Abstract
Rhizoremediation is a promising method based on the synergism between plant and rhizobacteria to remediate soil co-contaminated with heavy metals and total petroleum hydrocarbons (TPHs). A plant growth–promoting (PGP) rhizobacterium with diesel-degrading capacity and heavy metal tolerance was isolated from the rhizosphere of tall fescue (Festuca arundinacea L.), after which the effects of its inoculation on rhizoremediation performance were evaluated in heavy metal– and diesel-contaminated soil planted with tall fescue. The bacterial isolate (Novosphingobium sp. CuT1) was characterized by its indole-3-acetic acid (IAA) production, 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase activity, and siderophore productivity as PGP traits. CuT1 was able to grow on 1/10 LB-agar plates containing 5 mM of Cu or 5 mM of Pb. To evaluate the remediation effect of heavy metal– and diesel-contaminated soil by CuT1 inoculation, the experimental conditions were prepared as follows. The soil was artificially contaminated with heavy metals (Cu and Pb) at a final concentration of 500 ppm. The soil was then further contaminated with diesel at final concentrations of 0, 10,000, and 30,000 ppm. Finally, all plots were planted with tall fescue, a representative hyperaccumulating plant. Compared to the rhizoremediation performance of the co-contaminated soil (Cu + Pb + diesel) without inoculation, the bioavailable Cu concentrations in the soil and the tall fescue biomass were significantly increased in CuT1 inoculation. Additionally, the root growth of tall fescue was also promoted in CuT1 inoculation. Correlation analysis showed that Cu bioavailability and bioconcentration factor were positively correlated with CuT1 inoculation. The diesel removal efficiency showed a positive correlation with CuT1 inoculation, although the diesel removal was below 30%. CuT1 inoculation was positively correlated with IAA and dehydrogenase activity in the soil. Moreover, the dry biomass of the tall fescue’s roots was highly associated with CuT1 inoculation. Collectively, our findings suggest that Novosphingobium sp. CuT1 can be utilized as an applicable bioresource to enhance rhizoremediation performance in heavy metal– and TPH-contaminated soils.
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The datasets generated and/or analyzed during the current study are available from the corresponding author upon reasonable request.
References
Abdu N, Abdullahi AA, Abdulkadir A (2016) Heavy metals and soil microbes. Environ Chem Lett. https://doi.org/10.1007/s10311-016-0587-x
Abtahi H, Parhamfar M, Saeedi R et al (2020) Effect of competition between petroleum-degrading bacteria and indigenous compost microorganisms on the efficiency of petroleum sludge bioremediation: field application of mineral-based culture in the composting process. J Environ Manag 258:110013. https://doi.org/10.1016/j.jenvman.2019.110013
Acuña E, Castillo B, Queupuan M et al (2021) Assisted phytoremediation of lead contaminated soil using Atriplex halimus and its effect on some soil physical properties. Int J Environ Sci Technol 18:1925–1938. https://doi.org/10.1007/s13762-020-02978-5
Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals-concepts and applications. Chemosphere 91:869–881. https://doi.org/10.1016/j.chemosphere.2013.01.075
Almeida R, Mucha AP, Teixeira C et al (2013) Biodegradation of petroleum hydrocarbons in estuarine sediments: metal influence. Biodegradation 24:111–123. https://doi.org/10.1007/s10532-012-9562-9
