Abstract
Developing an optimal environmentally friendly bioremediation strategy for petroleum products is of high interest. This study investigated heavy fuel oil (HFO)-contaminated soil (4 and 6 g kg−1) remediation by individual and combined bioaugmentation-assisted phytoremediation with alfalfa (Medicago sativa L.) and with cold plasma (CP)-treated M. sativa. After 14 weeks of remediation, HFO removal efficiency was in the range between 61 and 80% depending on HFO concentration and remediation technique. Natural attenuation had the lowest HFO removal rate. As demonstrated by growth rate and biomass acquisition, M. sativa showed good tolerance to HFO contamination. Cultivation of M. sativa enhanced HFO degradation and soil quality improvement. Bioaugmentation-assisted phytoremediation was up to 18% more efficient in HFO removal through alleviated HFO stress to plants, stimulated plant growth, and biomass acquisition. Cold plasma seed treatment enhanced HFO removal by M. sativa at low HFO contamination and in combination with bioaugmentation it resulted in up to 14% better HFO removal compared to remediation with CP non-treated and non-bioaugmented M. sativa. Our results show that the combination of different remediation techniques is an effective soil rehabilitation strategy to remove HFO and improve soil quality. CP plant seed treatment could be a promising option in soil clean-up and valorization.
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The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Adams J, Bornstein JM, Munno K et al (2014) Identification of compounds in heavy fuel oil that are chronically toxic to rainbow trout embryos by effects-driven chemical fractionation. Environ Toxicol Chem 33:825–835. https://doi.org/10.1002/etc.2497
Aggelopoulos CA (2022) Recent advances of cold plasma technology for water and soil remediation: a critical review. Chem Eng J 428:131657. https://doi.org/10.1016/j.cej.2021.131657
Aggelopoulos CA, Svarnas P, Klapa MI, Tsakiroglou CD (2015a) Dielectric barrier discharge plasma used as a means for the remediation of soils contaminated by non-aqueous phase liquids. Chem Eng J 270:428–436. https://doi.org/10.1016/j.cej.2015.02.056
Aggelopoulos CA, Tsakiroglou CD, Ognier S, Cavadias S (2015b) Non-aqueous phase liquid-contaminated soil remediation by ex situ dielectric barrier discharge plasma. Int J Environ Sci Technol 12:1011–1020. https://doi.org/10.1007/s13762-013-0489-4
Agnello AC, Bagard M, van Hullebusch ED et al (2016a) Comparative bioremediation of heavy metals and petroleum hydrocarbons co-contaminated soil by natural attenuation, phytoremediation, bioaugmentation and bioaugmentation-assisted phytoremediation. Sci Total Environ 563–564:693–703. https://doi.org/10.1016/j.scitotenv.2015.10.061
Agnello AC, Huguenot D, van Hullebusch ED, Esposito G (2016b) Citric acid- and Tween® 80-assisted phytoremediation of a co-contaminated soil: alfalfa (Medicago sativa L.) performance and remediation potential. Environ Sci Pollut Res 23:9215–9226. https://doi.org/10.1007/s11356-015-5972-7
Antoniadis V, Levizou E, Shaheen SM et al (2017) Trace elements in the soil-plant interface: phytoavailability, translocation, and phytoremediation–a review. Earth-Science Rev 171:621–645. https://doi.org/10.1016/j.earscirev.2017.06.005
Araújo SS, Beebe S, Crespi M et al (2015) Abiotic stress responses in legumes: strategies used to cope with environmental challenges. CRC Crit Rev Plant Sci 34:237–280. https://doi.org/10.1080/07352689.2014.898450
