrandt, E. and Goodfellow, M., Eds., Nucleic acid techniques in bacterial systematics. John Wiley & Sons Chichester, 115–175.
Leahy, J. G., & Colwell, R. R. (1990). Microbial degradation of hydrocarbons in the environment. Microbiological reviews, 54(3), 305–15. http://www.ncbi.nlm.nih.gov/pubmed/2215423. Accessed 17 January 2019
Lei, X., Jia, Y., Chen, Y., & Hu, Y. (2019). Simultaneous nitrification and denitrification without nitrite accumulation by a novel isolated Ochrobactrum anthropic LJ81. Bioresource Technology, 272(September 2018), 442–450. https://doi.org/10.1016/j.biortech.2018.10.060
Leite, G. G. F., Figueirôa, J. V., Almeida, T. C. M., Valões, J. L., Marques, W. F., Duarte, M. D. D. C., & Gorlach-Lira, K. (2016). Production of rhamnolipids and diesel oil degradation by bacteria isolated from soil contaminated by petroleum. Biotechnology Progress, 32(2), 262–270. https://doi.org/10.1002/btpr.2208
Leys, N. M., Bastiaens, L., Verstraete, W., & Springael, D. (2005). Influence of the carbon/nitrogen/phosphorus ratio on polycyclic aromatic hydrocarbon degradation by Mycobacterium and Sphingomonas in soil. Applied Microbiology and Biotechnology, 66(6), 726–736. https://doi.org/10.1007/s00253-004-1766-4
Li, W., Zhang, Y., Wang, M. D., & Shi, Y. (2005). Biodesulfurization of dibenzothiophene and other organic sulfur compounds by a newly isolated Microbacterium strain ZD-M2. FEMS Microbiology Letters, 247(1), 45–50. https://doi.org/10.1016/j.femsle.2005.04.025
Lima, J. M. S., Pereira, J. O., Batista, I. H., Pereira Junior, R. C., Barroso, H. dos S., Neto, P. de Q. C., et al. (2017). Biossurfactantes produzidos por Microbacterium sp., isolada de macrófita aquática em área impactada por hidrocarbonetos no Rio Negro, Manaus, Amazonas. Acta Scientiarum - Biological Sciences, 39(1), 13–20. https://doi.org/10.4025/actascibiolsci.v39i1.33842
Lin, T. C., Pan, P. T., & Cheng, S. S. (2010). Ex situ bioremediation of oil-contaminated soil. Journal of Hazardous Materials, 176(1–3), 27–34. https://doi.org/10.1016/j.jhazmat.2009.10.080
Liu, Q., Tang, J., Bai, Z., Hecker, M., & Giesy, J. P. (2015). Distribution of petroleum degrading genes and factor analysis of petroleum contaminated soil from the Dagang Oilfield. China. Scientific Reports, 5(May), 1–12. https://doi.org/10.1038/srep11068
Lü, J., Wu, X., Jiang, Y., Cai, X., Huang, L., Yang, Y., et al. (2014). An extremophile Microbacterium strain and its protease production under alkaline conditions. Journal of Basic Microbiology, 54(5), 378–385. https://doi.org/10.1002/jobm.201200553
Martins, L. F., & Peixoto, R. S. (2012). Biodegradation of petroleum hydrocarbons in hypersaline environments. Brazilian Journal of Microbiology, 43(3), 865–872. https://doi.org/10.1590/S1517-83822012000300003
Mikkonen, A., Kondo, E., Lappi, K., Wallenius, K., Lindström, K., Hartikainen, H., & Suominen, L. (2011). Contaminant and plant-derived changes in soil chemical and microbiological indicators during fuel oil rhizoremediation with Galega orientalis. Geoderma, 160(3–4), 336–346. https://doi.org/10.1016/j.geoderma.2010.10.001
Mnif, S., Chamkha, M., Labat, M., & Sayadi, S. (2011). Simultaneous hydrocarbon biodegradation and biosurfactant production by oilfield-selected bacteria. Journal of Applied Microbiology, 111(3), 525–536. https://doi.org/10.1111/j.1365-2672.2011.05071.x
Moshabaki Isfahani, F., Tahmourespour, A., Hoodaji, M., Ataabadi, M., & Mohammadi, A. (2018). Characterizing the new bacterial isolates of high yielding exopolysaccharides under hypersaline conditions. Journal of Cleaner Production, 185, 922–928. https://doi.org/10.1016/j.jclepro.2018.03.030
Muthukrishnan, T., & Abed, R. M. M. (2018). Effects of irrigation on alkane biodegradation of oil-contaminated desert soils. Environmental Processes, 5(3), 631–648. https://doi.org/10.1007/s40710-018-0325-4