Aransiola EF, Ige OA, Ehinmitola EO, Layokun SK (2017) Heavy metals bioremediation potential of Klebsiella species isolated from diesel polluted soil. Afr J Biotechnol 16:1098–1105. https://doi.org/10.5897/AJB2016.15823
Asad SA, Farooq M, Afzal A, West H (2019) Integrated phytobial heavy metal remediation strategies for a sustainable clean environment - a review. Chemosphere 217:925–941. https://doi.org/10.1016/j.chemosphere.2018.11.021
Banda MF, Mokgalaka NS, Combrinck S, Regnier T (2022) Five-weeks pot trial evaluation of phytoremediation potential of Helichrysum splendidum Less. for copper-and lead-contaminated soils. Int J Environ Sci Technol 19(3):1837–1848. https://doi.org/10.1007/s13762-021-03243-z
Bandara T, Herath I, Kumarathilaka P et al (2017) Efficacy of woody biomass and biochar for alleviating heavy metal bioavailability in serpentine soil. Environ Geochem Health 39:391–401. https://doi.org/10.1007/s10653-016-9842-0
Bankar A, Zinjarde S, Shinde M et al (2018) Heavy metal tolerance in marine strains of Yarrowia lipolytica. Extremophiles 22:617–628. https://doi.org/10.1007/s00792-018-1022-y
Benitez E, Melgar R, Nogales R (2004) Estimating soil resilience to a toxic organic waste by measuring enzyme activities. Soil Biol Biochem 36:1615–1623. https://doi.org/10.1016/j.soilbio.2004.07.014
Bouhadi M, Talbi M, Tarik A (2021) Phytoremediation review: bioavailability of heavy metals and the role of bioaccumulative plants in the remediation of contaminated soils. J Anal Sci Appl Biotechnol 3:40–47. https://doi.org/10.48402/IMIST.PRSM/jasab-v3i1.28238
Cha GC, Hwang MG, Chung HK et al (2003) Characteristics of cell-growth and behavior of SMP in the MBR process. J Korean Soc Environ Eng 25:155–162
Chakraborty S, Das S, Banerjee S et al (2021) Heavy metals bio-removal potential of the isolated Klebsiella sp TIU20 strain which improves growth of economic crop plant (Vigna radiata L.) under heavy metals stress by exhibiting plant growth promoting and protecting traits. Biocatal Agric Biotechnol 38:102204. https://doi.org/10.1016/j.bcab.2021.102204
Chettri B, Singh AK (2019) Kinetics of hydrocarbon degradation by a newly isolated heavy metal tolerant bacterium Novosphingobium panipatense P5:ABC. Bioresour Technol 294:122190. https://doi.org/10.1016/j.biortech.2019.122190
Chlebek D, Płociniczak T, Gobetti S et al (2022) Analysis of the genome of the heavy metal resistant and hydrocarbon-degrading rhizospheric Pseudomonas qingdaonensis zcr6 strain and assessment of its plant-growth-promoting traits. Int J Mol Sci 23. https://doi.org/10.3390/ijms23010214
Deng Z, Cao L (2017) Fungal endophytes and their interactions with plants in phytoremediation: a review. Chemosphere 168:1100–1106. https://doi.org/10.1016/j.chemosphere.2016.10.097
Divya B, Kumar MD (2011) Plant-microbe interaction with enhanced bioremediation. Res J Biotechnol 6:72–79
Fu W, Chen X, Zheng X et al (2022) Phytoremediation potential, antioxidant response, photosynthetic behavior and rhizosphere bacterial community adaptation of tobacco (Nicotiana tabacum L.) in a bisphenol A - contaminated soil. Environ Sci Pollut Res 1–17. https://doi.org/10.1007/s11356-022-21765-y
Ghani A (2010) Toxic effects of heavy metals on plant growth and metal accumulation in maize ( Zea mays L.). Iran J Toxicol 3:325–334
Gogoleva NE, Nikolaichik YA, Ismailov TT et al (2019) Complete genome sequence of the abscisic acid-utilizing strain Novosphingobium sp P6W. 3 Biotech 9:1–8. https://doi.org/10.1007/s13205-019-1625-8
Gola D, Dey P, Bhattacharya A et al (2016) Multiple heavy metal removal using an entomopathogenic fungi Beauveria bassiana. Bioresour Technol 218:388–396. https://doi.org/10.1016/j.biortech.2016.06.096