Benson A, Ram G, John A, Melvin Joe M (2017) Inoculation of 1-aminocyclopropane-1-carboxylate deaminase–producing bacteria along with biosurfactant application enhances the phytoremediation efficiency of Medicago sativa in hydrocarbon-contaminated soils. Bioremediat J 21:20–29. https://doi.org/10.1080/10889868.2017.1282934
Bento FM, Camargo FAO, Okeke BC, Frankenberger WT (2005) Comparative bioremediation of soils contaminated with diesel oil by natural attenuation, biostimulation and bioaugmentation. Bioresour Technol 96:1049–1055. https://doi.org/10.1016/j.biortech.2004.09.008
Brown KE, King CK, Harrison PL (2017) Lethal and behavioral impacts of diesel and fuel oil on the Antarctic amphipod Paramoera walkeri. Environ Toxicol Chem 36:2444–2455. https://doi.org/10.1002/etc.3778
Butscher D, Van Loon H, Waskow A et al (2016) Plasma inactivation of microorganisms on sprout seeds in a dielectric barrier discharge. Int J Food Microbiol 238:222–232. https://doi.org/10.1016/j.ijfoodmicro.2016.09.006
CEC (2006) Thematic strategy for soil protection. COM(2006)231 Final. Comm Eur Communities
Chaîneau CH, Rougeux G, Yéprémian C, Oudot J (2005) Effects of nutrient concentration on the biodegradation of crude oil and associated microbial populations in the soil. Soil Biol Biochem 37:1490–1497. https://doi.org/10.1016/j.soilbio.2005.01.012
Chen L, Beiyuan J, Hu W et al (2022) Phytoremediation of potentially toxic elements PTEs contaminated soils using alfalfa (Medicago sativa L.) a comprehensive review. Chemosphere 293:133577. https://doi.org/10.1016/j.chemosphere.2022.133577
D’Angelo E, Crutchfield J, Vandiviere M (2001) Rapid, sensitive, microscale determination of phosphate in water and soil. J Environ Qual 30:2206–2209. https://doi.org/10.2134/jeq2001.2206
Duan C, Razavi BS, Shen G et al (2019) Deciphering the rhizobium inoculation effect on spatial distribution of phosphatase activity in the rhizosphere of alfalfa under copper stress. Soil Biol Biochem 137:107574. https://doi.org/10.1016/j.soilbio.2019.107574
Eurostat data base (2022). https://ec.europa.eu/eurostat. Accessed Jan 2023
Eze MO, George SC, Hose GC (2021) Dose-response analysis of diesel fuel phytotoxicity on selected plant species. Chemosphere 263:128382. https://doi.org/10.1016/j.chemosphere.2020.128382
Eze MO, Thiel V, Hose GC et al (2022a) Enhancing rhizoremediation of petroleum hydrocarbons through bioaugmentation with a plant growth-promoting bacterial consortium. Chemosphere 289:133143. https://doi.org/10.1016/j.chemosphere.2021.133143
Eze MO, Thiel V, Hose GC et al (2022b) Bacteria-plant interactions synergistically enhance biodegradation of diesel fuel hydrocarbons. Commun Earth Environ 3:192. https://doi.org/10.1038/s43247-022-00526-2
Fadhlalmawla SA, Mohamed A-AH, Almarashi JQM, Boutraa T (2019) The impact of cold atmospheric pressure plasma jet on seed germination and seedlings growth of fenugreek (Trigonella foenum-graecum). Plasma Sci Technol 21:105503. https://doi.org/10.1088/2058-6272/ab2a3e
Feng J, Wang D, Shao C et al (2018) Effects of cold plasma treatment on alfalfa seed growth under simulated drought stress. Plasma Sci Technol 20:035505. https://doi.org/10.1088/2058-6272/aa9b27
Fu D, Teng Y, Luo Y et al (2012) Effects of alfalfa and organic fertilizer on benzo[a]pyrene dissipation in an aged contaminated soil. Environ Sci Pollut Res 19:1605–1611. https://doi.org/10.1007/s11356-011-0672-4