Nedelkova, M., Merroun, M. L., Rossberg, A., Hennig, C., & Selenska-Pobell, S. (2007). Microbacterium isolates from the vicinity of a radioactive waste depository and their interactions with uranium. FEMS Microbiology Ecology, 59(3), 694–705. https://doi.org/10.1111/j.1574-6941.2006.00261.x
Oberoi, A. S., & Philip, L. (2017). Variation in toxicity during the biodegradation of various heterocyclic and homocyclic aromatic hydrocarbons in single and multi-substrate systems. Ecotoxicology and Environmental Safety, 135, 337–346. https://doi.org/10.1016/j.ecoenv.2016.10.016
Ölinger, R., Beck, T., Heilmann, B., & Beese, F. (1996). Soil respiration. In Methods in soil biology (pp. 93–110). Berlin, Heidelberg: Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-642-60966-4_6
Olsen, S. R., Cole, C. V., Watandbe, F., & Dean, L. (1954). Estimation of available phosphorus in soil by extraction with sodium bicarbonate. Journal of Chemical Information and Modeling, 53(9), 1689–1699. https://doi.org/10.1017/CBO9781107415324.004
Oren, A. (2013). Life at high salt concentrations. In The prokaryotes: Prokaryotic communities and ecophysiology (Vol. 9783642301, pp. 421–440). Berlin, Heidelberg: Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-642-30123-0_57
Ortega, M. F., Guerrero, D. E., García-Martínez, M. J., Bolonio, D., Llamas, J. F., Canoira, L., & Gallego, J. L. R. (2018). Optimization of landfarming amendments based on soil texture and crude oil concentration. Water, Air, and Soil Pollution, 229(7). https://doi.org/10.1007/s11270-018-3891-1
Pinedo, J., Ibáñez, R., Lijzen, J. P. A., & Irabien, Á. (2013). Assessment of soil pollution based on total petroleum hydrocarbons and individual oil substances. Journal of Environmental Management, 130, 72–79. https://doi.org/10.1016/j.jenvman.2013.08.048
Płaza, G. A., Zjawiony, I., & Banat, I. M. (2006). Use of different methods for detection of thermophilic biosurfactant-producing bacteria from hydrocarbon-contaminated and bioremediated soils. Journal of Petroleum Science and Engineering, 50(1), 71–77. https://doi.org/10.1016/j.petrol.2005.10.005
Powell, S. M., Bowman, J. P., Ferguson, S. H., & Snape, I. (2010). The importance of soil characteristics to the structure of alkane-degrading bacterial communities on sub-Antarctic Macquarie Island. Soil Biology and Biochemistry, 42(11), 2012–2021. https://doi.org/10.1016/j.soilbio.2010.07.027
Qin, X., Tang, J. C., Li, D. S., & Zhang, Q. M. (2012). Effect of salinity on the bioremediation of petroleum hydrocarbons in a saline-alkaline soil. Letters in Applied Microbiology, 55(3), 210–217. https://doi.org/10.1111/j.1472-765X.2012.03280.x
Rezaei, A., Hassani, H., Fard Mousavi, S. B., & Jabbari, N. (2019). Evaluation of heavy metals concentration in Jajarm bauxite deposit in northeast of Iran using environmental pollution indices. Malaysian Journal of Geosciences, 3(1), 12–20. https://doi.org/10.26480/mjg.01.2019.12.20
Richards, L. A. (1954). Diagnosis and improvement of saline and alkali soils. U.S. Department of Agriculture, Washington, DC (USDA Handb.). https://doi.org/10.1117/12.582159
Riis, V., Kleinsteuber, S., & Babel, W. (2003). Influence of high salinities on the degradation of diesel fuel by bacterial consortia. Canadian Journal of Microbiology, 49(11), 713–721. https://doi.org/10.1139/w03-083
Schwab, A. P., Su, J., Wetzel, S., Pekarek, S., & Banks, M. K. (1999). Extraction of petroleum hydrocarbons from soil by mechanical shaking. Environmental Science and Technology, 33(11), 1940–1945. https://doi.org/10.1021/es9809758
Soil Survey Staff. (2014). Keys to soil taxonomy (12th ed.). USDA Natural Resources Conservation Service.
