Abstract
The utilization of plant growth promoting rhizobacteria (PGPR) is a potential strategy to ameliorate the rhizoremediation effect in the heavy metals (HMs) contaminated soil. In this study, a new heavy metal tolerant PGPR, Sphingomonas sp. PbM2, was isolated from the rhizosphere of maize. The siderophore production and 1-aminocyclopropane-1-carboxylic acid deaminase activity of PbM2 were superior to that of Novosphingobium sp. CuT1, an HM-tolerant PGPR, while the indole-3-acetic acid productivity of PbM2 was inferior to that of CuT1. The inoculation effect of the PGPR (PbM2 alone or a mixture of PbM2 and CuT1) on the rhizoremediation performance of HM-contaminated soil planted with maize was compared. Cu bioavailability was enhanced with PGPR treatment, while the bioconcentration factor significantly increased or remained steady depending on the HM concentration (200, 500, or 1000 mg/kg-soil) and remediation period (20 or 60 d). PGPR inoculation significantly enhanced soil PGP activity except for siderophores but was not statistically associated with improved plant growth. The dynamics change in the bacterial communities during rhizoremediation was similar for all soil conditions regardless of PGPR inoculation. Network analysis revealed that both the inoculated PGPR and indigenous rhizobacteria contributed to Cu bioavailability and soil PGP activity. These results suggest that the inoculation of PGPR is effective in the remediation performance of contaminated soil in which autogenous PGPR is inhibited.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbaszadeh-Dahaji P, Atajan FA, Omidvari M et al (2021) Mitigation of copper stress in maize (Zea mays) and sunflower (Helianthus annuus) Plants by copper-resistant Pseudomonas strains. Curr Microbiol 78:1335–1343. https://doi.org/10.1007/s00284-021-02408-w
Adhikari A, Lee K, Khan MA et al (2020) Effect of silicate and phosphate solubilizing Rhizobacterium Enterobacter ludwigii GAK2 on Oryza sativa L. under cadmium stress. J Microbiol Biotechnol 30:118–126. https://doi.org/10.4014/jmb.1906.06010
Ahmad I, Akhtar MJ, Asghar HN et al (2016) Differential effects of plant growth-promoting rhizobacteria on maize growth and cadmium uptake. J Plant Growth Regul 35:303–315. https://doi.org/10.1007/s00344-015-9534-5
Alotaibi F, Hijri M, St-Arnaud M (2021) Overview of approaches to improve rhizoremediation of petroleum hydrocarbon-contaminated soils. Appl Microbiol 2021:329–351. https://doi.org/10.3390/applmicrobiol1020023
Altimira F, Yá̃ez C, Bravo G et al (2012) Characterization of copper-resistant bacteria and bacterial communities from copper-polluted agricultural soils of central Chile. BMC Microbiol 12:1–12. https://doi.org/10.1186/1471-2180-12-193
Al-Wabel MI, Usman ARA, El-Naggar AH et al (2015) Conocarpus biochar as a soil amendment for reducing heavy metal availability and uptake by maize plants. Saudi J Biol Sci 22:503–511. https://doi.org/10.1016/j.sjbs.2014.12.003
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
Asaf S, Numan M, Khan AL, Al-Harrasi A (2020) Sphingomonas: from diversity and genomics to functional role in environmental remediation and plant growth. Crit Rev Biotechnol 40:138–152. https://doi.org/10.1080/07388551.2019.1709793
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
Benidire L, Pereira SIA, Naylo A et al (2020) Do metal contamination and plant species affect microbial abundance and bacterial diversity in the rhizosphere of metallophytes growing in mining areas in a semiarid climate? J Soils Sediments 20:1003–1017. https://doi.org/10.1007/s11368-019-02475-4
