Abstract
Oil-contaminated soil is the main challenge for oil-rich countries, and this study aimed to investigate the performance of the H2O2-stimulated slurry bioreactor for the bioremediation of real oil-contaminated soil. The effect of biomass concentration, soil to water (S/W) ratio, slurry temperature, pH, and H2O2 concentration were optimized for the removal of total petroleum hydrocarbons (TPH) from oil-contaminated soil. TPH removal efficiency, biosurfactants production, and peroxidase and dehydrogenase activities were measured. The optimum conditions for the complete biodegradation of 32 \({\text{g}}_{{{\text{TPH}}}} /{\text{kg}}_{{{\text{soil}}}}\) in the slurry bioreactor during 6 days were biomass of 2250 mg/L, S/W ratio of 20%, the temperature of 30 °C, pH of 7, and an H2O2 concentration of 120 mg/L. The highest peroxidase, dehydrogenase, surfactin, and rhamnolipid formation were also obtained under optimum conditions. The results pointed out that complete biodegradation of 32 g/kg of TPH in oil-contaminated soil at a short reaction time of 6 days is achievable in the developed process operated under optimum conditions. The GC/FID analysis of solid and liquid phases showed that the bioprocess completely biodegraded the different TPH fractions. H2O2 efficiently stimulated the biosurfactant-generating bacteria to produce peroxidase and thereby accelerating the bioremediation rate. Accordingly, an H2O2-mediated slurry bioreactor inoculated with biosurfactant/peroxidase-generating bacteria is a promising technique for cleaning up oil-contaminated soils.
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References
Abena MTB, Li T, Shah MN, Zhong W (2019) Biodegradation of total petroleum hydrocarbons (TPH) in highly contaminated soils by natural attenuation and bioaugmentation. Chemosphere 234:864–874
Aghayani E, Moussavi G, Naddafi K (2019) Improved peroxidase-mediated biodegradation of toluene vapors in the moving-bed activated sludge diffusion (MASD) process using biosurfactant-generating biomass stimulated with H2O2. J Hazard Mater 361:259–266
Ali N, Dashti N, Khanafer M, Al-Awadhi H, Radwan S (2020) Bioremediation of soils saturated with spilled crude oil. Sci Rep 10(1):1–9
Alneyadi AH, Ashraf SS (2016) Differential enzymatic degradation of thiazole pollutants by two different peroxidases–a comparative study. Chem Eng J 303:529–538
Álvarez LM, Balbo AL, Mac Cormack W, Ruberto LAM (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
Atack JM, Kelly DJ (2006) Structure, mechanism and physiological roles of bacterial cytochrome c peroxidases. Adv Microb Physiol 52:73–106
Azubuike CC, Chikere CB, Okpokwasili GC (2016) Bioremediation techniques–classification based on site of application: principles, advantages, limitations and prospects. World J Microbiol Biotechnol 32(11):1–18
Bååth E, Anderson T-H (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35(7):955–963
Bahmani F, Ataei SA, Mikaili MA (2018) The effect of moisture content variation on the bioremediation of hydrocarbon contaminated soils: modeling and experimental investigation. J Environ Anal Chem 5(2):236
Banat IM (1995) Biosurfactants production and possible uses in microbial enhanced oil recovery and oil pollution remediation: a review. Bioresour Technol 51(1):1–12
Barbeau C, Deschenes L, Karamanev D, Comeau Y, Samson R (1997) Bioremediation of pentachlorophenol-contaminated soil by bioaugmentation using activated soil. Appl Microbiol Biotechnol 48(6):745–752
Bezerra MA, Santelli RE, Oliveira EP, Villar LS, Escaleira LA (2008) Response surface methodology (RSM) as a tool for optimization in analytical chemistry. Talanta 76(5):965–977
