Effects of bioremediation on soil fertility and microbial communities of degraded grassland soil under dual petroleum contamination and saline-alkali stress

Abstract

Petroleum extraction and its organic pollutants have numerous negative consequences on the composition and ecological function of grasslands, such as vegetation degradation, reduction in species diversity, and salinization. Thus, finding a comprehensive method for polluted soil and restoring grasslands faces many challenges, and the mechanism to influence soil environments and microbial community composition remains unclear. In this study, container experiments explored the potential of sulfonic acid group (–SO₃H groups) modified biochar combined with isolated bacterium (named Y-1, Acinetobacter-spp.) on physicochemical properties and microbial communities of polluted soil. The results show that modified biochar and Y-1 combined addition had the highest petroleum degradation rate (39.4%), and soil nutrients such as dissolved organic carbon (DOC), cation exchange capacity (CEC), available nitrogen, invertase and urease activities in CK were decreased by 35.4, 12.1, 30, 43.2 and 32.5% compared to treatments. The contents of available phosphorus in CM treatment were increased 2.4 times compared to CK. The –SO₃H groups efficiently improve salinity by accumulating Ca²⁺ and Mg²⁺ and inhibiting the aggregation of Na⁺. The correlation heatmap indicated that soil organic carbon, total nitrogen and CEC markedly interact with microbial communities. High-throughput sequencing indicated that the biomarkers enriched by the present integrated treatment are crucial for stimulating nitrogen and phosphorus cycles. The results indicate that -SO₃H groups modified biochar, and Y-1 has great potential to serve as a novel bioremediation technology to remediate soil from petroleum pollutants and alkalization and achieve better restoration of degradation grasslands.

Graphical abstract

References

[1] Abdalla K, Mutema M, Chivenge P, Everson C, Chaplot V. Grassland degradation significantly enhances soil CO₂ emission CATENA, 2018, 167: 284-292.

[2] Ajona M, Vasanthi P. Bioremediation of petroleum contaminated soils—a review Mater Today Proc, 2021, 45: 7117-7122.

[3] Akiyama T, Kawamura K. Grassland degradation in China: methods of monitoring, management and restoration Grassland Sci, 2007, 53(1): 1-17.

[4] Al-Hawash AB, Dragh MA, Li S, Alhujaily A, Abbood HA, Zhang XY, Ma FY. Principles of microbial degradation of petroleum hydrocarbons in the environment Egypt J Aquatic Res, 2018, 44(2): 71-76.

[5] Ameloot N, Sleutel S, Das KC, Kanagaratnam J, Neve SD. Biochar amendment to soils with contrasting organic matter level: effects on N mineralization and biological soil properties Glob Change Biol Bioenergy, 2015, 7(1): 135-144.

[6] Bhatnagar A, Hogland W, Marques M, Sillanpää M. An overview of the modification methods of activated carbon for its water treatment applications Chem Eng J, 2013, 219: 499-511.

[7] Bolan NS, Adriano DC, Kunhikrishnan A, James T, McDowell R, Senesi N. Dissolved organic matter: biogeochemistry, dynamics, and environmental significance in soils Adv Agron, 2011, 110: 1-75.

[8] Bronick CJ, Lal R. Soil structure and management: a review Geoderma, 2005, 124(1–2): 3-22.

[9] Chantigny MH. Dissolved and water-extractable organic matter in soils: a review on the influence of land use and management practices Geoderma, 2003, 113(3–4): 357-380.

[10] Chávez-García E, Siebe C. Rehabilitation of a highly saline-sodic soil using a rubble barrier and organic amendments Soil till Res, 2019, 189: 176-188.

[11] Denyes MJ, Rutter A, Zeeb BA. Bioavailability assessments following biochar and activated carbon amendment in DDT-contaminated soil Chemosphere, 2016, 144: 1428-1434.

[12] Deivakumari M, Sanjivkumar M, Suganya AM, Prabakaran JR, Palavesam A, Immanuel G. Studies on reclamation of crude oil polluted soil by biosurfactant producing Pseudomonas aeruginosa (DKB1) Biocatal Agric Biotechnol, 2020, 29. 101773

[13] Elumalai P, Parthipan P,Narenkumar J, Anandakumar B, Madhavan J, Oh BT, Rajasekar A (2019) Role of thermophilic bacteria (Bacillus and Geobacillus) on crude oil degradation and biocorrosion in oil reservoir environment. 3 Biotech 9(3):79. https://doi.org/10.1007/s13205-019-1604-0

[14] Elumalai P, Parthipan P, Huang MZ, Muthukumar B, Cheng L, Govarthanan M, Rajasekar A. Enhanced biodegradation of hydrophobic organic pollutants by the bacterial consortium: impact of enzymes and biosurfactants Environ Pollut, 2021, 289. 117956

[15] El-Sharkawy M, El-Naggar AH, Al-Huqail AA, Ghoneim AM. Acid-modified biochar impacts on soil properties and biochemical characteristics of crops grown in saline-sodic soils Sustainability, 2022, 14(13): 8190.