Benimeli CS, Fuentes MS, Abate CM, Amoroso MJ (2008) Bioremediation of lindane-contaminated soil by Streptomyces sp. M7 and its effects on Zea mays growth. Int Biodeterior Biodegrad 61:233–239. https://doi.org/10.1016/j.ibiod.2007.09.001
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
Bilal S, Khan AL, Shahzad R et al (2018) Mechanisms of Cr(VI) resistance by endophytic Sphingomonas sp. LK11 and its Cr(VI) phytotoxic mitigating effects in soybean (Glycine max L.). Ecotoxicol Environ Saf 164:648–658. https://doi.org/10.1016/j.ecoenv.2018.08.043
Cline MS, Smoot M, Cerami E et al (2007) Integration of biological networks and gene expression data using cytoscape. Nat Protoc 2:2366–2382. https://doi.org/10.1038/nprot.2007.324
Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678. https://doi.org/10.3389/fpls.2018.01473
Ding C, Zhao Y, Zhang Q et al (2022) Cadmium transfer between maize and soybean plants via common mycorrhizal networks. Ecotoxicol Environ Saf 232:113273. https://doi.org/10.1016/j.ecoenv.2022.113273
Dursun AY, Uslu G, Cuci Y, Aksu Z (2003) Bioaccumulation of copper(II), lead(II) and chromium(VI) by growing Aspergillus niger. Process Biochem 38:1647–1651. https://doi.org/10.1016/S0032-9592(02)00075-4
Fässler E, Robinson BH, Stauffer W et al (2010) Phytomanagement of metal-contaminated agricultural land using sunflower, maize and tobacco. Agric Ecosyst Environ 136:49–58. https://doi.org/10.1016/j.agee.2009.11.007
Fatnassi IC, Chiboub M, Saadani O et al (2015) Impact of dual inoculation with Rhizobium and PGPR on growth and antioxidant status of Vicia faba L. under copper stress. C R Biol 338:241–254. https://doi.org/10.1016/j.crvi.2015.02.001
Ferrarini A, Fracasso A, Spini G et al (2021) Bioaugmented phytoremediation of metal-contaminated soils and sediments by hemp and giant reed. Front Microbiol 12:1–20. https://doi.org/10.3389/fmicb.2021.645893
Ghazy N, El-Nahrawy S (2021) Siderophore production by Bacillus subtilis MF497446 and Pseudomonas koreensis MG209738 and their efficacy in controlling Cephalosporium maydis in maize plant. Arch Microbiol 203:1195–1209. https://doi.org/10.1007/s00203-020-02113-5
Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374. https://doi.org/10.1016/j.biotechadv.2010.02.001
Gopalakrishnan S, Sathya A, Vijayabharathi R et al (2015) Plant growth promoting rhizobia: challenges and opportunities. 3 Biotech 5:355–377. https://doi.org/10.1007/s13205-014-0241-x
Grobelak A, Kokot P, Światek J et al (2018) Bacterial ACC deaminase activity in promoting plant growth on areas contaminated with heavy metals. J Ecol Eng 19:150–157. https://doi.org/10.12911/22998993/89818
Guarino C, Marziano M, Tartaglia M et al (2020) Poaceae with PGPR bacteria and arbuscular mycorrhizae partnerships as a model system for plant microbiome manipulation for phytoremediation of petroleum hydrocarbons contaminated agricultural soils. Agronomy 10:1–17. https://doi.org/10.3390/agronomy10040547
Gulzar ABM, Mazumder PB (2022) Helping plants to deal with heavy metal stress: the role of nanotechnology and plant growth promoting rhizobacteria in the process of phytoremediation. Environ Sci Pollut Res 29:40319–40341. https://doi.org/10.1007/s11356-022-19756-0
Guo J, Chi J (2014) Effect of Cd-tolerant plant growth-promoting rhizobium on plant growth and Cd uptake by Lolium multiflorum Lam. and Glycine max (L.) Merr. in Cd-contaminated soil. Plant Soil 375:205–214. https://doi.org/10.1007/s11104-013-1952-1
Gupta VK, Nayak A, Agarwal S (2015) Bio adsorbents for remediation of heavy metals: current status and their future prospects. Environ Eng Res 20:1–18. https://doi.org/10.4491/eer.2015.018