Chen C, Sun N, Li D, Long S, Tang X, Xiao G, Wang L (2018) Optimization and characterization of biosurfactant production from kitchen waste oil using Pseudomonas aeruginosa. Environ Sci Pollut Res 25(15):14934–14943
Chiu H, Verpoort F, Liu J, Chang Y, Kao C (2017) Using intrinsic bioremediation for petroleum–hydrocarbon contaminated groundwater cleanup and migration containment: effectiveness and mechanism evaluation. J Taiwan Inst Chem Eng 72:53–61
Cisterna-Osorio P, Lavin AG, Sastre-Andres H (2015) Impact of previous acclimatization of biomass and alternative substrates in sunflower oil biodegradation. DYNA 82(193):56–61
Comeau Y, Greer CW, Samson R (1993) Role of inoculum preparation and density on the bioremediation of 2, 4-D-contaminated soil by bioaugmentation. Appl Microbiol Biotechnol 38(5):681–687
Das N, Chandran P (2011) Microbial degradation of petroleum hydrocarbon contaminants: an overview. Biotechnol Res Int 11:1–13
Das K, Mukherjee AK (2007) Crude petroleum-oil biodegradation efficiency of Bacillus subtilis and Pseudomonas aeruginosa strains isolated from a petroleum-oil contaminated soil from North-East India. Bioresour Technol 98(7):1339–1345
Di Gennaro P, Franzetti A, Bestetti G, Lasagni M, Pitea D, Collina E (2008) Slurry phase bioremediation of PAHs in industrial landfill samples at laboratory scale. Waste Manag 28(8):1338–1345
Doick KJ, Semple KT (2003) The effect of soil: water ratios on the mineralisation of phenanthrene: LNAPL mixtures in soil. FEMS Microbiol Lett 220(1):29–33
Effendi AJ, Kamath R, McMillen S, Sihota N, Zuo E, Sra K, Kong D, Wisono T, Syakir J (2017) Strategies for enhancing bioremediation for hydrocarbon-impacted soils. In: SPE Asia Pacific health, safety, security, environment and social responsibility conference. Society of Petroleum Engineers, Kuala Lumpur, Malaysia. https://doi.org/10.2118/185196-MS
Fanaei F, Moussavi G, Shekoohiyan S (2020) Enhanced treatment of the oil-contaminated soil using biosurfactant-assisted washing operation combined with H2O2-stimulated biotreatment of the effluent. J Environ Manag 271:110941
Fava F, Berselli S, Conte P, Piccolo A, Marchetti L (2004) Effects of humic substances and soya lecithin on the aerobic bioremediation of a soil historically contaminated by polycyclic aromatic hydrocarbons (PAHs). Biotechnol Bioeng 88(2):214–223
Ghaly A, Mahmoud N (2006) Optimum conditions for measuring dehydrogenase activity of Aspergillus niger using TTC. Am J Biochem Biotechnol 2:186–194
Ghorbanian M, Moussavi G, Farzadkia M (2014) Investigating the performance of an up-flow anoxic fixed-bed bioreactor and a sequencing anoxic batch reactor for the biodegradation of hydrocarbons in petroleum-contaminated saline water. Int Biodeter Biodegrad 90:106–114
Goudarztalejerdi A, Tabatabaei M, Eskandari MH, Mowla D (2019) Optimization conditions for maximum oil bioremediation and biopolymer production by Pseudomonads. Iran J Sci Technol Trans A 43(4):1439–1446
Hamzah A, Zarin MA, Hamid AA, Omar O, Senafi SJSM (2012) Optimal physical and nutrient parameters for growth of Trichoderma virens UKMP-1M for heavy crude oil degradation. Sains Malays 41(1):71–79
Karigar C, Rao S (2011) Role of microbial enzymes in the bioremediation of pollutants: a review. Enzyme Res 2011:1–11
Kaya A, Mariotti M, Gladyshev VN (2017) Cytochrome c peroxidase facilitates the beneficial use of H2O2 in prokaryotes. Proc Natl Acad Sci 114(33):8678–8680