[16] Gang CC, Zhou W, Chen YZ, Wang ZQ, Sun ZG, Li JL, Qi JG, Odeh I. Quantitative assessment of the contributions of climate change and human activities on global grassland degradation Environ Earth Sci, 2014, 72(11): 4273-4282.

[17] Gordon G, Stavi I, Shavit U, Rosenzweig R. Oil spill effects on soil hydrophobicity and related properties in a hyper-arid region Geoderma, 2018, 312: 114-120.

[18] Harris J. Soil microbial communities and restoration ecology: facilitators or followers? Science, 2009, 325(5940): 573-574.

[19] Hajabbasi MA. Importance of soil physical characteristics for petroleum hydrocarbons phytoremediation: a review Afr J Environ Sci Technol, 2016, 10(11): 394-405.

[20] Hazaimeh MD, Ahmed ES. Bioremediation perspectives and progress in petroleum pollution in the marine environment: a review Environ Sci Pollut Res, 2021, 28(39): 54238-54259.

[21] He CY, Tian J, Gao B, Zhao YY. Differentiating climate-and human-induced drivers of grassland degradation in the Liao River Basin China Environ Monit Assess, 2015, 187(1): 4199.

[22] Hii YS, Law AT, Shazili NAM, Abdul-Rashid MK, Lee CW. Biodegradation of Tapis blended crude oil in marine sediment by a consortium of symbiotic bacteria Int Biodeter Biodegr, 2009, 63(2): 142-150.

[23] Hill R, Hunt J, Sanders E, Tran M, Burk GA , Mlsna TE, Fitzkee NC (2019) Effect of biochar on microbial growth: A metabolomics and bacteriological investigation in E. coli. Environ. Sci. Technol. 53(5): 2635–2646 https://doi.org/10.1021/acs.est.8b05024

[24] Hosokawa S, Kuroda K, Narihiro T, Aoi Y, Ozaki N, Ohashi A, Kindaichi T. Cometabolism of the superphylum Patescibacteria with anammox bacteria in a long-term freshwater anammox column reactor Water, 2021, 13(2): 208.

[25] Hussain M, Farooq M, Nawaz A, Al-Sadi AM, Solaiman ZM, Alghamdi SS, Ammara U, Ok YS, Siddique KHM. Biochar for crop production: potential benefits and risks J Soils Sediments, 2016, 17(3): 685-716.

[26] Joshi SR, Morris JW, Tfaily MM, Young RP, McNear DH Jr. Low soil phosphorus availability triggers maize growth stage specific rhizosphere processes leading to mineralization of organic P Plant Soil, 2021, 459(1–2): 423-440.

[27] Kazemi R, Ronaghi A, Yasrebi J, Ghasemi-Fasaei R, Zarei M. Effect of shrimp waste–derived biochar and arbuscular mycorrhizal fungus on yield, antioxidant enzymes, and chemical composition of corn under salinity stress J Soil Sci Plant Nutr, 2019, 19(4): 758-770.

[28] Ke CY, Sun WJ, Li YB, Lu GM, Zhang QZ, Zhang XL. Microbial enhanced oil recovery in Baolige Oilfield using an indigenous facultative anaerobic strain Luteimonas huabeiensis sp. nov J Petrol Sci Eng, 2018, 167: 160-167.

[29] Khan S, Afzal M, Iqbal S, Khan QM. Plant-bacteria partnerships for the remediation of hydrocarbon contaminated soils Chemosphere, 2013, 90(4): 1317-1332.

[30] Khanpour-Alikelayeh E, Partovinia A, Talebi A, Kermanian H. Investigation of Bacillus licheniformis in the biodegradation of Iranian heavy crude oil: A two-stage sequential approach containing factor-screening and optimization Ecotox Environ Safe, 2020, 205. 111103

[31] Lin XW, Xie ZB, Zheng JY, Liu Q, Bei QC, Zhu JG. Effects of biochar application on greenhouse gas emissions, carbon sequestration and crop growth in coastal saline soil Eur J Soil Sci, 2015, 66(2): 329-338.