Hadi F, Bano A (2010) Effect of diazotrophs (Rhizobium and azatebactor) on growth of maize (Zea mays L.) and accumulation of lead (Pb) in different plant parts. Pakistan J Bot 42:4363–4370
Han JH, Kwon HJ, Lee CH (2014) Effect of arsenic types in soil on growth and arsenic accumulation of Pteris multifida. Korean J Plant Resour 27:344–353. https://doi.org/10.7732/kjpr.2014.27.4.344
Hong S, Min SL, Lee EY (2011) Bioremediation efficiency of oil-contaminated soil using microbial agents. Korean J Microbiol Biotechnol 39:301–307
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
Hussein KA, Joo JH (2014) Potential of siderophore production by bacteria isolated from heavy metal: Polluted and rhizosphere soils. Curr Microbiol 68:717–723. https://doi.org/10.1007/s00284-014-0530-y
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
Jinal HN, Gopi K, Kumar K, Amaresan N (2021) Effect of zinc-resistant Lysinibacillus species inoculation on growth, physiological properties, and zinc uptake in maize (Zea mays L.). Environ Sci Pollut Res 28:6540–6548. https://doi.org/10.1007/s11356-020-10998-4
Kamran MA, Syed JH, Eqani SAMAS et al (2015) Effect of plant growth-promoting rhizobacteria inoculation on cadmium (Cd) uptake by Eruca sativa. Environ Sci Pollut Res 22:9275–9283. https://doi.org/10.1007/s11356-015-4074-x
Khan AL, Waqas M, Kang SM et al (2014) Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. J Microbiol 52:689–695. https://doi.org/10.1007/s12275-014-4002-7
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 photobioractor. J Korea Org Resour Recycl Assoc 23:38–44. https://doi.org/10.17137/korrae.2015.23.1.038
Kim M, Min H, Lee S, Kim J (2020) Effects of amendments on heavy metal uptake by leafy, root, fruit vegetables in alkali upland soil. Ecol Resilient Infrastruct 7:63–71. https://doi.org/10.17820/eri.2020.7.1.063
Koo S, Cho K (2007) Characterization of a heavy metal-resistant and plant growth-promoting rhizobacterium, Methylo-bacterium sp. SY-NiR1. Kor J Microbiol Biotechnol 35:58–65
Kou B, He Y, Wang Y et al (2023) The relationships between heavy metals and bacterial communities in a coal gangue site. Environ Pollut 322:121136. https://doi.org/10.1016/j.envpol.2023.121136
Krzyżak J, Pogrzeba M, Rusinowski S et al (2017) Heavy metal uptake by novel miscanthus seed-based hybrids cultivated in heavy metal contaminated soil. Civil Environ Eng Rep 26:121–132. https://doi.org/10.1515/ceer-2017-0040
Kwag J-S, Cho G-J, Jeong M-E et al (2019) Contamination indices and heavy metal concentrations in urban garden soil of busan metropolis. Korean J Soil Sci Fert 52:502–512. https://doi.org/10.7745/KJSSF.2019.52.4.502
Lasudee K, Tokuyama S, Lumyong S, Pathom-Aree W (2017) Mycorrhizal spores associated Lysobacter soli and its plant growth promoting activity. Chiang Mai J Sci 44:94–101
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. Korean J Microbiol Biotechnol 37:176–182
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 YY, Seo Y, Ha M et al (2021) 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 YY, Lee SY, Lee SD, Cho K (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
Lee SY, Lee YY, Cho KS (2023) 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. https://doi.org/10.1007/s11356-022-23339-4
Li X, Geng X, Xie R et al (2016) The endophytic bacteria isolated from elephant grass (Pennisetum purpureum Schumach) promote plant growth and enhance salt tolerance of Hybrid Pennisetum. Biotechnol Biofuels 9:1–12. https://doi.org/10.1186/s13068-016-0592-0
Li FL, Qiu Y, Xu X et al (2020) EDTA-enhanced phytoremediation of heavy metals from sludge soil by Italian ryegrass (Lolium perenne L.). Ecotoxicol Environ Saf 191:110185. https://doi.org/10.1016/j.ecoenv.2020.110185