Gao H, Wu M, Liu H et al (2022) Effect of petroleum hydrocarbon pollution levels on the soil microecosystem and ecological function. Environ Pollut 293:118511. https://doi.org/10.1016/j.envpol.2021.118511
Ghasemzadeh N, Iranbakhsh A, Oraghi-Ardebili Z et al (2022) Cold plasma can alleviate cadmium stress by optimizing growth and yield of wheat (Triticum aestivum L.) through changes in physio-biochemical properties and fatty acid profile. Environ Sci Pollut Res 29:35897–35907. https://doi.org/10.1007/s11356-022-18630-3
Giovanella P, de Azevedo DL, Kita DM et al (2021) Effect of biostimulation and bioaugmentation on hydrocarbon degradation and detoxification of diesel-contaminated soil: a microcosm study. J Microbiol 59:634–643. https://doi.org/10.1007/s12275-021-0395-2
Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374. https://doi.org/10.1016/j.biotechadv.2010.02.001
Gómez-Sagasti MT, Garbisu C, Urra J et al (2021) Mycorrhizal-assisted phytoremediation and intercropping strategies improved the health of contaminated soil in a peri-urban area. Front Plant Sci 12. https://doi.org/10.3389/fpls.2021.693044
Gospodarek J, Rusin M, Barczyk G, Nadgórska-Socha A (2021) The effect of petroleum-derived substances and their bioremediation on soil enzymatic activity and soil invertebrates. Agronomy 11:80. https://doi.org/10.3390/agronomy11010080
Hall J, Soole K, Bentham R (2011) Hydrocarbon phytoremediation in the family Fabacea—a review. Int J Phytoremediation 13:317–332. https://doi.org/10.1080/15226514.2010.495143
Hamdi H, Benzarti S, Aoyama I, Jedidi N (2012) Rehabilitation of degraded soils containing aged PAHs based on phytoremediation with alfalfa (Medicago sativa L.). Int Biodeterior Biodegradation 67:40–47. https://doi.org/10.1016/j.ibiod.2011.10.009
Hewelke E, Gozdowski D (2020) Hydrophysical properties of sandy clay contaminated by petroleum hydrocarbon. Environ Sci Pollut Res 27:9697–9706. https://doi.org/10.1007/s11356-020-07627-5
Hoang SA, Lamb D, Seshadri B et al (2021) Rhizoremediation as a green technology for the remediation of petroleum hydrocarbon-contaminated soils. J Hazard Mater 401:123282. https://doi.org/10.1016/j.jhazmat.2020.123282
Hood-Nowotny R, Umana NH-N, Inselbacher E et al (2010) Alternative methods for measuring inorganic, organic, and total dissolved nitrogen in soil. Soil Sci Soc Am J 74:1018–1027. https://doi.org/10.2136/sssaj2009.0389
Howieson JG, Yates RJ, Foster KJ et al (2008) Prospects for the future use of legumes. Nitrogen-fixing leguminous symbioses. Springer, Netherlands, Dordrecht, pp 363–394
Hutchinson SL, Schwab AP, Banks MK (2001) Phytoremediation of aged petroleum sludge: effect of irrigation techniques and scheduling. J Environ Qual 30:1516–1522. https://doi.org/10.2134/jeq2001.3051516x
ISO (2005) Iso 10390:2005. Soil qality-determination of pH
Kabir AH, Rahman MM, Das U et al (2019) Reduction of cadmium toxicity in wheat through plasma technology. PLoS ONE 14:e0214509. https://doi.org/10.1371/journal.pone.0214509
Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6. https://doi.org/10.1007/BF00257924
Kauppi S, Sinkkonen A, Romantschuk M (2011) Enhancing bioremediation of diesel-fuel-contaminated soil in a boreal climate: comparison of biostimulation and bioaugmentation. Int Biodeterior Biodegradation 65:359–368. https://doi.org/10.1016/j.ibiod.2010.10.011
