Abstract
Persistent free radicals (PFRs) are emerging contaminants of increasing concern, yet their formation, fate, toxicity and health risk are poorly known. Thermal treatment, a common remediation technique to clean industrial soils, induces the formation of PFRs, which could paradoxically increase soil toxicity, contrary to the original objective of remediation. Actually, there is little knowledge on the formation and toxicity of PFRs in soils contaminated by polycyclic aromatic hydrocarbons (PAHs). Here we studied the generation of PFRs of soils spiked with anthracene and heated 1 h from 100 to 600 °C, using electron paramagnetic resonance. We also investigated the formation of reactive oxygen species (ROS), e.g. superoxide radical (O2·−), hydrogen peroxide (H2O2) and hydroxyl radical (·OH), in the aqueous phase of thermal-treated soil, and the impact of heating on soil oxidative potential, wheat growth and green algae activity. Results showed that PFRs, ROS, soil oxidative potential, plant toxicity and algal toxicity show a similar trend with an increase from 100 to 300 °C, followed by a decrease to 600 °C. Scavenger trapping tests reveal that algal toxicity is mainly due to the generation of O2·−, ·OH and H2O2 induced by anthracene-PFRs and that anthracene and anthracene-PFRs have negligible direct algal toxicity. Overall, our findings reveal the unintended formation of toxic compounds peaking at 300 °C during the thermal remediation of PAH-contaminated soils. These results should help to assess the environmental risk of thermally treated PAH-contaminated soils.
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Ahmed CMS, Cui Y, Frie AL, Burr A, Bahreini R (2019) Exposure to dimethyl selenide (DMSe)-derived secondary organic aerosol alters transcriptomic profiles in human airway epithelial cells. Environ Sci Technol 53:14660–14669. https://doi.org/10.1021/acs.est.9b04376
Banks MK, Schultz KE (2005) Comparison of plants for germination toxicity tests in petroleum-contaminated soils. Water Air Soil Poll 167:211–219. https://doi.org/10.1007/s11270-005-8553-4
Bastos AC, Prodana M, Abrantes N, Keizer JJ, Soares AMVM, Loureiro S (2014) Potential risk of biochar-amended soil to aquatic systems: an evaluation based on aquatic bioassays. Ecotoxicology 23:1784–1793. https://doi.org/10.1007/s10646-014-1344-1
Bryselbout C, Henner P, Carsignol J, Lichtfouse E (2000) Polycyclic aromatic hydrocarbons in highway plants and soils. Evidence for a local distillation effect. Analysis 28:290–293. https://doi.org/10.1051/analusis:2000280290
Chang T, Guo Q, Hao H, Wu B, Yang Y (2017) Formation of radicals in coal pyrolysis examined by electron spin resonance. AIP Adv 7:095303. https://doi.org/10.1063/1.4986270
Chen Q, Wang M, Sun H, Wang X, Wang Y, Li Y, Zhang L, Mu Z (2018) Enhanced health risks from exposure to environmentally persistent free radicals and the oxidative stress of PM2.5 from Asian dust storms in Erenhot, Zhangbei and Jinan. China Environ Int 121:260–268. https://doi.org/10.1016/j.envint.2018.09.012
Chen Q, Wang M, Wang Y, Zhang L, Li Y, Han Y (2019) Oxidative potential of water-soluble matter associated with chromophoric substances in PM2.5 over Xi’an. China Environ Sci Technol 53:8574–8584. https://doi.org/10.1021/acs.est.9b01976
Chen W, Chen M, Sun C, Chen T, Yan J (2020) Eggshell and plant ash addition during the thermal desorption of polycyclic aromatic hydrocarbon–contaminated coke soil for improved removal efficiency and soil quality. Environ Sci Pollut R 27:11050–11065. https://doi.org/10.1007/s11356-019-07531-7
Chowdhury PH, He Q, Carmieli R, Li C, Pardo M (2019) Connecting the oxidative potential of secondary organic aerosols with reactive oxygen species in exposed lung cells. Environ Sci Technol 53:13949–13958. https://doi.org/10.1021/acs.est.9b04449