Limanska N, Ivanytsia T, Basiul O et al (2013) Effect of Lactobacillus plantarum on germination and growth of tomato seedlings. Acta Physiol Plant 35:1587–1595. https://doi.org/10.1007/s11738-012-1200-y
Liu A, Wang W, Chen X et al (2022) Phytoremediation of DEHP and heavy metals co-contaminated soil by rice assisted with a PGPR consortium: Insights into the regulation of ion homeostasis, improvement of photosynthesis and enrichment of beneficial bacteria in rhizosphere soil. Environ Pollut 314:120303. https://doi.org/10.1016/j.envpol.2022.120303
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, Oliveira RS, Freitas H, Zhang C (2016a) Biochemical and molecular mechanisms of plant-microbe-metal interactions: relevance for phytoremediation. Front Plant Sci 7:918. https://doi.org/10.3389/fpls.2016.00918
Ma Y, Rajkumar M, Zhang C, Freitas H (2016b) Inoculation of Brassica oxyrrhina with plant growth promoting bacteria for the improvement of heavy metal phytoremediation under drought conditions. J Hazard Mater 320:36–44. https://doi.org/10.1016/j.jhazmat.2016.08.009
Ma Y, Wang Y, Chen Q et al (2020) Assessment of heavy metal pollution and the effect on bacterial community in acidic and neutral soils. Ecol Indic 117:106626. https://doi.org/10.1016/j.ecolind.2020.106626
Ma C, Hua J, Li H et al (2022a) Inoculation with carbofuran-degrading rhizobacteria promotes maize growth through production of IAA and regulation of the release of plant-specialized metabolites. Chemosphere 307:136027. https://doi.org/10.1016/j.chemosphere.2022.136027
Ma L, An R, Jiang L et al (2022b) Effects of ZmHIPP on lead tolerance in maize seedlings: novel ideas for soil bioremediation. J Hazard Mater 430:128457. https://doi.org/10.1016/j.jhazmat.2022.128457
Madhaiyan M, Poonguzhali S, Senthilkumar M et al (2015) Arachidicoccus rhizosphaerae gen. Nov., sp. nov., a plant-growth-promoting bacterium in the family Chitinophagaceae isolated from rhizosphere soil. Int J Syst Evol Microbiol 65:578–586. https://doi.org/10.1099/ijs.0.069377-0
Madline A, Benidire L, Boularbah A (2021) Alleviation of salinity and metal stress using plant growth-promoting rhizobacteria isolated from semiarid Moroccan copper-mine soils. Environ Sci Pollut Res 28:67185–67202. https://doi.org/10.1007/s11356-021-15168-8
Malekzadeh E, Alikhani HA, Savaghebi-Firoozabadi GR, Zarei M (2012) Bioremediation of cadmium-contaminated soil through cultivation of maize inoculated with plant growth-promoting rhizobacteria. Bioremediat J 16:204–211. https://doi.org/10.1080/10889868.2012.703258
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
Meng M, Yang L, Wei B et al (2021) Plastic shed production systems: the migration of heavy metals from soil to vegetables and human health risk assessment. Ecotoxicol Environ Saf 215:112106. https://doi.org/10.1016/j.ecoenv.2021.112106
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
Mushtaq Z, Liaquat M, Nazir A et al (2022) Potential of plant growth promoting rhizobacteria to mitigate chromium contamination. Environ Technol Innov. https://doi.org/10.1016/j.eti.2022.102826
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
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
Ni G, Shi G, Hu C et al (2021) Selenium improved the combined remediation efficiency of Pseudomonas aeruginosa and ryegrass on cadmium-nonylphenol co-contaminated soil. Environ Pollut 287:117552. https://doi.org/10.1016/j.envpol.2021.117552