[32] Lim MW, Lau EV, Poh PE. A comprehensive guide of remediation technologies for oil contaminated soil—present works and future directions Mar Pollut Bull, 2016, 109(1): 14-45.

[33] Li S, Yang YC, Li YC, Gao B, Tang YF, Xie JZ, Zhao HC. Remediation of saline-sodic soil using organic and inorganic amendments: physical, chemical, and enzyme activity properties J Soils Sediments, 2019, 20(3): 1454-1467.

[34] Li HL, Lai RQ, Jin YL, Fang XX, Cui K, Sun SS, Gong YJ, Li HN, Zhang ZZ, Zhang GQ, Zhang ZY. Directional culture of petroleum hydrocarbon degrading bacteria for enhancing crude oil recovery J Hazard Mater, 2020, 390. 122160

[35] Li Q, Huang YN, Wen DD, Fu RB, Feng LY. Application of alkyl polyglycosides for enhanced bioremediation of petroleum hydrocarbon-contaminated soil using Sphingomonas changbaiensis and Pseudomonas stutzeri Sci Total Environ, 2020, 719. 137456

[36] Li M, Yin H, Zhu MH, Yu YY, Lu GN, Dang Z. Co-metabolic and biochar-promoted biodegradation of mixed PAHs by highly efficient microbial consortium QY1 J Environ Sci, 2021, 107: 65-76.

[37] Liu XY, He LH, Zhang XY, Kong DW, Chen ZZ, Lin J, Wang CH (2022) Bioremediation of petroleum-contaminated saline soil by Acinetobacter baumannii and Talaromyces sp. and functional potential analysis using metagenomic sequencing. Environ. Pollut 311:119970. https://doi.org/10.1016/j.envpol.2022.119970

[38] Liu Z, Li Z, Chen SG, Zhou WZ. Enhanced phytoremediation of petroleum-contaminated soil by biochar and urea J Hazard Mater, 2023, 453. 131404

[39] Liu Q, Meki K, Zheng H, Yuan YF, Shao MY, Luo XX, Li XY, Jiang ZX, Li FM, Xing BS. Biochar application in remediating salt-affected soil to achieve carbon neutrality and abate climate change Biochar, 2023, 5: 45.

[40] Luo A, Wu YR, Xu Y, Kan J, Qiao J, Liang L, Huang TW, Hu Z (2016) Characterization of a cytochrome P450 monooxygenase capable of high molecular weight PAHs oxidization from Rhodococcus sp. P14. Process. Biochem. 51(12): 2127–2133.https://doi.org/10.1016/j.procbio.2016.07.024

[41] Lv YF, Bao JF, Zhu LD. A comprehensive review of recent and perspective technologies and challenges for the remediation of oil-contaminated sites Energy Rep, 2022, 8: 7976-7988.

[42] Marchand C, St-Arnaud M, Hogland W, Bell TH, Hijri M. Petroleum biodegradation capacity of bacteria and fungi isolated from petroleum-contaminated soil Int Biodete Biodegr, 2017, 116: 48-57.

[43] Medynska-Juraszek A, Alvarez ML, Bialowiec A, Jerzykiewicz M. Characterization and sodium cations sorption capacity of chemically modified biochars produced from agricultural and forestry wastes Materials, 2021, 14(16): 4714.

[44] Meki K, Liu Q, Wu S, Yuan YF. Plant- and microbe-assisted biochar amendment technology for petroleum hydrocarbon remediation in saline-sodic soils: A review Pedosphere, 2022, 32(1): 211-221.

[45] Mishra VK, Jha SK, Damodaran T, Singh YP, Srivastava S, Sharma DK, Prasad J. Feasibility of coal combustion fly ash alone and in combination with gypsum and green manure for reclamation of degraded sodic soils of the Indo-Gangetic Plains: a mechanism evaluation Land Degrad Dev, 2019, 30(11): 1300-1312.

[46] Muthukumar B, Parthipan P, AlSalhi MS, Prabhu NS, Rao TN, Devanesan S, Maruthamuthu MK, Rajasekar A. Characterization of bacterial community in oil-contaminated soil and its biodegradation efficiency of high molecular weight (>C40) hydrocarbon Chemosphere, 2022, 289. 133168

[47] Muthukumar B, AlSalhi MS, Narenkumar J, Devanesan S, Rao TN, Kim W, Rajasekar A. Characterization of two novel strains of Pseudomonas aeruginosa on biodegradation of crude oil and its enzyme activities Environ Pollut, 2022, 304. 119223

[48] Nguyen BT, Dinh GD, Dong HP, Le LB. Sodium adsorption isotherm and characterization of biochars produced from various agricultural biomass wastes J Clean Prod, 2022, 346. 131250

[49] Parthipan P, Preetham E, Machuca LL, Rahman PKSM, Murugan K, Rajasekar A. Biosurfactant and degradative enzymes mediated crude oil degradation by Bacterium Bacillus subtilis A1 Front Microbiol, 2017, 8: 193.