Crépineau C, Rychen G, Feidt C, Le Roux Y, Lichtfouse E, Laurent F (2003) Contamination of pastures by polycyclic aromatic hydrocarbons (PAHs) in the vicinity of a highway. J Agric Food Chem 51:4841–4845. https://doi.org/10.1021/jf0210371
Dellinger B, Pryor WA, Cueto R, Squadrito GL, Hegde V, Deutsch WA (2001) Role of free radicals in the toxicity of airborne fine particulate matter. Chem Res Toxicol 14:1371–1377. https://doi.org/10.1021/tx010050x
Eriksson M, Dalhammar G, Borgkarlson A (2000) Biological degradation of selected hydrocarbons in an old PAH/creosote contaminated soil from a gas work site. Appl Microbiol Biot 53:619–626. https://doi.org/10.1007/s002530051667
Falciglia PP, Giustra MG, Vagliasindi FGA (2011) Low-temperature thermal desorption of diesel polluted soil: Influence of temperature and soil texture on contaminant removal kinetics. J Hazard Mater 185:392–400. https://doi.org/10.1016/j.jhazmat.2010.09.046
Fan X, Li M, Cao T, Cheng C, Li F, Xie Y, Wei S, Song J, Peng P (2018) Optical properties and oxidative potential of water- and alkaline-soluble brown carbon in smoke particles emitted from laboratory simulated biomass burning. Atmos Environ 194:48–57. https://doi.org/10.1016/j.atmosenv.2018.09.025
Gehling W, Khachatryan L, Dellinger B (2014) Hydroxyl radical generation from environmentally persistent free radicals (EPFRs) in PM2.5. Environ Sci Technol 48:4266–4272. https://doi.org/10.1021/es401770y
Gao P, Yao D, Qian Y, Zhong S, Zhang L, Xue G, Jia H (2018) Factors controlling the formation of persistent free radicals in hydrochar during hydrothermal conversion of rice straw. Environ Chem Lett 16:1463–1468. https://doi.org/10.1007/s10311-018-0757-0
Grova N, Laurent C, Feidt C, Rychen G, Laurent F, Lichtfouse E (2000) Gas chromatography-mass spectrometry study of polycyclic aromatic hydrocarbons in grass and milk from urban and rural farms. Eur J Mass Spectrom. https://doi.org/10.1255/ejms.371
Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15. https://doi.org/10.1016/j.jhazmat.2009.03.137
Henner P, Schiavon M, Morel JL, Lichtfouse E (1997) Polycyclic aromatic hydrocarbon (PAH) occurrence and remediation methods. Analysis 25:56–59
Henner P, Schiavon M, Druelle V, Lichtfouse E (1999) Phytotoxicity of ancient gaswork soils. Effect of polycyclic aromatic hydrocarbons (PAHs) on plant germination. Org Geochem 30:963–969. https://doi.org/10.1016/S0146-6380(99)00080-7
Inckot RC, Santos GDO, Souza LAD, Bona C (2011) Germination and development of Mimosa pilulifera in petroleum-contaminated soil and bioremediated soil. Flora 206:261–266. https://doi.org/10.1016/j.flora.2010.09.005
Jin W, Su S, Wang B, Zhu X, Tao S (2016) Properties and cellular effects of particulate matter from direct emissions and ambient sources. J Environ Sci Heal A 51:1–9. https://doi.org/10.1080/10934529.2016.1198632
Jia H, Gu C, Boyd SA, Teppen BJ, Johnston CT (2011) Comparison of reactivity of nanoscaled zero-valent iron formed on clay surfaces. Soil Sci Soc Am J 75:357–364. https://doi.org/10.2136/sssaj2010.0080nps
Jia H, Nulaji G, Gao H, Wang F, Zhu Y, Wang C (2016) Formation and stabilization of environmentally persistent free radicals induced by the interaction of anthracene with Fe(III)-modified clays. Environ Sci Technol 50:6310–6319. https://doi.org/10.1021/acs.est.6b00527
Jia H, Zhao S, Shi Y, Zhu L, Wang C, Sharma VK (2018) Transformation of polycyclic aromatic hydrocarbons and formation of environmentally persistent free radicals on modified montmorillonite: the role of surface metal ions and polycyclic aromatic hydrocarbon molecular properties. Environ Sci Technol 52:5725–5733. https://doi.org/10.1021/acs.est.8b00425