Govarthanan M, Mythili R, Selvankumar T et al (2016) Bioremediation of heavy metals using an endophytic bacterium Paenibacillus sp. RM isolated from the roots of Tridax procumbens. 3 Biotech 6:1–7. https://doi.org/10.1007/s13205-016-0560-1
Gran-Scheuch A, Ramos-Zuñiga J, Fuentes E et al (2020) Effect of co-contamination by PAHs and heavy metals on bacterial communities of diesel contaminated soils of South Shetland Islands, Antarctica. Microorganisms 8:1–17. https://doi.org/10.3390/microorganisms8111749
Ha J, Kim S, Lim H et al (2021) Selective enrichment to obtain an indigenous microbial consortium degrading recalcitrant TPHs (total petroleum hydrocarbons) from petroleum-contaminated soil in Kuwait. J Soil Groundw Environ 26:20–26. https://doi.org/10.7857/JSGE.2021.26.4.020
He X, Xu M, Wei Q et al (2020) Promotion of growth and phytoextraction of cadmium and lead in Solanum nigrum L. mediated by plant-growth-promoting rhizobacteria. Ecotoxicol Environ Saf 205:111333. https://doi.org/10.1016/j.ecoenv.2020.111333
He L, Zhu Q, Wang Y et al (2021) Irrigating digestate to improve cadmium phytoremediation potential of Pennisetum hybridum. Chemosphere 279:130592. https://doi.org/10.1016/j.chemosphere.2021.130592
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
Hong S, Cho K-S (2007) Effects of plants, rhizobacteria and physicochemical factors on the phytoremediation of contaminated soil. Kor J Microbiol Biotechnol 35:261–271
Huang X, El-alawi Y, Gurska J et al (2005) A multi-process phytoremediation system for decontamination of persistent total petroleum hydrocarbons (TPHs) from soils. Microchem J 81:139–147. https://doi.org/10.1016/j.microc.2005.01.009
Huang SS, Liao QL, Hua M et al (2007) Survey of heavy metal pollution and assessment of agricultural soil in Yangzhong district, Jiangsu Province, China. Chemosphere 67:2148–2155. https://doi.org/10.1016/j.chemosphere.2006.12.043
Hwang JS, Song HG (2020) Antifungal activity of Bacillus subtilis isolates against toxigenic fungi. Korean J Microbiol 56:28–35. https://doi.org/10.7845/kjm.2020.0011
Islam MR, Sultana T, Joe MM et al (2013) Nitrogen-fixing bacteria with multiple plant growth-promoting activities enhance growth of tomato and red pepper. J Basic Microbiol 53:1004–1015. https://doi.org/10.1002/jobm.201200141
Jin ZM, Sha W, Zhang YF et al (2013) Isolation of Burkholderia cepacia JB12 from lead- and cadmium-contaminated soil and its potential in promoting phytoremediation with tall fescue and red clover. Can J Microbiol 59:449–455. https://doi.org/10.1139/cjm-2012-0650
Jung HK, Kim JR, Woo SM, Kim SD (2007) Selection of the auxin, siderophore, and cellulose-producing PGPR, Bacillus licheniformis K11 and its plant growth promoting mechanism. J Korean Soc Appl Biol Chem 50:23–28
Ke T, Guo G, Liu J et al (2021) Improvement of the Cu and Cd phytostabilization efficiency of perennial ryegrass through the inoculation of three metal-resistant PGPR strains. Environ Pollut 271:116314. https://doi.org/10.1016/j.envpol.2020.116314
Khan WU, Ahmad SR, Yasin NA et al (2017) Effect of Pseudomonas fluorescens RB4 and Bacillus subtilis 189 on the phytoremediation potential of Catharanthus roseus (L.) in Cu and Pb contaminated soils. Int J Phytoremediation 19:1–33
Kim T-S, Choi S-I, Yang J-K et al (2010) A study on the application of enhanced phytoremediation with plant growth promoting rhizobacteria for Zn contaminated rice paddy soil. 15–26
Kim TG, Moon KE, Yun J, Cho K-S (2013) Comparison of RNA- and DNA-based bacterial communities in a lab-scale methane-degrading biocover. Appl Microbiol Biotechnol 97:3171–3181. https://doi.org/10.1007/s00253-012-4123-z