Sorkhoh, N. A., Ali, N., Salamah, S., Eliyas, M., Khanafer, M., & Radwan, S. S. (2010). Enrichment of rhizospheres of crop plants raised in oily sand with hydrocarbon-utilizing bacteria capable of hydrocarbon consumption in nitrogen free media. International Biodeterioration and Biodegradation, 64(7), 659–664. https://doi.org/10.1016/j.ibiod.2010.08.002
Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30(12), 2725–2729. https://doi.org/10.1093/molbev/mst197
Thavasi, R., Sharma, S., & Jayalakshmi, S. (2013). Evaluation of screening methods for the isolation of biosurfactant producing marine bacteria. Journal of Petroleum & Environmental Biotechnology, 04(02), 1–6. https://doi.org/10.4172/2157-7463.s1-001
Vaishnavi, J., Devanesan, S., AlSalhi, M. S., Rajasekar, A., Selvi, A., Srinivasan, P., & Govarthanan, M. (2021). Biosurfactant mediated bioelectrokinetic remediation of diesel contaminated environment. Chemosphere, 264, 128377. https://doi.org/10.1016/j.chemosphere.2020.128377
Varadavenkatesan, T., & Murty, V. R. (2013). Production and properties of a lipopeptide biosurfactant by B. subtilis subsp. inaquosorum. Journal of Microbiology and Biotechnology Research, 3(4), 63–73. http://eprints.manipal.edu/137669/
Veil, J. A., Puder, M. G., Elcock, D., & Redweik, R. J. Jr. (2004). A white paper describing produced water from production of crude oil, natural gas, and coal bed methane. Prepared by: Argonne National Laboratory. Prepared for: U.S. Department of Energy National Energy Technology Laboratory Under Contract W-31–109-Eng-38 (p. 87). https://doi.org/10.2172/821666
Ventosa, A., & Arahal, D. R. (2009). Physico-chemical characteristics of hypersaline environments and their biodiversity. Extremophiles, 2, 247–262.
Ventosa, A., Nieto, J. J., & Oren, A. (1998). Biology of moderately halophilic aerobic bacteria. Microbiology and Molecular Biology Reviews, 62(2), 504–544. https://doi.org/10.1128/mmbr.62.2.504-544.1998
Walkley, A. J., & Black, I. A. (1934). Estimation of soil organic carbon by the chromic acid titration method. Soil Science, 37, 29–38.
Walworth, J. L., Woolard, C. R., Braddock, J. F., & Reynolds, C. M. (1997). Enhancement and inhibition of soil petroleum biodegradation through the use of fertilizer nitrogen: An approach to determining optimum levels. Soil and Sediment Contamination, 6(5), 465–480. https://doi.org/10.1080/15320389709383580
Wang, W., & Shao, Z. (2012). Diversity of flavin-binding monooxygenase genes (almA) in marine bacteria capable of degradation long-chain alkanes. FEMS Microbiology Ecology, 80(3), 523–533. https://doi.org/10.1111/j.1574-6941.2012.01322.x
Wang, W., Wang, L., & Shao, Z. (2010a). Diversity and abundance of oil-degrading bacteria and alkane hydroxylase (alkB) genes in the subtropical seawater of Xiamen Island. Microbial Ecology, 60(2), 429–439. https://doi.org/10.1007/s00248-010-9724-4
Wang, X., Feng, J., & Zhao, J. (2010b). Effects of crude oil residuals on soil chemical properties in oil sites, Momoge Wetland. China. Environmental Monitoring and Assessment, 161(1–4), 271–280. https://doi.org/10.1007/s10661-008-0744-1
Wang, X. Y., Feng, J., & Wang, J. (2009). Petroleum hydrocarbon contamination and impact on soil characteristics from oilfield Momoge wetland. Environmental Science, 30(8), 2394–2401.