Jia H, Liu J, Zhu K, Gao P, Lichtfouse E (2020) High contribution of hydrocarbon transformation during the removal of polycyclic aromatic hydrocarbons from soils, humin and clay by thermal treatment at 100–200 °C. Environ Chem Lett 18:923–930. https://doi.org/10.1007/s10311-020-00972-4
Kanaly RA, Harayama S (2000) Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182:2059–2067. https://doi.org/10.1128/JB.182.8.2059-2067.2000
Kronimus A, Schwarzbauer J, Ricking M (2006) Analysis of non-extractable DDT-related compounds in riverine sediments of the Teltow Canal, Berlin, by pyrolysis and thermochemolysis. Environ Sci Technol 40:5882–5890. https://doi.org/10.1021/es0605568
Khachatryan L, Mcferrin CA, Hall RW, Dellinger B (2014) Environmentally persistent free radicals (EPFRs). 3. Free versus bound hydroxyl radicals in EPFR aqueous solutions. Environ Sci Technol 48:9220–9226. https://doi.org/10.1021/es501158r
Khachatryan L, Vejerano E, Lomnicki S, Dellinger B (2011) Environmentally persistent free radicals (EPFRs). 1. Generation of reactive oxygen species in aqueous solutions. Environ Sci Technol 45:8559–8566. https://doi.org/10.1021/es201309c
Kuppusamy S, Thavamani P, Venkateswarlu K (2016) Remediation approaches for polycyclic aromatic hydrocarbons (PAHs) contaminated soils: technological constraints, emerging trends and future directions. Chemosphere 168:944–968. https://doi.org/10.1016/j.chemosphere.2016.10.115
Laurent C, Feidt C, Grova N, Mpassi D, Lichtfouse E, Laurent F, Rychen G (2002) Portal absorption of 14C after ingestion of spiked milk with 14C-phenanthrene, 14C-benzo[a]pyrene or 14C-TCDD in growing pigs. Chemosphere 48:843–848. https://doi.org/10.1016/S0045-6535(02)00145-5
Laurent C, Feidt C, Lichtfouse E, Grova N, Laurent F, Rychen G (2001) Milk-blood transfer of 14C-tagged polycyclic aromatic hydrocarbons (PAHs) in pigs. J Agric Food Chem 49:2493–2496. https://doi.org/10.1021/jf0014011
Liao S, Pan B, Li H, Zhang D, Xing B (2014) Detecting free radicals in biochars and determining their ability to inhibit the germination and growth of corn, wheat and rice seedlings. Environ Sci Technol 48:8581–8587. https://doi.org/10.1021/es404250a
Lichtfouse E, Budzinski H, Garrigues P, Eglinton TI (1997) Ancient polycyclic aromatic hydrocarbons in modern soils: 13C, 14C and biomarker evidence. Org Geochem 26:353–359. https://doi.org/10.1016/S0146-6380(97)00009-0
Lichtfouse E, Wehrung P, Albrecht P (1998) Plant wax n-alkanes trapped in soil humin by noncovalent bonds. Naturwissenschaften 85:449–452. https://doi.org/10.1007/s001140050529
Liu J, Jia H, Zhu K, Zhao S, Lichtfouse E (2020) Formation of environmentally persistent free radicals and reactive oxygen species during the thermal treatment of soils contaminated by polycyclic aromatic hydrocarbons. Environ Chem Lett 18:1329–1336. https://doi.org/10.1007/s10311-020-00991-1
Lomnicki S, Truong H, Vejerano E, Dellinger B (2008) Copper oxide-based model of persistent free radical formation on combustion-derived particulate matter. Environ Sci Technol 42:4982–4988. https://doi.org/10.1021/es071708h
Merino J, Bucala V (2007) Effect of temperature on the release of hexadecane from soil by thermal treatment. J Hazard Mater 143:455–461. https://doi.org/10.1016/j.jhazmat.2006.09.050
Odinga ES, Waigi MG, Gudda FO, Wang J, Gao Y (2019) Occurrence, formation, environmental fate and risks of environmentally persistent free radicals in biochars. Environ Int 134:105172.1–105172.19. https://doi.org/10.1016/j.envint.2019.105172
Paul A, Solomon M, Costantini T, J., Grahame, Miriam, E. (2012) Air pollution and health: bridging the gap from sources to health outcomes: conference summary. Air Qual Atmos Health 5:9–62. https://doi.org/10.1007/s11869-011-0161-4
Peng N, Huang C, Su J (2018) An experimental and kinetic study of thermal decomposition of phenanthrene. J Hazard Mater 365:565–571. https://doi.org/10.1016/j.jhazmat.2018.11.026