Nozari RM, Ortolan F, Astarita LV, Santarém ER (2021) Streptomyces spp. enhance vegetative growth of maize plants under saline stress. Brazilian J Microbiol 52:1371–1383. https://doi.org/10.1007/s42770-021-00480-9
Patel TM, Minocheherhomji FP (2020) Isolation and screening of phytohormones producing pgpr from cotton plant rhizospheric soil. J Adv Sci Res 11:148–154
Pianelli K, Mari S, Marquès L et al (2005) Nicotianamine over-accumulation confers resistance to nickel in Arabidopsis thaliana. Transgenic Res 14:739–748. https://doi.org/10.1007/s11248-005-7159-3
Putrie RFW, Widowati T, Sukiman H (2017) Studies for IAA (Indole-3-Acetic Acid) production by isolates H6 with nitric acid mutation. Microbiol Indones 11:18–22. https://doi.org/10.5454/mi.11.1.3
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
Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574. https://doi.org/10.1016/j.biotechadv.2012.04.011
Raklami A, Oubane M, Meddich A et al (2021) Phytotoxicity and genotoxicity as a new approach to assess heavy metals effect on Medicago sativa L.: Role of metallo-resistant rhizobacteria. Environ Technol Innov 24:101833. https://doi.org/10.1016/j.eti.2021.101833
Romdhane L, Panozzo A, Radhouane L et al (2021) Root characteristics and metal uptake of maize (Zea mays L.) under extreme soil contamination. Agronomy 11:178. https://doi.org/10.3390/agronomy11010178
Roriz M, Pereira SIA, Castro PML et al (2021) Iron metabolism in soybean grown in calcareous soil is influenced by plant growth-promoting rhizobacteria – A functional analysis. Rhizosphere 17:100274. https://doi.org/10.1016/j.rhisph.2020.100274
Sangsuwan P, Prapagdee B (2021) Cadmium phytoremediation performance of two species of Chlorophytum and enhancing their potentials by cadmium-resistant bacteria. Environ Technol Innov 21:101311. https://doi.org/10.1016/j.eti.2020.101311
Sani RK, Peyton BM, Brown LT (2001) Copper-induced inhibition of growth of Desulfovibrio desulfuricans G20: assessment of its toxicity and correlation with those of zinc and lead. Appl Environ Microbiol 67:4765–4772. https://doi.org/10.1128/AEM.67.10.4765
Sazykin I, Khmelevtsova L, Azhogina T, Sazykina M (2023) Heavy metals influence on the bacterial community of soils: a review. Agriculture 13:653. https://doi.org/10.3390/agriculture13030653
Srinivasan R, Mageswari A, Subramanian P et al (2017) Exogenous expression of ACC deaminase gene in psychrotolerant bacteria alleviates chilling stress and promotes plant growth in millets under chilling conditions. Indian J Exp Biol 55:463–468
Sukweenadhi J, Kim YJ, Kang CH et al (2015) Sphingomonas panaciterrae sp. nov. a plant growth-promoting bacterium isolated from soil of a ginseng field. Arch Microbiol 197:973–981. https://doi.org/10.1007/s00203-015-1134-z
Tang X, Huang Y, Li Y et al (2022) The response of bacterial communities to V and Cr and novel reducing bacteria near a vanadium titanium magnetite refinery. Sci Total Environ 806:151214. https://doi.org/10.1016/j.scitotenv.2021.151214
Tangaromsuk J, Pokethitiyook P, Kruatrachue M, Upatham ES (2002) Cadmium biosorption by Sphingomonas paucimobilis biomass. Bioresour Technol 85:103–105. https://doi.org/10.1016/S0960-8524(02)00066-4
Tirry N, Kouchou A, El Omari B et al (2021) Improved chromium tolerance of Medicago sativa by plant growth-promoting rhizobacteria (PGPR). J Genet Eng Biotechnol 19:149. https://doi.org/10.1186/s43141-021-00254-8
Tsavkelova EA, Egorova MA, Leontieva MR et al (2016) Dendrobium nobile Lindl. seed germination in co-cultures with diverse associated bacteria. Plant Growth Regul 80:79–91. https://doi.org/10.1007/s10725-016-0155-1