Kuppusamy S, Thavamani P, Megharaj M, Naidu R (2016) Bioaugmentation with novel microbial formula vs. natural attenuation of a long-term mixed contaminated soil—treatability studies in solid-and slurry-phase microcosms. Water Air Soil Pollut 227(1):1–15
Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Mol Biol Rev 54(3):305–315
Lee P-H, Ong SK, Golchin J, Nelson GS (2001) Use of solvents to enhance PAH biodegradation of coal tar. Water Res 35(16):3941–3949
Lee S-H, Ji W, Kang DM, Kim M-S (2018) Effect of soil water content on heavy mineral oil biodegradation in soil. J Soils Sediments 18(3):983–991
Lin T-C, Shen F-T, Chang J-S, Young C-C, Arun A, Lin S-Y, Chen T-L (2009) Hydrocarbon degrading potential of bacteria isolated from oil-contaminated soil. J Taiwan Inst Chem Eng 40(5):580–582
Machín-Ramírez C, Okoh A, Morales D, Mayolo-Deloisa K, Quintero R, Trejo-Hernández M (2008) Slurry-phase biodegradation of weathered oily sludge waste. Chemosphere 70(4):737–744
Margesin R, Schinner F (1997) Effect of temperature on oil degradation by a psychrotrophic yeast in liquid culture and in soil. FEMS Microbiol Ecol 24(3):243–249
Mohd Kamil NAF, Hamzah N, Abdul Talib S, Hussain N (2016) Improving mathematical model in biodegradation of PAHs contaminated soil using gram-positive Bacteria. Soil Sediment Contam 25(4):443–458
Molaei S, Moussavi G, Talebbeydokhti N, Shekoohiyan S (2022) Biodegradation of the petroleum hydrocarbons using an anoxic packed-bed biofilm reactor with in-situ biosurfactant-producing bacteria. J Hazard Mater 421:126699
Mottaleb MA, Ferdous M, Islam MS, Salehuddin S, Hossain MA (1999) Determination of normal saturated hydrocarbons in the Buriganga river water of Bangladesh by gas liquid chromatography. Anal Sci 15(10):995–1000
Moussavi G, Ghorbanian M (2015) The biodegradation of petroleum hydrocarbons in an upflow sludge-blanket/fixed-film hybrid bioreactor under nitrate-reducing conditions: Performance evaluation and microbial identification. Chem Eng J 280:121–131
Moussavi G, Shekoohiyan S, Naddafi K (2017) The accelerated enzymatic biodegradation and COD removal of petroleum hydrocarbons in the SCR using active bacterial biomass capable of in-situ generating peroxidase and biosurfactants. Chem Eng J 308:1081–1089
Nedwell DB (1999) Effect of low temperature on microbial growth: lowered affinity for substrates limits growth at low temperature. FEMS Microbiol Ecol 30(2):101–111
Partovinia A, Naeimpoor F, Hejazi P (2010) Carbon content reduction in a model reluctant clayey soil: slurry phase n-hexadecane bioremediation. J Hazard Mater 181(1–3):133–139
Pawar RM (2015) The effect of soil pH on bioremediation of polycyclic aromatic hydrocarbons (PAHS). J Bioremediat Biodegrad 6(3):291–304
Pino-Herrera DO, Pechaud Y, Huguenot D, Esposito G, van Hullebusch ED, Oturan MA (2017) Removal mechanisms in aerobic slurry bioreactors for remediation of soils and sediments polluted with hydrophobic organic compounds: an overview. J Hazard Mater 339:427–449
Pourakbar M, Moussavi G, Yaghmaeian K (2018) Enhanced biodegradation of phenol in a novel cyclic activated sludge integrated with a rotating bed bioreactor in anoxic and peroxidase-mediated conditions. RSC Adv 8(12):6293–6305
Qureshi T, Memon N, Memon SQ, Ashraf MA (2016) Decontamination of ofloxacin: optimization of removal process onto sawdust using response surface methodology. Desalin Water Treat 57(1):221–229
Rahman K, Thahira-Rahman J, Lakshmanaperumalsamy P, Banat IM (2002) Towards efficient crude oil degradation by a mixed bacterial consortium. Bioresource Technol 85(3):257–261
Reddy MV, Devi MP, Chandrasekhar K, Goud RK, Mohan SV (2011) Aerobic remediation of petroleum sludge through soil supplementation: microbial community analysis. J Hazard Mater 197:80–87