Kim Y-N, Chung M-H, Kim E-J et al (2015) Study on the productivity of microalgae Nannochloropsis sp. using the highly efficient vertical photobioreactor. J Korean Org Resour Recycl Assoc 23:38–44. https://doi.org/10.17137/korrae.2015.23.1.038
Koo SY, Cho K-S (2007) Characterization of a heavy metal-resistant and plant growth-promoting rhizobacterium, Methylobacterium sp. SY-NiR1. Kor J Microbiol Biotechnol 35:58–65
Korean Ministry of Environment Soil Environment Conservation Act, Revised in 2018a. Available online: http://www.me.go.kr/home/web/law/read.do?pagerOffset=0&maxPageItems=10&maxIndexPages=10&searchKey=lawTitle&searchValue=%ED%86%A0%EC%96%91&menuId=70&orgCd=&condition.typeCode=law&typeCode=law&lawSeq=158. Accessed on 15 September 2022
Korean Ministry of Environment Korean Standard Soil Analysis Method, Revised in 2018b. Available online: http://me.go.kr/home/web/law/read.do?pagerOffset=0&maxPageItems=10&maxIndexPages=10&searchKey=lawTitle&searchValue=%ED%86%A0%EC%96%91&menuId=71&orgCd=&condition.typeCode=admrul&typeCode=admrul&lawSeq=586. Accessed on 21 January 2022
Korean Ministry of Environment Korean Standard Wastes Analysis Method, Revised in 2017. Available online:http://me.go.kr/home/web/law/read.do?pagerOffset=0&maxPageItems=10&maxIndexPages=10&searchKey=lawTitle&searchValue=%ED%8F%90%EA%B8%B0%EB%AC%BC&menuId=71&orgCd=&condition.typeCode=admrul&typeCode=admrul&lawSeq=1296. Accessed on 21 January 2022
Krishnan R, Menon RR, Likhitha A et al (2017) Novosphingobium pokkalii sp nov, a novel rhizosphere-associated bacterium with plant beneficial properties isolated from saline-tolerant pokkali rice. Res Microbiol 168:113–121. https://doi.org/10.1016/j.resmic.2016.09.001S
Krzyżak J, Pogrzeba M, Rusinowski S et al (2017) Heavy metal uptake by novel Miscanthus Seed-Based Hybrids Cultivated in Heavy Metal Contaminated Soil. Civ Environ Eng Rep 26:121–132. https://doi.org/10.1515/ceer-2017-0040
Kujawska J, Pawłowska M (2022) The effect of amendment addition drill cuttings on heavy metals accumulation in soils and plants: experimental study and artificial network simulation. J Hazard Mater 425:127920. https://doi.org/10.1016/j.jhazmat.2021.127920
Kumar P, Thakur S, Dhingra GK et al (2018) Inoculation of siderophore producing rhizobacteria and their consortium for growth enhancement of wheat plant. Biocatal Agric Biotechnol 15:264–269. https://doi.org/10.1016/j.bcab.2018.06.019
Kunito T, Saeki K, Nagaoka K et al (2001) Characterization of copper-resistant bacterial community in rhizosphere of highly copper-contaminated soil. Eur J Soil Biol 37:95–102. https://doi.org/10.1016/S1164-5563(01)01070-6
Kwag J-S (2019) Contamination indices and heavy metal concentrations in urban garden soil of Busan Metropolis. Korean J Soil Sci Fertil 52:502–512. https://doi.org/10.7745/KJSSF.2019.52.4.502
Lee EY (2009) Effect on the concentration of glucose and sucrose on the hydrogen production using by the facultative anaerobic hydrogen producing bacterium Rhodopseudomonas sp. MeL 6–2. Kor J Microbiol Biotechnol 37:176–182
Lee A-R, Bae B-H (2011) Improved germination and seedling growth of Echinochloa crus-galli var. frumentacea in heavy metal contaminated medium by inoculation of a multiple-plant growth promoting rhizobacterium (m-PGPR). J Soil Groundw Environ 16:9–17. https://doi.org/10.7857/JSGE.2011.16.5.009
Lee J-D, Park J-A, Park B-J et al (2016) Effect of shading, light quality, and chemical elicitation on growth and bioactive compound content of Potentilla kleiniana Wight et Arnott. Korean J Plant Resour 29:363–375. https://doi.org/10.7732/kjpr.2016.29.4.363
