Abstract
The enhanced biodegradation of oil-contaminated soil by fixing microorganisms with corn cob biochar was investigated. It was found that the components of oil in the test soil were mainly straight-chain alkanes and branched alkanes. When using corn cob biochar as a carrier to immobilize microorganisms, the best particle size of corn cob biochar as an immobilization carrier was 0.08 mm, and the best immobilization time was 18 h. SEM analysis confirmed that the microorganisms were immobilized on the corn cob biochar. Immobilized microorganisms exhibited high biodegradability under stress to high concentrations of petroleum pollutants, heavy metals, and organic pollutants. Infrared spectroscopy analysis showed that oxygen-containing groups such as hydroxyl, carboxyl, and methoxy on the surface of biochar were involved in the complexation of heavy metals. The mechanism of immobilization promoted microbial degradation of oil contamination was explained by gas chromatography mass. First, alkanes and aromatics were adsorbed by corn cob biochar and passed to immobilized microorganisms to promote their degradation. Their bioavailability increased, especially for aromatics. Second, biochar provided a more suitable environment for microorganisms to degrade. Third, the conversion of ketones to acids was accelerated during the biodegradation of alkanes, and the biodegradation of alkanes was accelerated by immobilization. The biodegradable efficiency of oil by immobilized microorganisms in soil was 70.10% within 60 days, 28.80% higher than that of free microorganisms. The degradation of immobilized microorganisms was highly correlated with the activities of catalase, urease, and polyphenol oxidase.
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Ali Khan AH, Tanveer S, Anees M, Muhammad YS, Lqbal M, Sohail Y (2016) Role of nutrients and illuminance in predicting the fate of fungal mediated petroleum hydrocarbon degradation and biomass production. J Environ Manag 176:54–60. https://doi.org/10.1016/j.jenvman.2016.03.040
Asif M, Grice K, Fazeelat T (2009) Assessment of petroleum biodegradation using stable hydrogen isotopes of individual saturated hydrocarbon and polycyclic aromatic hydrocarbon distributions in oils from the Upper Indus Basin. Pakistan Org Geochem 40(3):301–311. https://doi.org/10.1016/j.orggeochem.2008.12.007
Banjoo DR, Nelson PK (2005) Improved ultrasonic extraction procedure for the determination of polycyclic aromatic hydrocarbons in sediments. J Chromatogr A 1066(1–2):9–18. https://doi.org/10.1016/j.chroma.2005.01.033
Basak B, Bhunia B, Dey A (2014) Studies on the potential use of sugarcane bagasse as carrier matrix for immobilization of Candida tropicalis PHB5 for phenol biodegradation. Int Biodeterior Biodegrad 93(23):107–117. https://doi.org/10.1016/j.ibiod.2014.05.012
Bayat Z, Hassanshahian M, Cappello S (2015) Immobilization of microbes for bioremediation of crude oil polluted environments: a mini review. Open Microbiol J 9(02):48–54. https://doi.org/10.2174/1874285801509010048
Bzura J, Koncki R (2019) A mechanized urease activity assay. Enzym Microb Technol 123(41):1–7. https://doi.org/10.1016/j.enzmictec.2019.01.001
Chang Y, Liu W, Mao Y, Yang T, Chen Y (2022) Biochar addition alters C: N: P stoichiometry in moss crust-soil continuum in Gurbantünggüt desert. Plants 11(6):814. https://doi.org/10.3390/plants11060814
Chen Y, Yu B, Lin J, Naidu R, Chen Z (2016) Simultaneous adsorption and biodegradation (SAB) of diesel oil using immobilized Acinetobacter venetianus on porous material. Chem Eng J 289:463–470. https://doi.org/10.1016/j.cej.2016.01.010
Chen Z, Jing Y, Wang Y, Meng X, Zhang C, Chen Z, Zhou J, Qiu R, Zhang X (2020) Enhanced removal of aqueous Cd(II) by a biochar derived from salt-sealing pyrolysis coupled with NaOH treatment. Appl Surf Sci 511(36):145619–145635. https://doi.org/10.1016/j.apsusc.2020.145619
Dellagnezze BM, Vasconcellos SP, Angelim AL, Melo VMM, Santisi S, Cappello S, Oliveira VM (2016) Bioaugmentation strategy employing a microbial consortium immobilized in chitosan beads for oil degradation in mesocosm scale. Mar Pollut Bull 107(1):107–117. https://doi.org/10.1016/j.marpolbul.2016.04.011