Khan S, Afzal M, Iqbal S, Khan QM (2013) Plant-bacteria partnerships for the remediation of hydrocarbon contaminated soils. Chemosphere 90:1317–1332
Kumar V, AlMomin S, Al-Aqeel H et al (2018) Metagenomic analysis of rhizosphere microflora of oil-contaminated soil planted with barley and alfalfa. PLoS ONE 13:e0202127. https://doi.org/10.1371/journal.pone.0202127
Lacalle RG, Gómez-Sagasti MT, Artetxe U et al (2018) Brassica napus has a key role in the recovery of the health of soils contaminated with metals and diesel by rhizoremediation. Sci Total Environ 618:347–356. https://doi.org/10.1016/j.scitotenv.2017.10.334
Li Y, Wang T, Meng Y et al (2017) Air atmospheric dielectric barrier discharge plasma induced germination and growth enhancement of wheat seed. Plasma Chem Plasma Process 37:1621–1634. https://doi.org/10.1007/s11090-017-9835-5
Li Y, Lian J, Wu B et al (2020) Phytoremediation of pharmaceutical-contaminated wastewater: insights into rhizobacterial dynamics related to pollutant degradation mechanisms during plant life cycle. Chemosphere 253:126681. https://doi.org/10.1016/j.chemosphere.2020.126681
Li F, Guo Y, Wang Z, Mu Y (2022a) Influence of different phytoremediation on soil microbial diversity and community composition in saline-alkaline land. Int J Phytoremediation 24:507–517. https://doi.org/10.1080/15226514.2021.1955240
Li Y, Ma J, Li Y et al (2022b) Nitrogen addition facilitates phytoremediation of PAH-Cd cocontaminated dumpsite soil by altering alfalfa growth and rhizosphere communities. Sci Total Environ 806:150610. https://doi.org/10.1016/j.scitotenv.2021.150610
Lim MW, Von LE, Poh PE (2016) A comprehensive guide of remediation technologies for oil contaminated soil — present works and future directions. Mar Pollut Bull 109:14–45. https://doi.org/10.1016/j.marpolbul.2016.04.023
Ling L, Jiangang L, Minchong S et al (2015) Cold plasma treatment enhances oilseed rape seed germination under drought stress. Sci Rep 5:13033. https://doi.org/10.1038/srep13033
Liu C, Yu R, Shi G (2017) Effects of drought on the accumulation and redistribution of cadmium in peanuts at different developmental stages. Arch Agron Soil Sci 63:1049–1057. https://doi.org/10.1080/03650340.2016.1271120
Liu L, Li W, Song W, Guo M (2018) Remediation techniques for heavy metal-contaminated soils: principles and applicability. Sci Total Environ 633:206–219. https://doi.org/10.1016/j.scitotenv.2018.03.161
Marchand C, Mench M, Jani Y et al (2018) Pilot scale aided-phytoremediation of a co-contaminated soil. Sci Total Environ 618:753–764. https://doi.org/10.1016/j.scitotenv.2017.08.143
McCallum MH, Kirkegaard JA, Green TW et al (2004) Improved subsoil macroporosity following perennial pastures. Aust J Exp Agric 44:299. https://doi.org/10.1071/EA03076
Mildaziene V, Pauzaite G, Naucienė Z, et al (2018) Pre‐sowing seed treatment with cold plasma and electromagnetic field increases secondary metabolite content in purple coneflower (Echinacea purpurea) leaves. Plasma Process Polym 15. https://doi.org/10.1002/ppap.201700059
Mildažienė V, Aleknavičiūtė V, Žūkienė R, et al (2019) Treatment of common sunflower (Helianthus annus L.) seeds with radio-frequency electromagnetic field and cold plasma induces changes in seed phytohormone balance, seedling development and leaf protein expression. Sci Rep 9: 6437 https://doi.org/10.1038/s41598-019-42893-5
