Comparison of exogenous degrader-enhanced bioremediation with low-dose persulfate oxidation for polycyclic aromatic hydrocarbon removal in alkaline soil: efficiency and influence on ecological health

Zhuoyue Yang , Zuotao Zhang , Yiwei Zuo , Jing Zhang , Panyue Zhang

Front. Environ. Sci. Eng. ›› 2023, Vol. 17 ›› Issue (11) : 133

PDF (3106KB)
Front. Environ. Sci. Eng. ›› 2023, Vol. 17 ›› Issue (11) : 133 DOI: 10.1007/s11783-023-1733-x
RESEARCH ARTICLE
RESEARCH ARTICLE

Comparison of exogenous degrader-enhanced bioremediation with low-dose persulfate oxidation for polycyclic aromatic hydrocarbon removal in alkaline soil: efficiency and influence on ecological health

Author information +
History +
PDF (3106KB)

Abstract

● Bioaugmentation and low-dose persulfate were effective in degrading PAHs.

● Indigenous microorganisms participated in the degradation process.

● Low-dose persulfate oxidation made a high activated phosphorus content.

● Low microbial species diversity made microbial system weak in BA system.

Polycyclic aromatic hydrocarbon (PAH)-contaminated soils are usually complex and characterized by a lack of nutrition and soil salinization, resulting in difficulties in soil remediation. In this study, bioaugmentation with a PAH-degrading Bacillus PheN7 (BA) and low-dose persulfate oxidation (PS), along with natural biodegradation, were utilized to remediate alkaline PAH-contaminated soil. The soil used in the study had a pH of 9.35, and the total PAH content was 568.8 ± 31.0 mg/kg dry soil. After 42 d of remediation, the degradation efficiency of PAHs was 96.72% and 93.88% using persulfate oxidation and bioaugmentation, respectively, whereas 38.66% of PAHs were degraded in natural attenuation (NA). Bacillus was the dominant genera throughout the process of bioremediation with the relative abundance of 79.3% on day 42 in the BA system, whereas, Alcanivorax was enriched and became the dominant genera in PS systems. In the meantime, PAH degradation genes were detected with remarkably higher level in the BA system than in PS system during the remediation. In addition to the degradation of contaminants, persulfate oxidation promotes microbial bioremediation efficiency mainly by lowering the pH to neutral and increasing the active phosphorus content in the soil. Microbial species and ecological niches were less reduced in the PS system than in the BA system. Collectively, persulfate oxidation had a better impact on the soil microbiome and is more suitable for long-term soil health than bioaugmentation through PheN7 addition.

Graphical abstract

Keywords

Bioaugmentation / Low-dose persulfate oxidation / Polycyclic aromatic hydrocarbon / Remediation

Cite this article

Download citation ▾
Zhuoyue Yang, Zuotao Zhang, Yiwei Zuo, Jing Zhang, Panyue Zhang. Comparison of exogenous degrader-enhanced bioremediation with low-dose persulfate oxidation for polycyclic aromatic hydrocarbon removal in alkaline soil: efficiency and influence on ecological health. Front. Environ. Sci. Eng., 2023, 17(11): 133 DOI:10.1007/s11783-023-1733-x

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Ahtiainen J , Valo R , Jarvinen M , Joutti A . (2002). Microbial toxicity tests and chemical analysis as monitoring parameters at composting of creosote-contaminated soil. Ecotoxicological and Environmental Safety, 53(2): 323–329

[2]

Antizar-Ladislao B , Lopez-Real J , Beck A J . (2006). Bioremediation of polycyclic aromatic hydrocarbons (PAH) in an aged coal-tar-contaminated soil using different in-vessel composting approaches. Journal of Hazardous Materials, 137(3): 1583–1588

[3]

Bacosa H P , Erdner D L , Rosenheim B E , Shetty P , Seitz K W , Baker B J , Liu Z . (2018). Hydrocarbon degradation and response of seafloor sediment bacterial community in the northern Gulf of Mexico to light Louisiana sweet crude oil. ISME Journal, 12(10): 2532–2543

[4]

Bezza F A , Nkhalambayausi Chirwa E M . (2015). Biosurfactant from Paenibacillus dendritiformis and its application in assisting polycyclic aromatic hydrocarbon (PAH) and motor oil sludge removal from contaminated soil and sand media. Process Safety and Environmental Protection, 98: 354–364

[5]