[50] Palansooriya KN, Wong JTF, Hashimoto Y, Huang LB, Rinklebe J, Chang SX, Bolan N, Wang HL, Ok YS. Response of microbial communities to biochar-amended soils: a critical review Biochar, 2019, 1(1): 3-22.

[51] Philippot L, Chenu C, Kappler A, Rillig MC, Fierer N. The interplay between microbial communities and soil properties Nat Rev Microbiol, 2023, 22(4): 226-239.

[52] Polyak YM, Bakina LG, Chugunova MV, Mayachkina NV, Gerasimov AO, Bure VM. Effect of remediation strategies on biological activity of oil-contaminated soil-A field study Int Biodete Biodegr, 2018, 126: 57-68.

[53] Quintella CM, Mata AMT, Lima LCP. Overview of bioremediation with technology assessment and emphasis on fungal bioremediation of oil contaminated soils J Environ Manage, 2019, 241: 156-166.

[54] Sahin O, Taskin MB, Kaya EC, Atakol O, Emir E, Inal A, Gunes A. Effect of acid modification of biochar on nutrient availability and maize growth in a calcareous soil Soi Use Manage, 2017, 33(3): 447-456.

[55] Safdari MS, Kariminia HR, Rahmati M, Fazlollahi F, Polasko A, Mahendra S, Wilding WV, Fletcher TH. Development of bioreactors for comparative study of natural attenuation, biostimulation, and bioaugmentation of petroleum-hydrocarbon contaminated soil J Hazard Mater, 2018, 342: 270-278.

[56] Saifullah DS, Naeem A, Rengel Z, Naidu R. Biochar application for the remediation of salt-affected soils: challenges and opportunities Sci Total Environ, 2018, 625: 320-335.

[57] Shahi A, Aydin S, Ince B, Ince O. Reconstruction of bacterial community structure and variation for enhanced petroleum hydrocarbons degradation through biostimulation of oil contaminated soil Chem Eng J, 2016, 306: 60-66.

[58] Sharma S, Verma R, Pandey LM. Crude oil degradation and biosurfactant production abilities of isolated Agrobacterium fabrum SLAJ731 Biocatal Agric Biotechnol, 2019, 21. 101322

[59] Sima NAK, Ebadi A, Reiahisamani N, Rasekh B. Bio-based remediation of petroleum-contaminated saline soils: challenges, the current state-of-the-art and future prospects J Environ Manage, 2019, 250. 109476

[60] Song NN, Ma J, Yu Y, Yang ZF, Li YX. New observations on PAH pollution in old heavy industry cities in northeastern China Environ Pollut, 2015, 205: 415-423.

[61] Su YZ, Li YL, Cui JY, Zhao WZ. Influences of continuous grazing and livestock exclusion on soil properties in a degraded sandy grassland, Inner Mongolia, northern China CATENA, 2005, 59(3): 267-278.

[62] Sun J, He FH, Hb S, Zhang ZH, Xu G. Effects of biochar application on Suaeda salsa growth and saline soil properties Environ Earth Sci, 2016, 75(8): 630.

[63] Suda K, Ikarashi M, Tamaki H, Tamazawa S, Sakata S, Haruo M, Kamagata Y, Kaneko M, Ujiie T, Shinotsuka Y, Wakayama T, Iwama H, Osaka N, Mayumi D, Yonebayashi H. Methanogenic crude oil degradation induced by an exogenous microbial community and nutrient injections J Pet Sci Eng, 2021, 201. 108458

[64] Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling Environ Microbiol, 2005, 7(12): 1985-1995.

[65] Tran HT, Lin C, Bui XT, Ngo HH, Cheruiyot NK, Hoang HG, Vu CT (2021) Aerobic composting remediation of petroleum hydrocarbon-contaminated soil. Current and future perspectives. Sci Total Environ 753:142250. https://doi.org/10.1016/j.scitotenv.2020.142250

[66] Wang Y, Feng J, Lin QX, Lyu XG, Wang XY, Wang GP. Effects of crude oil contamination on soil physical and chemical properties in Momoge wetland of China Chin Geogra Sci, 2013, 23(6): 708-715.