Rezaei M, Moussavi G, Naddafi K, Johnson MS (2020) Enhanced biodegradation of styrene vapors in the biotrickling filter inoculated with biosurfactant-generating bacteria under H2O2 stimulation. Sci Total Environ 704:135325
Robinson PK (2015) Enzymes: principles and biotechnological applications. Essays Biochem 59:1–41
Rodríguez-Rojas A, Kim JJ, Johnston PR, Makarova O, Eravci M, Weise C, Hengge R, Rolff J (2020) Non-lethal exposure to H2O2 boosts bacterial survival and evolvability against oxidative stress. PLoS Genet 16(3):e1008649
Safdari M-S, Kariminia H-R, Rahmati M, Fazlollahi F, Polasko A, Mahendra S, Wilding WV, Fletcher TH (2018) Development of bioreactors for comparative study of natural attenuation, biostimulation, and bioaugmentation of petroleum-hydrocarbon contaminated soil. J Hazard Mater 342:270–278
Shekoohiyan S, Moussavi G, Naddafi K (2016) The peroxidase-mediated biodegradation of petroleum hydrocarbons in a H2O2-induced SBR using in-situ production of peroxidase: biodegradation experiments and bacterial identification. J Hazard Mater 313:170–178
Suja F, Rahim F, Taha MR, Hambali N, Razali MR, Khalid A, Hamzah A (2014) Effects of local microbial bioaugmentation and biostimulation on the bioremediation of total petroleum hydrocarbons (TPH) in crude oil contaminated soil based on laboratory and field observations. Int Biodeter Biodegrad 90:115–122
Tomei MC, Daugulis AJ (2013) Ex situ bioremediation of contaminated soils: an overview of conventional and innovative technologies. Crit Rev Environ Sci Technol 43(20):2107–2139
Torlapati J, Boufadel MC (2014) Evaluation of the biodegradation of Alaska North Slope oil in microcosms using the biodegradation model BIOB. Front Microbiol 5:212
Vyas TK, Dave B (2007) Effect of crude oil concentrations, temperature and pH on growth and degradation of crude oil by marine bacteria. Indian J Mar Sci 36:76–85
Woo SH, Lee MW, Park JM (2004) Biodegradation of phenanthrene in soil-slurry systems with different mass transfer regimes and soil contents. J Biotechnol 110(3):235–250
Wu M, Dick WA, Li W, Wang X, Yang Q, Wang T, Xu L, Zhang M, Chen L (2016) Bioaugmentation and biostimulation of hydrocarbon degradation and the microbial community in a petroleum-contaminated soil. Int Biodeter Biodegrad 107:158–164
Wu M, Wu J, Zhang X, Ye X (2019) Effect of bioaugmentation and biostimulation on hydrocarbon degradation and microbial community composition in petroleum-contaminated loessal soil. Chemosphere 237:124456
Acknowledgements
This manuscript was funded by INSF, Iran under the Grant No. 97009235. The authors are also grateful to the Tarbiat Modares University for providing technical and financial support under the Grant No. IG-39801.
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FF: Investigation, Writing—original draft, Writing—review and editing, Visualization. GM: Conceptualization, Methodology, Resources, Writing—original draft, Writing—review and editing, Supervision, Funding acquisition. SS: Conceptualization, Methodology, Writing—review and editing, Supervision, Funding acquisition.
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Fanaei, F., Moussavi, G. & Shekoohiyan, S. Enhanced bioremediation of oil-contaminated soil in a slurry bioreactor by H2O2-stimulation of oil-degrading/biosurfactant-generating bacteria: performance optimization and bacterial metagenomics. Biodegradation 34, 83–101 (2023). https://doi.org/10.1007/s10532-022-10008-z
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DOI: https://doi.org/10.1007/s10532-022-10008-z