Wang H, Zhong G, Shi G, Pan F (2011) Toxicity of Cu, Pb, and Zn on seed germination and young seedlings of wheat (Triticum aestivum L.). IFIP Adv Inf Commun Technol 346:231–240. https://doi.org/10.1007/978-3-642-18354-6_29
Wang T, Wang X, Tian W et al (2020a) Screening of heavy metal-immobilizing bacteria and its effect on reducing Cd2+ and Pb2+ concentrations in water spinach (Ipomoea aquatic forsk.). Int J Environ Res Public Health 17:3122. https://doi.org/10.3390/ijerph17093122
Wang Y, Liu Y, Zhan W et al (2020b) Long-term stabilization of Cd in agricultural soil using mercapto-functionalized nano-silica (MPTS/nano-silica): a three-year field study. Ecotoxicol Environ Saf 197:110600. https://doi.org/10.1016/j.ecoenv.2020.110600
Wang G, Jin Z, Wang X et al (2022) Simulated root exudates stimulate the abundance of Saccharimonadales to improve the alkaline phosphatase activity in maize rhizosphere. Appl Soil Ecol 170:104274. https://doi.org/10.1016/j.apsoil.2021.104274
Wang L, Wang N, Guo D et al (2023) Rhizobacteria helps to explain the enhanced efficiency of phytoextraction strengthened by Streptomyces pactum. J Environ Sci (china) 125:73–81. https://doi.org/10.1016/j.jes.2022.01.022
Widawati S, Suliasih, (2018) The effect of plant growth promoting rhizobacteria (PGPR) on germination and seedling growth of Sorghum bicolor L. Moench. IOP Conf Ser Earth Environ Sci 166:9–14. https://doi.org/10.1088/1755-1315/166/1/012022
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
Xia LC, Steele JA, Cram JA et al (2011) Extended local similarity analysis (eLSA) of microbial community and other time series data with replicates. BMC Syst Biol. https://doi.org/10.1186/1752-0509-5-S2-S15
Xiong C, Zhang Y, Xu X et al (2013) Lotus roots accumulate heavy metals independently from soil in main production regions of China. Sci Hortic 164:295–302. https://doi.org/10.1016/j.scienta.2013.09.013
Xu Z, Wang D, Tang W et al (2020) Phytoremediation of cadmium-polluted soil assisted by D-gluconate-enhanced Enterobacter cloacae colonization in the Solanum nigrum L. rhizosphere. Sci Total Environ 732:139265. https://doi.org/10.1016/j.scitotenv.2020.139265
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 H, Dang Z, Zheng LC, Yi XY (2009) Remediation of soil co-contaminated with pyrene and cadmium by growing maize (Zea mays L.). Int J Environ Sci Technol 6:249–258. https://doi.org/10.1007/BF03327629
Zhang L, Xue L, Wang H et al (2022a) Immobilization of Pb and Cd by two strains and their bioremediation effect to an iron tailings soil. Process Biochem 113:194–202. https://doi.org/10.1016/j.procbio.2021.12.026
Zhang S, Kong Z, Wang H et al (2022b) Enhanced nitrate removal by biochar supported nano zero-valent iron (nZVI) at biocathode in bioelectrochemical system (BES). Chem Eng J 433:133535. https://doi.org/10.1016/j.cej.2021.133535
Acknowledgements
This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean Government through the Ministry of Science and ICT (MSIT) (2019R1A2C2006701 & 2022R1A2C2006615).
Author information
Authors and Affiliations
Contributions
Data curation, visualization, validation, writing—original draft and review were contributed by SYL; data curation, validation, review were contributed by Y-YL; review, edition, supervision were contributed by K-SC.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Editorial responsibility: Josef Trögl.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Lee, S.Y., Lee, YY. & Cho, KS. Inoculation effect of heavy metal tolerant and plant growth promoting rhizobacteria for rhizoremediation. Int. J. Environ. Sci. Technol. 21, 1419–1434 (2024). https://doi.org/10.1007/s13762-023-05078-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13762-023-05078-2