Mitra A, Li Y-F, Klämpfl TG et al (2014) Inactivation of surface-borne microorganisms and increased germination of seed specimen by cold atmospheric plasma. Food Bioprocess Technol 7:645–653. https://doi.org/10.1007/s11947-013-1126-4
Mulligan CN, Yong RN (2004) Natural attenuation of contaminated soils. Environ Int 30:587–601. https://doi.org/10.1016/j.envint.2003.11.001
Nicula N-O, Lungulescu E-M, Ieropoulos IA et al (2022) Nutrients removal from aquaculture wastewater by biofilter/antibiotic-resistant bacteria systems. Water 14:607. https://doi.org/10.3390/w14040607
Nie M, Lu M, Yang Q et al (2011a) Plants’ use of different nitrogen forms in response to crude oil contamination. Environ Pollut 159:157–163. https://doi.org/10.1016/j.envpol.2010.09.013
Nie M, Wang Y, Yu J et al (2011b) Understanding plant-microbe interactions for phytoremediation of petroleum-polluted soil. PLoS ONE 6:e17961. https://doi.org/10.1371/journal.pone.0017961
Nwankwegu AS, Zhang L, Xie D et al (2022) Bioaugmentation as a green technology for hydrocarbon pollution remediation. Problems and Prospects J Environ Manage 304:114313. https://doi.org/10.1016/j.jenvman.2021.114313
Panagos P, Van Liedekerke M, Yigini Y, Montanarella L (2013) Contaminated sites in Europe: review of the current situation based on data collected through a European network. J Environ Public Health 2013:1–11. https://doi.org/10.1155/2013/158764
Panchenko L, Muratova A, Turkovskaya O (2017) Comparison of the phytoremediation potentials of Medicago falcata L. and Medicago sativa L. in aged oil-sludge-contaminated soil. Environ Sci Pollut Res 24:3117–3130. https://doi.org/10.1007/s11356-016-8025-y
Pande A, Pandey P, Mehra S et al (2017) Phenotypic and genotypic characterization of phosphate solubilizing bacteria and their efficiency on the growth of maize. J Genet Eng Biotechnol 15:379–391. https://doi.org/10.1016/j.jgeb.2017.06.005
Pardo T, Clemente R, Epelde L et al (2014) Evaluation of the phytostabilisation efficiency in a trace elements contaminated soil using soil health indicators. J Hazard Mater 268:68–76. https://doi.org/10.1016/j.jhazmat.2014.01.003
Payá Pérez A, Rodríguez Eugenio N (2018) Status of local soil contamination in Europe. JRC Tech Reports
Pourbabaee AA, Khazaei M, Alikhani HA, Emami S (2021) Root nodulation of alfalfa by Ensifer meliloti in petroleum contaminated soil. Rhizosphere 17:100305. https://doi.org/10.1016/j.rhisph.2021.100305
Radwan SS, Al-Mailem DM, Kansour MK (2019) Bioaugmentation failed to enhance oil bioremediation in three soil samples from three different continents. Sci Rep 9:19508. https://doi.org/10.1038/s41598-019-56099-2
Rane NR, Tapase S, Kanojia A et al (2022) Molecular insights into plant–microbe interactions for sustainable remediation of contaminated environment. Bioresour Technol 344:126246
Riser-Roberts E (2019) Remediation of petroleum contaminated soils: biological, physical, and chemical processes. CRC Press, p 580
Rostami S, Azhdarpoor A (2019) The application of plant growth regulators to improve phytoremediation of contaminated soils: a review. Chemosphere 220:818–827. https://doi.org/10.1016/j.chemosphere.2018.12.203
Roy AS, Baruah R, Borah M et al (2014) Bioremediation potential of native hydrocarbon degrading bacterial strains in crude oil contaminated soil under microcosm study. Int Biodeterior Biodegradation 94:79–89. https://doi.org/10.1016/j.ibiod.2014.03.024