Cappello S , Denaro R , Genovese M , Giuliano L , Yakimov M M . (2007). Predominant growth of Alcanivorax during experiments on “oil spill bioremediation” in mesocosms. Microbiological Research, 162(2): 185–190

[6]

Chaudhary D K , Kim J . (2019). New insights into bioremediation strategies for oil-contaminated soil in cold environments. International Biodeterioration & Biodegradation, 142: 58–72

[7]

Cui H , Sun W , Delgado-Baquerizo M , Song W , Ma J Y , Wang K , Ling X . (2020). The effects of mowing and multi-level N fertilization on soil bacterial and fungal communities in a semiarid grassland are year-dependent. Soil Biology and Biochemistry, 151(1): 1–12

[8]

Dagher D J , de la Providencia I E , Pitre F E , St-Arnaud M , Hijri M . (2019). Plant identity shaped rhizospheric microbial communities more strongly than bacterial bioaugmentation in petroleum hydrocarbon-polluted sediments. Frontiers in Microbiology, 10: 2144–2157

[9]

Dores-Silva P R , Cotta J A O , Landgraf M D , Rezende M O O . (2019). The application of the vermicomposting process in the bioremediation of diesel contaminated soils. Journal of Environmental Science and Health. Part B, 54(7): 598–604

[10]

Douglas G M , Maffei V J , Zaneveld J R , Yurgel S N , Brown J R , Taylor C M , Huttenhower C , Langille M G I . (2020). PICRUSt2 for prediction of metagenome functions. Nature Biotechnology, 38(6): 685–688

[11]

Gou Y , Zhao Q , Yang S , Wang H , Qiao P , Song Y , Cheng Y , Li P . (2020). Removal of polycyclic aromatic hydrocarbons (PAHs) and the response of indigenous bacteria in highly contaminated aged soil after persulfate oxidation. Ecotoxicology and Environmental Safety, 190: 110092

[12]

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

[13]

Huang Z , Ni B , Jiang C Y , Wu Y F , He Y Z , Parales R E , Liu S J . (2016). Direct sensing and signal transduction during bacterial chemotaxis toward aromatic compounds in Comamonas testosteroni. Molecular Microbiology, 101(2): 224–237

[14]

Jin S , Jin W , Bai Y , Dong C , Jin D , Hu Z , Huang Y . (2020). Response of rice and bacterial community to phosphorus-containing materials in soil-plant ecosystem of rare earth mining area. Journal of Hazardous Materials, 381: 121004

[15]

Jouanneau Y , Meyer C , Duraffourg N . (2016). Dihydroxylation of four- and five-ring aromatic hydrocarbons by the naphthalene dioxygenase from Sphingomonas CHY-1. Applied Microbiology and Biotechnology, 100(3): 1253–1263

[16]

Kadri T , Rouissi T , Magdouli S , Brar S K , Hegde K , Khiari Z , Daghrir R , Lauzon J M . (2018). Production and characterization of novel hydrocarbon degrading enzymes from Alcanivorax borkumensis. International Journal of Biological Macromolecules, 112: 230–240

[17]

Kuo W C , Chao Y C , Wang Y C , Cheng S S . (2012). Bioaugmentation strategies to improve cellulolytic and hydrogen producing characteristics in CSTR intermittent fed with vegetable kitchen waste and napiergrass. Energy Procedia, 29: 82–91

[18]

Li X , Song Y , Wang F , Bian Y , Jiang X . (2019). Combined effects of maize straw biochar and oxalic acid on the dissipation of polycyclic aromatic hydrocarbons and microbial community structures in soil: a mechanistic study. Journal of Hazardous Materials, 364: 325–331

[19]

Liang C , Huang C F , Mohanty N , Kurakalva R M . (2008). A rapid spectrophotometric determination of persulfate anion in ISCO. Chemosphere, 73(9): 1540–1543

[20]

Liao J , Wang J , Huang Y . (2015). Bacterial community features are shaped by geographic location, physicochemical properties, and oil contamination of soil in main oil fields of China. Microbial Ecology, 70(2): 380–389

[21]

Liao X , Wu Z , Li Y , Cao H , Su C . (2019). Effect of various chemical oxidation reagents on soil indigenous microbial diversity in remediation of soil contaminated by PAHs. Chemosphere, 226: 483–491

[22]

Lim M W , Lau E V , Poh P E . (2016). A comprehensive guide of remediation technologies for oil contaminated soil: present works and future directions. Marine Pollution Bulletin, 109(1): 14–45