Pourfadakari S, Ahmadi M, Jaafarzadeh N, Takdastan A, Neisi A, Ghafari S, Jorfi S (2019) Remediation of PAHs contaminated soil using a sequence of soil washing with biosurfactant produced by Pseudomonas aeruginosa strain PF2 and electrokinetic oxidation of desorbed solution, effect of electrode modification with Fe3O4 nanoparticles. J Hazard Mater 379:120839.1–120839.14. https://doi.org/10.1016/j.jhazmat.2019.120839
Ruan X, Sun Y, Du W, Tang Y, Liu Q, Zhang Z, Doherty W, Frost RL, Qian G, Tsang DCW (2019) Formation, characteristics, and applications of environmentally persistent free radicals in biochars: a review. Bioresour Technol 281:457–468. https://doi.org/10.1016/j.biortech.2019.02.105
Strak M, Janssen NAH, Godri KJ, Gosens I, Mudway IS, Cassee FR, Lebret E, Kelly FJ, Harrison RM, Brunekreef B (2012) Respiratory health effects of airborne particulate matter: the role of particle size, composition, and oxidative potential-the RAPTES project. Environ Health Perspect 120:1183–1189. https://doi.org/10.1289/ehp.1104389
Tang J, Wang M, Wang F, Sun Q, Zhou Q (2011) Eco-toxicity of petroleum hydrocarbon contaminated soil. J Environ Sci 23:845–851. https://doi.org/10.1016/S1001-0742(10)60517-7
Tong H, Lakey PSJ, Arangio AM, Socorro J, Shen F, Lucas K, Brune WH, Pöschl U, Shiraiwa M (2018) Reactive oxygen species formed by secondary organic aerosols in water and surrogate lung fluid. Environ Sci Technol 52:11642–11651. https://doi.org/10.1021/acs.est.8b03695
Wang Y, Zhang C, Lin M, Ge Y (2016) A symbiotic bacterium differentially influences arsenate absorption and transformation in Dunaliella salina under different phosphate regimes. J Hazard Mater 318:443–451. https://doi.org/10.1016/j.jhazmat.2016.07.031
Zhang L, Cao Y, Colella NS, Liang Y, Bredas JL, Houk KN, Briseno AL (2015) Unconventional, chemically stable, and soluble two-dimensional angular polycyclic aromatic hydrocarbons: from molecular design to device applications. Acc Chem Res 48:500–509. https://doi.org/10.1021/ar500278w
Zhang Y, Guo X, Si X, Yang R, Quan X (2019) Environmentally persistent free radical generation on contaminated soil and their potential biotoxicity to luminous bacteria. Sci Total Environ 687:348–354. https://doi.org/10.1016/j.scitotenv.2019.06.137
Zhao S, Zhang C, Ni Z, Zhu K, Liu J, Dai Y, Jia H (2020) Optimized extraction of environmentally persistent free radicals from clays contaminated by polycyclic aromatic hydrocarbons. Environ Chem Lett 18:949–955. https://doi.org/10.1007/s10311-020-00982-2
Zhu K, Jia H, Zhao S, Xia T, Guo X, Wang T, Zhu L (2019) Formation of environmentally persistent free radicals on microplastics under light irradiation. Environ Sci Technol 53:8177–8186. https://doi.org/10.1021/acs.est.9b01474
Zhu K, Jia H, Sun Y, Dai Y, Zhang C, Guo X, Wang T, Zhu L (2020) Long-term phototransformation of microplastics under simulated sunlight irradiation in aquatic environments: roles of reactive oxygen species. Water Res. https://doi.org/10.1016/j.watres.2020.115564
Acknowledgements
This study was supported by the National Natural Science Foundation of China (Grant No. 41877126), the Shaanxi Science Fund for Distinguished Young Scholars (Grant No. 2019JC-18), the National Key R&D Program of China (Grant No. 2018YFC1802004), the “One Hundred Talents” program of Shaanxi Province (Grant No. SXBR9171).
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Liu, J., Gao, N., Wen, X. et al. Plant and algal toxicity of persistent free radicals and reactive oxygen species generated by heating anthracene-contaminated soils from 100 to 600 °C. Environ Chem Lett 19, 2695–2703 (2021). https://doi.org/10.1007/s10311-021-01193-z
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DOI: https://doi.org/10.1007/s10311-021-01193-z