Denyes MJ, Rutter A, Zeeb BA (2016) Bioavailability assessments following biochar and activated carbon amendment in DDT-contaminated soil. Chemosphere 144(45):1428–1434. https://doi.org/10.1016/j.chemosphere.2015.10.029
Diaz MP, Boyd KG, Grigson SJW, Burgess JG (2002) Biodegradation of crude oil across a wide range of salinities by an extremely halotolerant bacterial consortium MPD-M, immobilized onto polypropylene fibers. Biotechnol Bioeng 79(2):145–153. https://doi.org/10.1002/bit.10318
Ding Y, Peng N, Du Y, Ji L, Cao B (2014) Disruption of putrescine biosynthesis in Shewanella oneidensis enhances biofilm cohesiveness and performance in Cr(VI) immobilization. Appl Environ Microbiol 80(4):1498–1506. https://doi.org/10.1128/AEM.03461-13
Dzionek A, Wojcieszynska D, Guzik U (2016) Natural carriers in bioremediation: a review. Electron J Biotechnol 23(32):28–36. https://doi.org/10.1016/j.ejbt.2016.07.003
Eroglu E, Agarwal V, Bradshaw M, Chen X, Smith SM, Raston CL, Swaminathan Iyer K (2012) Nitrate removal from liquid effluents using microalgae immobilized on chitosan nanofiber mats. Green Chem 14(1):2682–2685. https://doi.org/10.1039/c2gc35970g
Ge X, Cao Y, Zhou B, Wang X, Yang Z, Li M (2019) Biochar addition increases subsurface soil microbial biomass but has limited effects on soil CO2 emissions in subtropical moso bamboo plantations. Appl Soil Ecol 142(11):155–165. https://doi.org/10.1016/j.apsoil.2019.04.021
Goh CL, Sethupathi S, Bashir MJ, Ahmed W (2019) Adsorptive behaviour of palm oil mill sludge biochar pyrolyzed at low temperature for copper and cadmium removal. J Environ Manag 237(46):281–288. https://doi.org/10.1016/j.jenvman.2018.12.103
Hajieghrari M, Hejazi P (2020) Enhanced biodegradation of n-Hexadecane in solid-phase of soil by employing immobilized Pseudomonas Aeruginosa on size-optimized coconut fibers. J Hazard Mater 389(46):122134. https://doi.org/10.1016/j.jhazmat.2020.122134
Hu G, Li J, Hou H (2015) A combination of solvent extraction and freeze thaw for oil recovery from petroleum refinery wastewater treatment pond sludge. J Hazard Mater 283:832–840. https://doi.org/10.1016/j.jhazmat.2014.10.028
Kappaun K, Piovesan AR, Carlini CR, Ligabue-Braun R (2018) Ureases: historical aspects, catalytic, and non-catalytic properties—a review. J Adv Res 13(21):3–17. https://doi.org/10.1016/j.jare.2018.05.010
Karamalidis AK, Voudrias EA (2007) Release of Zn, Ni, Cu, SO42- and CrO42- as a function of pH from cement-based stabilized/solidified refinery oily sludge and ash from incineration of oily sludge. J Hazard Mater 141(3):591–606. https://doi.org/10.1016/j.jhazmat.2006.07.034
Ławniczak A, Kaczorek E, Olszanowski A (2011) The influence of cell immobilization by biofilm forming on the biodegradation capabilities of bacterial consortia. World J Microbiol Biotechnol 27(5):1183–1188. https://doi.org/10.1007/s11274-010-0566-5
Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota—a review. Soil Biol Biochem 43(9):1812–1836. https://doi.org/10.1016/j.soilbio.2011.04.022
Li H, Dong X, Da Silva EB, de Oliveira LM, Chen Y, Ma LQ (2017) Mechanisms of metal sorption by biochars: biochar characteristics and modifications. Chemosphere 178(46):466–478. https://doi.org/10.1016/j.chemosphere.2017.03.072
Li J, Wu K, Chen Z, Wang W, Yang B, Wang K, Luo J, Yu R (2019) Effects of energetic heterogeneity on gas adsorption and gas storage in geologic shale systems. Appl Energy 251(45):113368. https://doi.org/10.1016/j.apenergy.2019.113368
Li R, Wang B, Niu A, Cheng N, Chen M, Zhang X, Yu Z, Wang S (2022) Application of biochar immobilized microorganisms for pollutants removal from wastewater: a review. Sci Total Environ 837:155563. https://doi.org/10.1016/j.scitotenv.2022.155563
Lin J, Gan L, Chen Z, Naidu R (2015) Biodegradation of tetradecane using Acinetobacter venetianus immobilized on bagasse. Biochem Eng J 100(18):76–82. https://doi.org/10.1016/j.bej.2015.04.014