Russelle MP, Birr AS (2004) Large-scale assessment of symbiotic dinitrogen fixation by crops: soybean and alfalfa in the Mississippi River Basin. Agron J 96:1754–1760. https://doi.org/10.2134/agronj2004.1754
Samac DA, Jung H-JG, Lamb JFS (2016) Development of alfalfa (Medicago sativa L.) as a feedstock for production of ethanol and other bioproducts. In: Alcoholic Fuels. CRC Press, pp 79–98
Sharov P, Dowling R, Gogishvili M et al (2016) The prevalence of toxic hotspots in former Soviet countries. Environ Pollut 211:346–353. https://doi.org/10.1016/j.envpol.2016.01.019
Staniak M, Harasim E (2018) Changes in nutritive value of alfalfa (Medicago × varia T. Martyn) and Festulolium (Festulolium braunii (K. Richt) A. Camus) under drought stress. J Agron Crop Sci 204:456–466. https://doi.org/10.1111/jac.12271
Stolárik T, Henselová M, Martinka M et al (2015) Effect of low-temperature plasma on the structure of seeds, growth and metabolism of endogenous phytohormones in pea (Pisum sativum L.). Plasma Chem Plasma Process 35:659–676. https://doi.org/10.1007/s11090-015-9627-8
Sui X, Wang X, Li Y, Ji H (2021) Remediation of petroleum-contaminated soils with microbial and microbial combined methods: advances, mechanisms, and challenges. Sustainability 13:9267. https://doi.org/10.3390/su13169267
Suriyasak C, Hatanaka K, Tanaka H et al (2021) Alterations of DNA methylation caused by cold plasma treatment restore delayed germination of heat-stressed rice (Oryza sativa L.) seeds. ACS Agric Sci Technol 1:5–10. https://doi.org/10.1021/acsagscitech.0c00070
Tamošiūnė I, Gelvonauskienė D, Haimi P, et al (2020) Cold plasma treatment of sunflower seeds modulates plant-associated microbiome and stimulates root and lateral organ growth. Front Plant Sci 11. https://doi.org/10.3389/fpls.2020.568924
Thompson OA, Wolf DC, Mattice JD, Thoma GJ (2008) Influence of nitrogen addition and plant root parameters on phytoremediation of pyrene-contaminated soil. Water Air Soil Pollut 189:37–47. https://doi.org/10.1007/s11270-007-9552-4
Tong J, He R, Zhang X et al (2014) Effects of atmospheric pressure air plasma pretreatment on the seed germination and early growth of Andrographis paniculata. Plasma Sci Technol 16:260–266. https://doi.org/10.1088/1009-0630/16/3/16
Tsai TT, Kao CM, Surampalli RY, Chien HY (2009) Enhanced bioremediation of fuel-oil contaminated soils: laboratory feasibility study. J Environ Eng 135:845–853. https://doi.org/10.1061/(ASCE)EE.1943-7870.0000049
Tyagi M, da Fonseca MMR, de Carvalho CCCR (2011) Bioaugmentation and biostimulation strategies to improve the effectiveness of bioremediation processes. Biodegradation 22:231–241. https://doi.org/10.1007/s10532-010-9394-4
Van Liedekerke M, Prokop G, Rabl-Berger S et al (2014) Progress in the management of contaminated sites in Europe. Joint Research Centre. https://doi.org/10.2788/4658
Varjani SJ (2017) Microbial degradation of petroleum hydrocarbons. Bioresour Technol 223:277–286. https://doi.org/10.1016/j.biortech.2016.10.037
Wang X, Song Y, Ma Y et al (2011) Screening of Cd tolerant genotypes and isolation of metallothionein genes in alfalfa (Medicago sativa L.). Environ Pollut 159:3627–3633. https://doi.org/10.1016/j.envpol.2011.08.001
Wang X, Fang L, Beiyuan J et al (2021) Improvement of alfalfa resistance against Cd stress through rhizobia and arbuscular mycorrhiza fungi co-inoculation in Cd-contaminated soil. Environ Pollut 277:116758. https://doi.org/10.1016/j.envpol.2021.116758