[23]

Liu Q , Tang J , Liu X , Song B , Zhen M , Ashbolt N J . (2019). Vertical response of microbial community and degrading genes to petroleum hydrocarbon contamination in saline alkaline soil. Journal of Environmental Sciences-China, 81: 80–92

[24]

Liu Y F , Galzerani D D , Mbadinga S M , Zaramela L S , Gu J D , Mu B Z , Zengler K . (2018). Metabolic capability and in situ activity of microorganisms in an oil reservoir. Microbiome, 6(1): 5–17

[25]

Lominchar M A , Lorenzo D , Romero A , Santos A . (2018). Remediation of soil contaminated by PAHs and TPH using alkaline activated persulfate enhanced by surfactant addition at flow conditions. Journal of Chemical Technology and Biotechnology, 93(5): 1270–1278

[26]

Louca S , Polz M F , Mazel F , Albright M B N , Huber J A , O’Connor M I , Ackermann M , Hahn A S , Srivastava D S , Crowe S A . . (2018). Function and functional redundancy in microbial systems. Nature Ecology & Evolution, 2(6): 936–943

[27]

Lu M , Zhang Z Z , Wang J X , Zhang M , Xu Y X , Wu X J . (2014). Interaction of heavy metals and pyrene on their fates in soil and tall fescue (Festuca arundinacea). Environmental Science & Technology, 48(2): 1158–1165

[28]

Medina R , David Gara P M , Fernandez-Gonzalez A J , Rosso J A , Del Panno M T . (2018). Remediation of a soil chronically contaminated with hydrocarbons through persulfate oxidation and bioremediation. Science of the Total Environment, 618: 518–530

[29]

Morgan B, Rate A W, Burton E D, Smirk M N (2012). Enrichment and fractionation of rare earth elements in FeS- and organic-rich estuarine sediments receiving acid sulfate soil drainage. Chemical Geology, 308–309: 60–73

[30]

Mrozik A , Piotrowska-Seget Z , Abuzek S . (2003). Bacterial degradation and bioremediation of polycyclic aromatic hydrocarbons. Polish Journal of Environmental Studies, 12(1): 15–25

[31]

Ni N, Li X, Yao S, Shi R, Kong D, Bian Y, Jiang X, Song Y (2021). Biochar applications combined with paddy-upland rotation cropping systems benefit the safe use of PAH-contaminated soils: from risk assessment to microbial ecology. Journal of Hazardous Materials, 404(Pt A): 124123

[32]

Niu D , Willoughby P H , Woods B P , Baire B , Hoye T R . (2013). Alkane desaturation by concerted double hydrogen atom transfer to benzyne. Nature, 501(7468): 531–534

[33]

Pan W , Zhou J , Tang S , Wu L , Ma Q , Marsden K A , Chadwick D R , Jones D L . (2023). Utilisation and transformation of organic and inorganic nitrogen by soil microorganisms and its regulation by excessive carbon and nitrogen availability. Biology and Fertility of Soils, 59(4): 379–389

[34]

Prakash A A , Prabhu N S , Rajasekar A , Parthipan P , Alsalhi M S , Devanesan S , Govarthanan M . (2021). Bioelectrokinetic remediation of crude oil contaminated soil enhanced by bacterial biosurfactant. Journal of Hazardous Materials, 405: 124061

[35]

Schneiker S , Martins dos Santos V A , Bartels D , Bekel T , Brecht M , Buhrmester J , Chernikova T N , Denaro R , Ferrer M , Gertler C . . (2006). Genome sequence of the ubiquitous hydrocarbon-degrading marine bacterium Alcanivorax borkumensis. Nature Biotechnology, 24(8): 997–1004

[36]

Shen F T , Young L S , Hsieh M F , Lin S Y , Young C C . (2010). Molecular detection and phylogenetic analysis of the alkane 1-monooxygenase gene from Gordonia spp. Systematic and Applied Microbiology, 33(2): 53–59

[37]

Sun W , Li J , Jiang L , Sun Z , Fu M , Peng X . (2015). Profiling microbial community structures across six large oilfields in China and the potential role of dominant microorganisms in bioremediation. Applied Microbiology and Biotechnology, 99(20): 8751–8764

[38]