Liu Y, Gan L, Chen Z, Megharaj M, Naidu R (2012) Removal of nitrate using Paracoccus sp. YF1 immobilized on bamboo carbon. J. Hazard. Mater. 229–230(38):419–425. https://doi.org/10.1016/j.jhazmat.2012.06.029
Liu J, Yang M, Wang Y, Qu L, Zhong G (2019) Enhanced diuron remediation by microorganism-immobilized silkworm excrement composites and their impact on soil microbial communities. J Hazard Mater 376(12):29–36. https://doi.org/10.1016/j.jhazmat.2019.05.014
Małachowska-Jutsz A, Matyja K (2019) Discussion on methods of soil dehydrogenase determination. Int J Environ Sci Technol 16(12):7777–7790. https://doi.org/10.1007/s13762-019-02375-7
Nunal SN, Leon SMS, Bacolod E, Koyama J, Uno S, Hidaka M, Yoshikawa T, Maeda H (2014) Bioremediation of heavily oil-polluted seawater by a bacterial consortium immobilized in cocopeat and rice hull powder. Biocontrol Sci 19(1):11–22. https://doi.org/10.4265/bio.19.11
Partovinia A, Naeimpoor F (2013) Phenanthrene biodegradation by immobilized microbial consortium in polyvinyl alcohol cryogel beads. Int Biodeterior Biodegrad 85(22):337–344. https://doi.org/10.1016/j.ibiod.2013.08.017
Phale PS, Basu A, Majhi PD, Deveryshetty J, Vamsee-Krishna C, Shrivastava R (2007) Metabolic diversity in bacterial degradation of aromatic compounds. OMICS 11(3):252–279. https://doi.org/10.1089/omi.2007.0004
Qiao L, Donghui W, Jianlong W (2010) Biodegradation of pyridine by Paracoccus sp. KT-5 immobilized on bamboo-based activated carbon. Bioresour. Technol. 101(14):5229–5234. https://doi.org/10.1016/j.biortech.2010.02.059
Ren H, Wei Z, Wang Y, Deng Y, Li M, Wang B (2020) Effects of biochar properties on the bioremediation of the petroleum-contaminated soil from a shale-gas field. Environ Sci Pollut Res 27(29):36427–36438. https://doi.org/10.1007/s11356-020-09715-y
Sarma H, Sonowal S, Prasad M (2019) Plant-microbiome assisted and biochar-amended remediation of heavy metals and polyaromatic compounds horizontal line a microcosmic study. Ecotox Environ Safe 176:288–299. https://doi.org/10.1016/j.ecoenv.2019.03.081
Seiler T, Best N, Fernqvist MM, Hercht H, Smith KEC, Braunbeck T, Mayer P, Hollert H (2014) PAH toxicity at aqueous solubility in the fish embryo test with Danio rerio using passive dosing. Chemosphere 112(23):77–84. https://doi.org/10.1016/j.chemosphere.2014.02.064
Siddique T, Semple K, Li C, Foght JM (2020) Methanogenic biodegradation of iso-alkanes and cycloalkanes during long-term incubation with oil sands tailings. Environ Pollut 258(34):113768. https://doi.org/10.1016/j.envpol.2019.113768
Su D, Li P, Frank S, Xiong X (2006) Biodegradation of benzo[a]pyrene in soil by Mucor sp. SF06 and Bacillus sp. SB02 co-immobilized on vermiculite. J Environ Sci 18(6):1204–1209. https://doi.org/10.1016/s1001-0742(06)60063-6
Teixido M, Pignatello JJ, Beltran JL, Granados M, Peccia J (2011) Speciation of the ionizable antibiotic sulfamethazine on black carbon (biochar). Environ Sci Technol 45(23):10020–10027. https://doi.org/10.1021/es202487h
Vidonish JE, Zygourakis K, Masiello CA, Gao X, Mathieu J, Alvarez PJJ (2016) Pyrolytic treatment and fertility enhancement of soils contaminated with heavy hydrocarbons. Environ Sci Technol 50(5):2498–2506. https://doi.org/10.1021/acs.est.5b02620
Wang S, Wang D, Yu Z, Dong X, Liu S, Cui H, Sun B (2020a) Advances in research on petroleum biodegradability in soil. Environ Sci Process Impacts 12(23):9–27. https://doi.org/10.1039/D0EM00370K
Wang S, Wang D, Yu Z, Dong X, Liu S, Cui H, Sun B (2020b) Advances in research on petroleum biodegradability in soil. Environ Sci Process Impacts 23(1):9–27
Wu P, Wang Z, Bhatnagar A, Jeyakumar P, Wang H, Wang Y, Li X (2021) Microorganisms-carbonaceous materials immobilized complexes: synthesis, adaptability and environmental applications. J Hazard Mater 416:125915. https://doi.org/10.1016/j.jhazmat.2021.125915
Xiao X, Chen B, Chen Z, Zhu L, Schnoor JL (2018) Insight into multiple and multilevel structures of biochars and their potential environmental applications: a critical review. Environ Sci Technol 52(9):5027–5047. https://doi.org/10.1021/acs.est.7b06487