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. https://doi.org/10.1016/j.chemosphere.2019.124456
Wyszkowska J, Wyszkowski M (2010) Activity of soil dehydrogenases, urease, and acid and alkaline phosphatases in soil polluted with petroleum. J Toxicol Environ Heal Part A 73:1202–1210. https://doi.org/10.1080/15287394.2010.492004
Xie W, Zhang Y, Li R et al (2017) The responses of two native plant species to soil petroleum contamination in the Yellow River Delta, China. Environ Sci Pollut Res 24:24438–24446. https://doi.org/10.1007/s11356-017-0085-0
Yavari S, Courchesne F, Brisson J (2021) Nutrient-assisted phytoremediation of wood preservative–contaminated technosols with co-planting of Salix interior and Festuca arundinacea. Environ Sci Pollut Res 28:58018–58034. https://doi.org/10.1007/s11356-021-14076-1
Zhang H, Ma D, Qiu R et al (2017a) Non-thermal plasma technology for organic contaminated soil remediation: a review. Chem Eng J 313:157–170. https://doi.org/10.1016/j.cej.2016.12.067
Zhang JJ, Jo JO, Huynh DL et al (2017b) Growth-inducing effects of argon plasma on soybean sprouts via the regulation of demethylation levels of energy metabolism-related genes. Sci Rep 7:41917. https://doi.org/10.1038/srep41917
Zhao J, Zhang A, Héroux P et al (2021a) Remediation of diesel fuel polluted soil using dielectric barrier discharge plasma. Chem Eng J 417:128143. https://doi.org/10.1016/j.cej.2020.128143
Zhao L, Deng M, Teng Y, et al (2021b) Enhanced biomass and cadmium accumulation by three cadmium-tolerant plant species following cold plasma seed treatment. J Environ Managehttps://doi.org/10.1016/j.jenvman.2021.113212
Zhou Z, Yu M, Ding G et al (2020) Effects of Hedysarum leguminous plants on soil bacterial communities in the Mu Us Desert, northwest China. Ecol Evol 10:11423–11439. https://doi.org/10.1002/ece3.6779
Zukiene R, Nauciene Z, Januskaitiene I et al (2019) Dielectric barrier discharge plasma treatment-induced changes in sunflower seed germination, phytohormone balance, and seedling growth. Appl Phys Express 12:126003. https://doi.org/10.7567/1882-0786/ab5491
Zuzolo D, Guarino C, Tartaglia M, Sciarrillo R (2021) Plant-soil-microbiota combination for the removal of total petroleum hydrocarbons (TPH): an in-field experiment. Front Microbiol 11. https://doi.org/10.3389/fmicb.2020.621581
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Jūratė Žaltauskaitė: conceptualization, methodology, formal analysis, supervision, resources, writing—original draft, writing—review and editing. Rimas Meištininkas: methodology, formal analysis, data curation, investigation, visualization, writing—original draft, writing—review and editing. Austra Dikšaitytė: formal analysis, investigation, writing—original draft. Laima Degutytė-Fomins: investigation, writing—original draft. Vida Mildažienė: methodology, investigation, writing—original draft, resources. Zita Naučienė: investigation, writing—original draft. Rasa Žūkienė: investigation, writing—original draft. Kazunori Koga: resources.
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Žaltauskaitė, J., Meištininkas, R., Dikšaitytė, A. et al. Heavy fuel oil-contaminated soil remediation by individual and bioaugmentation-assisted phytoremediation with Medicago sativa and with cold plasma-treated M. sativa. Environ Sci Pollut Res 31, 30026–30038 (2024). https://doi.org/10.1007/s11356-024-33182-4
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DOI: https://doi.org/10.1007/s11356-024-33182-4