Lee SY, Lee Y-Y, Cho K-S (2021a) Characterization of heavy metal tolerant and plant growth-promoting rhizobacteria isolated from soil contaminated with heavy metal and diesel. Microbiol Biotechnol Lett 49:413–424. https://doi.org/10.48022/mbl.2106.06013
Lee Y-Y, Seo Y, Ha M et al (2021b) Evaluation of rhizoremediation and methane emission in diesel-contaminated soil cultivated with tall fescue (Festuca arundinacea). Environ Res 194:110606. https://doi.org/10.1016/j.envres.2020.110606
Lee Y-Y, Seo Y, Ha M et al (2021c) Dynamics of bacterial functional genes and community structures during rhizoremediation of diesel-contaminated compost-amended soil. J Environ Sci Heal - Part A Toxic/hazardous Subst Environ Eng 56:1107–1120. https://doi.org/10.1080/10934529.2021.1965817
Lee Y-Y, Lee SY, Lee SD, Cho K-S (2022) Seasonal dynamics of bacterial community structure in diesel oil-contaminated soil cultivated with tall fescue (Festuca arundinacea). Int J Environ Res Public Heal 19:4629. https://doi.org/10.3390/ijerph19084629
Li Y, Sun M, He W et al (2021a) Effect of phosphorus supplementation on growth, nutrient uptake, physiological responses, and cadmium absorption by tall fescue (Festuca arundinacea Schreb.) exposed to cadmium. Ecotoxicol Environ Saf 213:112021. https://doi.org/10.1016/j.ecoenv.2021.112021
Li Z, Cao H, Yuan Y et al (2021b) Combined passivators regulate the heavy metal accumulation and antioxidant response of Brassica chinensis grown in multi-metal contaminated soils. Environ Sci Pollut Res 28(35):49166–49178. https://doi.org/10.1007/s11356-021-14193-x
Liu W, Sun J, Ding L et al (2013) Rhizobacteria (Pseudomonas sp. SB) assist phytoremediation of oily-sludge-contaminated soil by tall fescue (Festuca arundinacea L.). Plant Soil 371:533–542. https://doi.org/10.1007/s11104-013-1717-x
Liu Q, Li Q, Wang N et al (2018) Bioremediation of petroleum-contaminated soil using aged refuse from landfills. Waste Manag 77:576–585. https://doi.org/10.1016/j.wasman.2018.05.010
Liu A, Wang W, Zheng X et al (2022) Improvement of the Cd and Zn phytoremediation efficiency of rice (Oryza sativa) through the inoculation of a metal-resistant PGPR strain. Chemosphere 302:134900. https://doi.org/10.1016/j.chemosphere.2022.134900
Long Z, Huang Y, Zhang W et al (2021) Effect of different industrial activities on soil heavy metal pollution, ecological risk, and health risk. Environ Monit Assess 193:20. https://doi.org/10.1007/s10661-020-08807-z
Ma Y, Dickinson NM, Wong MH (2002) Toxicity of Pb/Zn mine tailings to the earthworm Pheretima and the effects of burrowing on metal availability. Biol Fertil Soils 36:79–86. https://doi.org/10.1007/s00374-002-0506-0
Małachowska-Jutsz A, Matyja K (2019) Discussion on methods of soil dehydrogenase determination. Int J Environ Sci Technol 16:7777–7790. https://doi.org/10.1007/s13762-019-02375-7
Mapanda F, Mangwayana EN, Nyamangara J, Giller KE (2005) The effect of long-term irrigation using wastewater on heavy metal contents of soils under vegetables in Harare, Zimbabwe. Agric Ecosyst Environ 107:151–165. https://doi.org/10.1016/j.agee.2004.11.005
Mir AR, Pichtel J, Hayat S (2021) Copper: uptake, toxicity and tolerance in plants and management of Cu-contaminated soil. Biometals 34:737–759. https://doi.org/10.1007/s10534-021-00306-z
Mitra A, Chatterjee S, Kataki S et al (2021) Bacterial tolerance strategies against lead toxicity and their relevance in bioremediation application. Environ Sci Pollut Res 28:14271–14284. https://doi.org/10.1007/s11356-021-12583-9