Xie Q, Liu N, Lin D, Qu R, Zhou Q, Ge F (2020) The complexation with proteins in extracellular polymeric substances alleviates the toxicity of Cd (II) to Chlorella vulgaris. Environ Pollut 263(Pt A):114102–114115. https://doi.org/10.1016/j.envpol.2020.114102
Xiong D, Wang C, Huang X (2021) Particular pollutants, physical properties, and environmental performance of porous ceramsite materials containing oil-based drilling cuttings residues. Environ Sci Pollut Res Int 29(5):7202–7213. https://doi.org/10.1007/s11356-021-16120-6
Yang M, Zhang H, Ni J, Chen W, Yang L, Wei R (2020) Effect of cadmium on pyrene biodegradation in solution and soil using free and immobilized Escherichia sp. on biochar. Appl Soil Ecol 150(27):103472–103488. https://doi.org/10.1016/j.apsoil.2019.103472
Yuan F, Yin S, Xu Y, Xiang L, Wang H, Li Z, Fan K, Pan G (2021) The richness and diversity of catalases in bacteria. Front Microbiol 12:645477. https://doi.org/10.3389/fmicb.2021.645477
Zhang S, Wang J (2021) Removal of chlortetracycline from water by Bacillus cereus immobilized on Chinese medicine residues biochar. Environ Technol Innov 24(18):101930. https://doi.org/10.1016/j.eti.2021.101930
Zhang B, Zhang L, Zhang X (2019) Bioremediation of petroleum hydrocarbon-contaminated soil by petroleum-degrading bacteria immobilized on biochar. RSC Adv 9(60):35304–35311. https://doi.org/10.1039/c9ra06726d
Zhang W, Shen J, Zhang H, Zheng C, Wei R, Gao Y, Yang L (2021a) Efficient nitrate removal by Pseudomonas mendocina GL6 immobilized on biochar. Bioresour Technol 320(Pt A):124324. https://doi.org/10.1016/j.biortech.2020.124324
Zhang W, Shen J, Zhang H, Zheng C, Wei R, Gao Y, Yang L (2021b) Efficient nitrate removal by Pseudomonas mendocina GL6 immobilized on biochar. Bioresourc Technol 320(Pt A):124324–124338. https://doi.org/10.1016/j.biortech.2020.124324
Zhou X, Wang E, Han G (2008) Studies on acute toxic effects of Cd, Pb and as on Photobacterium phosphoreum. J Northeastern Univ 29(11):1645–1647
Zhu T, Xie Y, Wu B, Zhang Q, Xu Q (2017) Study on soil biodegradability in Changning and Weiyuan National Shale gas area. Guangzhou Chem Ind 45(03):60–62
Acknowledgements
The research was supported by Open Fund of State Environmental Protection Key Laboratory of Collaborative Control and Remediation of Soil and Water Pollution (GHBK-003), Opening Project of Oil & Gas Field Applied Chemistry Key Laboratory of Sichuan Province (YQKF202107), Science and Technology Cooperation Project of the CNPC-SWPU Innovation Alliance (2020CX020300), and Open Fund of Key Laboratory of Shale Gas Exploration, Ministry of Natural Resources, Chongqing Institute of Geology and Mineral Resources (KLSGE-MLR-202004).
Funding
The research was supported by Open Fund of State Environmental Protection Key Laboratory of Collaborative Control and Remediation of Soil and Water Pollution (GHBK-003), Opening Project of Oil & Gas Field Applied Chemistry Key Laboratory of Sichuan Province (YQKF202107), Science and Technology Cooperation Project of the CNPC-SWPU Innovation Alliance (2020CX020300), and Open Fund of Key Laboratory of Shale Gas Exploration, Ministry of Natural Resources, Chongqing Institute of Geology and Mineral Resources (KLSGE-MLR-202004).
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HR: Conceptualization, Validation, Writing—Original Draft. Y-PD: Formal analysis, Data Curation, Visualization. LM: Methodology, Data Curation. ZW: Funding acquisition, Project administration. LM: Investigation, Resources. DY: Data Curation, Resources. BW: Visualization, Funding acquisition. Z-YL: Writing—Review & Editing, Funding acquisition, Supervision.
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Ren, H., Deng, Y., Ma, L. et al. Enhanced biodegradation of oil-contaminated soil oil in shale gas exploitation by biochar immobilization. Biodegradation 33, 621–639 (2022). https://doi.org/10.1007/s10532-022-09999-6
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DOI: https://doi.org/10.1007/s10532-022-09999-6