Wang, Y., Feng, J., Lin, Q., Lyu, X., Wang, X., & Wang, G. (2013). Effects of crude oil contamination on soil physical and chemical properties in momoge wetland of China. Chinese Geographical Science, 23(6), 708–715. https://doi.org/10.1007/s11769-013-0641-6
Wrenn, B. A., & Venosa, A. D. (1996). Selective enumeration of aromatic and aliphatic hydrocarbon degrading bacteria by a most-probable-number procedure. Canadian Journal of Microbiology, 42(3), 252–258. https://doi.org/10.1139/m96-037
Wu, M., Li, W., Dick, W. A., Ye, X., Chen, K., Kost, D., & Chen, L. (2017). Bioremediation of hydrocarbon degradation in a petroleum-contaminated soil and microbial population and activity determination. Chemosphere, 169, 124–130. https://doi.org/10.1016/j.chemosphere.2016.11.059
Yang, Y., Wang, J., Liao, J., Xie, S., & Huang, Y. (2014). Abundance and diversity of soil petroleum hydrocarbon-degrading microbial communities in oil exploring areas. Applied Microbiology and Biotechnology, 99(4), 1935–1946. https://doi.org/10.1007/s00253-014-6074-z
Youssef, N. H., Duncan, K. E., Nagle, D. P., Savage, K. N., Knapp, R. M., & McInerney, M. J. (2004). Comparison of methods to detect biosurfactant production by diverse microorganisms. Journal of Microbiological Methods, 56(3), 339–347. https://doi.org/10.1016/j.mimet.2003.11.001
Yu, Y., Zhang, Y., Zhao, N., Guo, J., Xu, W., Ma, M., & Li, X. (2020). Remediation of crude oil-polluted soil by the bacterial rhizosphere community of Suaeda salsa revealed by 16S rRNA genes. International Journal of Environmental Research and Public Health, 17(5), 1471. https://doi.org/10.3390/ijerph17051471
Zhao, B., Wang, H., Mao, X., & Li, R. (2009). Biodegradation of phenanthrene by a halophilic bacterial consortium under aerobic conditions. Current Microbiology, 58(3), 205–210. https://doi.org/10.1007/s00284-008-9309-3
Zheng, J., Feng, J. Q., Zhou, L., Mbadinga, S. M., Gu, J. D., & Mu, B. Z. (2018). Characterization of bacterial composition and diversity in a long-term petroleum contaminated soil and isolation of high-efficiency alkane-degrading strains using an improved medium. World Journal of Microbiology and Biotechnology, 34(2). https://doi.org/10.1007/s11274-018-2417-8
Acknowledgements
We appreciate Mr. Moradi from the National Iranian South Oil Company for his cooperation in preparing various soil samples. We would like to express our gratitude to Dr. Mahyar Marzban for his valuable cooperation.
Funding
This research received financial support from the University College of Agriculture and Natural Resources, University of Tehran.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Highlights
- The feasibility of bioremediation in oil-polluted hypersaline soils of Khuzestan province was investigated.
- Thirty-nine hydrocarbondegrading bacteria were isolated and most of them showed effective bioremediation traits for oil-polluted soils of Khuzestan.
- In these soils, Ochrobactrum species possessing the alkB gene showed the highest population and the highest adaptation to harsh environmental conditions.
- Phosphorus is an essential limiting factor in the bioremediation of these soils by considering the diversity of bacteria and soil physicochemical characteristics.
- The third group of alkB gene was detected in Ochrobactrum, and Microbacterium isolates through the touchdown nested PCR method.
- MPN of degrading bacteria did not have any correlation with the amount of hydrocarbon pollution and other variables.
- MPN of degrading bacteria had a linear relationship with variables of soil respiration, organic carbon, available P, total N, EC, pH, and TPH through regression line.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kalami, R., Pourbabaee, AA. Investigating the potential of bioremediation in aged oil-polluted hypersaline soils in the south oilfields of Iran. Environ Monit Assess 193, 517 (2021). https://doi.org/10.1007/s10661-021-09304-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10661-021-09304-7