Sun W , Xiao E , Dong Y , Tang S , Krumins V , Ning Z , Sun M , Zhao Y , Wu S , Xiao T . (2016). Profiling microbial community in a watershed heavily contaminated by an active antimony (Sb) mine in Southwest China. Science of the Total Environment, 550: 297–308

[39]

Sutton N B , Grotenhuis J T C , Langenhoff A A M , Rijnaarts H H M . (2010). Efforts to improve coupled in situ chemical oxidation with bioremediation: a review of optimization strategies. Journal of Soils and Sediments, 11(1): 129–140

[40]

Wang L , Li F , Zhan Y , Zhu L . (2016a). Shifts in microbial community structure during in situ surfactant-enhanced bioremediation of polycyclic aromatic hydrocarbon-contaminated soil. Environmental Science and Pollution Research International, 23(14): 14451–14461

[41]

Wang X , Dong G , Liu X , Zhang S , Li C , Lu X , Xia T . (2020). Poly-gamma-glutamic acid-producing bacteria reduced Cd uptake and effected the rhizosphere microbial communities of lettuce. Journal of Hazardous Materials, 398: 123146

[42]

Wang Y , Wang J , Leng F , Chen J . (2016b). Effects of oil pollution on indigenous bacterial diversity and community structure of soil in Fushun, Liaoning Province, China. Geomicrobiology Journal, 38(2): 115–126

[43]

Wang Y Q , Wang M X , Chen Y Y , Li C M , Zhou Z F . (2021a). Microbial community structure and co-occurrence are essential for methanogenesis and its contribution to phenanthrene degradation in paddy soil. Journal of Hazardous Materials, 417: 126086

[44]

Wang Z , Tan W , Yang D , Zhang K , Zhao L , Xie Z , Xu T , Zhao Y , Wang X , Pan X , Zhang D . (2021b). Mitigation of soil salinization and alkalization by bacterium-induced inhibition of evaporation and salt crystallization. Science of the Total Environment, 755: 142511

[45]

Wasak-Sęk K , Jelonkiewicz Ł , Drewnik M . (2021). Buffering role of soil in chemical denudation in mountainous areas affected by windfall events: in light of experimental research. Geomorphology, 381: 107642

[46]

Xiao R , Ye T , Wei Z , Luo S , Yang Z , Spinney R . (2015). Quantitative structure-activity relationship (QSAR) for the oxidation of trace organic contaminants by sulfate radical. Environmental Science & Technology, 49(22): 13394–13402

[47]

Xu S , Wang W , Zhu L . (2019). Enhanced microbial degradation of benzo[a]pyrene by chemical oxidation. Science of the Total Environment, 653: 1293–1300

[48]

Yang Z , Guo R , Shi X , He S , Wang L , Dai M , Qiu Y , Dang X . (2016). Bioaugmentation of Hydrogenispora ethanolica LX-B affects hydrogen production through altering indigenous bacterial community structure. Bioresource Technology, 211: 319–326

[49]

Yu H , Li T , Liu Y , Ma L . (2019). Spatial distribution of polycyclic aromatic hydrocarbon contamination in urban soil of China. Chemosphere, 230: 498–509

[50]

Zhang B , Guo Y , Huo J , Xie H , Xu C , Liang S . (2020). Combining chemical oxidation and bioremediation for petroleum polluted soil remediation by BC-nZVI activated persulfate. Chemical Engineering Journal, 382: 123055

[51]

Zhang K , Hu Z , Zeng F , Yang X , Wang J , Jing R , Zhang H , Li Y , Zhang Z . (2019). Biodegradation of petroleum hydrocarbons and changes in microbial community structure in sediment under nitrate-, ferric-, sulfate-reducing and methanogenic conditions. Journal of Environmental Management, 249: 109425

[52]

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

[53]

Zhou N , Guo H , Liu Q , Zhang Z , Sun J , Wang H . (2022). Bioaugmentation of polycyclic aromatic hydrocarbon (PAH)-contaminated soil with the nitrate-reducing bacterium PheN7 under anaerobic condition. Journal of Hazardous Materials, 439: 129643

[54]

Zhou Z , Liu X , Sun K , Lin C , Ma J , He M , Ouyang W . (2019). Persulfate-based advanced oxidation processes (AOPs) for organic-contaminated soil remediation: a review. Chemical Engineering Journal, 372: 836–851

RIGHTS & PERMISSIONS

Higher Education Press

AI Summary AI Mindmap
PDF (3106KB)

Supplementary files

FSE-23039-OF-YZY_suppl_1

2584

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/