Moon S-J, Yoon M-H (2019) Plant growth promotion effect of Arthrobacter enclensis Yangsong-1 isolated from a button mushroom bed. J Mushrooms 17:12–18. https://doi.org/10.14480/JM.2019.17.1.12
Nagarajkumar M, Bhaskaran R, Velazhahan R (2004) Involvement of secondary metabolites and extracellular lytic enzymes produced by Pseudomonas fluorescens in inhibition of Rhizoctonia solani, the rice sheath blight pathogen. Microbiol Res 159:73–81. https://doi.org/10.1016/j.micres.2004.01.005
Nayak AK, Basu A, Panda SS et al (2019) Phytoremediation of heavy metal-contaminated tailings soil by symbiotic interaction of Cymbopogon citratus and Solanum torvum with Bacillus cereus T1B3. Soil Sediment Contam 28:547–568. https://doi.org/10.1080/15320383.2019.1634001
Nenova L, Zgorelec Z, Benkova M et al (2018) Solubility and availability of copper, zinc lead and iron in technosols under the effect of increasing copper levels. Int J Hydrol 2:379–386. https://doi.org/10.15406/ijh.2018.02.00100
Oh S-J, Kim S-C, Kim R-Y et al (2012) Change of bioavailability in heavy metal contaminated soil by chemical amendment. Korean J Soil Sci Fertil 45:973–982. https://doi.org/10.7745/KJSSF.2012.45.6.973
Peng H, Liang K, Luo H et al (2021) A Bacillus and Lysinibacillus sp. bio-augmented Festuca arundinacea phytoremediation system for the rapid decontamination of chromium influenced soil. Chemosphere 283:131186. https://doi.org/10.1016/j.chemosphere.2021.131186
Rajapaksha AU, Vithanage M, Oze C et al (2012) Nickel and manganese release in serpentine soil from the Ussangoda Ultramafic Complex, Sri Lanka. Geoderma 189–190:1–9. https://doi.org/10.1016/j.geoderma.2012.04.019
Ramirez D, Shaw LJ, Collins CD (2021) Ecotoxicity of oil sludges and residuals from their washing with surfactants: soil dehydrogenase and ryegrass germination tests. Environ Sci Pollut Res 28:13312–13322. https://doi.org/10.1007/s11356-020-11300-2
Rizwan MS, Imtiaz M, Zhu J, Yousaf B, Hussain M, Ali L, … Hu H (2021) Immobilization of Pb and Cu by organic and inorganic amendments in contaminated soil. Geoderma 385:114803
Sandrin TR, Maier RM (2003) Impact of metals on the biodegradation of organic pollutants. Environ Health Perspect 111:1093–1101. https://doi.org/10.1289/ehp.5840
Segura A, Hernández-Sánchez V, Marqués S, Molina L (2017) Insights in the regulation of the degradation of PAHs in Novosphingobium sp. HR1a and utilization of this regulatory system as a tool for the detection of PAHs. Sci Total Environ 590–591:381–393. https://doi.org/10.1016/j.scitotenv.2017.02.180
Seo Y, Cho K-S (2020) Rhizoremdiation of petroleum hydrocarbon-contaminated soils and greenhouse gas emission characteristics: a review. Microbiol Biotechnol Lett 48:99–112. https://doi.org/10.4014/mbl.1911.11014
Sprocati AR, Alisi C, Tasso F et al (2012) Effectiveness of a microbial formula, as a bioaugmentation agent, tailored for bioremediation of diesel oil and heavy metal co-contaminated soil. Process Biochem 47:1649–1655. https://doi.org/10.1016/j.procbio.2011.10.001
Vives-Peris V, Gómez-Cadenas A, Pérez-Clemente RM (2018) Salt stress alleviation in citrus plants by plant growth-promoting rhizobacteria Pseudomonas putida and Novosphingobium sp. Plant Cell Rep 37:1557–1569. https://doi.org/10.1007/s00299-018-2328-z
Wang C, Tan H, Li H et al (2020) Mechanism study of Chromium influenced soil remediated by an uptake-detoxification system using hyperaccumulator, resistant microbe consortium, and nano iron complex. Environ Pollut 257:113558. https://doi.org/10.1016/j.envpol.2019.113558