[67] Wang GW, Jin ZX, Wang XX, George TS, Feng G, Zhang L. Simulated root exudates stimulate the abundance of Saccharimonadales to improve the alkaline phosphatase activity in maize rhizosphere Appl Soil Ecol, 2022, 170. 104274

[68] Wei KH, Ma J, Xi BD, Yu MD, Cui J, Chen BL, L Y, Gu QB, He XS, . Recent progress on in-situ chemical oxidation for the remediation of petroleum contaminated soil and groundwater J Hazard Mater, 2022, 432. 128738

[69] Xia WT, Niu CC, Yu QB, Wang Q, Wang JQ, Sun X, Wang ZX, Shan XH. Experimental investigation of the erodibility of soda saline-alkali soil under freeze-thaw cycle from a microscopic view CATENA, 2023, 232. 107430

[70] Xu WH, Wang GB, Deng FF, Zou XM, Ruan HH, Chen HYH. Responses of soil microbial biomass, diversity and metabolic activity to biochar applications in managed poplar plantations on reclaimed coastal saline soil Soil Use Manage, 2018, 34(4): 597-605.

[71] Xu Y, Ge Y, Lou YH, Meng J, Shi L, Xia F. Assembly strategies of the wheat root-associated microbiome in soils contaminated with phenanthrene and copper J Hazard Mater, 2021, 412. 125340

[72] Yu J, Chang JS, Guo HL, Han S, Lee DJ. Sodium ions removal by sulfuric acid-modified biochars Environ Res, 2023, 235. 116592

[73] Yue Y, Guo WN, Lin QM, Li GT, Zhao XR (2016) Improving salt leaching in a simulated saline soil column by three biochars derived from rice straw (Oryza sativa L.), sunflower straw (Helianthus annuus), and cow manure. J Soil Water Conserv 71(6):467–475. https://doi.org/10.2489/jswc.71.6.467

[74] Yu Y, Zheng L, Zhou YJ, Sang WG, Zhao JN, Liu L, Li C, Xiao CW, Deng Y. Changes in soil microbial community structure and function following degradation in a temperate grassland J Plant Ecol, 2021, 14: 384-397.

[75] Yuan YF, Liu Q, Zheng H, Li M, Liu YF, Wang X, Peng Y, Luo XX, Li FM, Li XY, Xing BS. Biochar as a sustainable tool for improving the health of salt-affected soils Soil Environ Health, 2023, 1(3. 100033

[76] Zhang XY, Kong DW, Liu XY, Xie HH, Lou XY, Zeng C. Combined microbial degradation of crude oil under alkaline conditions by Acinetobacter baumannii and Talaromyces sp Chemosphere, 2021, 273. 129666

[77] Zhang Y, Liu S, Niu LL, Su AX, Li MY, Wang YQ, Xu Y. Sustained and efficient remediation of biochar immobilized with Sphingobium abikonense on phenanthrene-copper co-contaminated soil and microbial preferences of the bacteria colonized in biochar Biochar, 2023, 5: 43.

[78] Zhang SH, Zhang MR, Han F, Liu Z, Zhao CF, Lei JH, Zhou WZ (2023b) Enhanced degradation of petroleum in saline soil by nitrogen stimulation and halophilic emulsifying bacteria Bacillus sp. Z-13. J Hazard Mater 459:132102. https://doi.org/10.1016/j.jhazmat.2023.132102

[79] Zhao L, Xiao DL, Liu Y, Xu HC, Nan HY, Li DP, Kan Y, Cao XD. Biochar as simultaneous shelter, adsorbent, pH buffer, and substrate of Pseudomonas citronellolis to promote biodegradation of high concentrations of phenol in wastewater Water Res, 2020, 172. 115494

[80] Zhao YX, Guo L, Wang L, Jiang ND, Chen KX, Dai YJ. Biodegradation of the pyridinecarboxamide insecticide flonicamid by Microvirga flocculans and characterization of two novel amidases involved Ecotoxicol Environ Saf, 2021, 220. 112384

[81] Zheng H, Wang X, Chen L, Wang ZY, Xia Y, Zhang YP, Wang HF, Luo XX, Xing BS. Enhanced growth of halophyte plants in biochar-amended coastal soil: roles of nutrient availability and rhizosphere microbial modulation Plant Cell Environ, 2018, 41 3): 517-532.

RIGHTS & PERMISSIONS

Northeast Forestry University