Wang L, Zhang Q, Liao X et al (2021) Phytoexclusion of heavy metals using low heavy metal accumulating cultivars: a green technology. J Hazard Mater 413:125427. https://doi.org/10.1016/j.jhazmat.2021.125427
Wang W, Liu A, Fu W et al (2022) Tobacco-associated with Methylophilus sp. FP-6 enhances phytoremediation of benzophenone-3 through regulating soil microbial community, increasing photosynthetic capacity and maintaining redox homeostasis of plant. J Hazard Mater 431:128588. https://doi.org/10.1016/j.jhazmat.2022.128588
Wolf DC, Cryder Z, Khoury R et al (2020) Bioremediation of PAH-contaminated shooting range soil using integrated approaches. Sci Total Environ 726:138440. https://doi.org/10.1016/j.scitotenv.2020.138440
Wu SC, Cheung KC, Luo YM, Wong MH (2006) Effects of inoculation of plant growth-promoting rhizobacteria on metal uptake by Brassica juncea. Environ Pollut 140:124–135. https://doi.org/10.1016/j.envpol.2005.06.023
Wu B, He T, Wang Z et al (2020) Insight into the mechanisms of plant growth promoting strain SNB6 on enhancing the phytoextraction in cadmium contaminated soil. J Hazard Mater 385:121587. https://doi.org/10.1016/j.jhazmat.2019.121587
Xu DM, Fu RB, Liu HQ, Guo XP (2021) Current knowledge from heavy metal pollution in Chinese smelter contaminated soils, health risk implications and associated remediation progress in recent decades: A critical review. J Clean Prod 286:124989. https://doi.org/10.1016/j.jclepro.2020.124989
Yahaya SM, Abubakar F, Abdu N (2021) Ecological risk assessment of heavy metal-contaminated soils of selected villages in Zamfara State, Nigeria. SN Appl Sci 3:1–13. https://doi.org/10.1007/s42452-021-04175-6
Zhang Z, Rengel Z, Meney K et al (2011) Polynuclear aromatic hydrocarbons (PAHs) mediate cadmium toxicity to an emergent wetland species. J Hazard Mater 189:119–126. https://doi.org/10.1016/j.jhazmat.2011.02.007
Zhang WH, He LY, Wang Q, Sheng XF (2015) Inoculation with endophytic Bacillus megaterium 1Y31 increases Mn accumulation and induces the growth and energy metabolism-related differentially-expressed proteome in Mn hyperaccumulator hybrid pennisetum. J Hazard Mater 300:513–521. https://doi.org/10.1016/j.jhazmat.2015.07.049
Zhong W, Xie C, Hu D et al (2020) Effect of 24-epibrassinolide on reactive oxygen species and antioxidative defense systems in tall fescue plants under lead stress. Ecotoxicol Environ Saf 187:109831. https://doi.org/10.1016/j.ecoenv.2019.109831
Zhuang X, Chen J, Shim H, Bai Z (2007) New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int 33:406–413. https://doi.org/10.1016/j.envint.2006.12.005
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This study was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (NRF-2019R1A2C2006701).
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Soo Yeon Lee, Yun-Yeong Lee, and Kyung Suk Cho contributed to the study conception and design. Material preparation and data collection were performed by Soo Yeon Lee and Yun-Yeong Lee. Data analysis was performed by Soo Yeon Lee and Kyung Suk Cho. The first draft of the manuscript was written by Soo Yeon Lee, and Kyung Suk Cho commented on the previous version of the manuscript. All the authors read and approved the final manuscript.
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Lee, S.Y., Lee, YY. & Cho, KS. Effect of Novosphingobium sp. CuT1 inoculation on the rhizoremediation of heavy metal- and diesel-contaminated soil planted with tall fescue. Environ Sci Pollut Res 30, 16612–16625 (2023). https://doi.org/10.1007/s11356-022-23339-4
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DOI: https://doi.org/10.1007/s11356-022-23339-4