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Effects of Enterobacter sp. Zm-123 and spent mushroom substrate on rape growth promotion and cadmium toxicity reduction in cadmium-contaminated soil

  • Soils, Sec 4 • Ecotoxicology • Research Article
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Abstract

Purpose

The present study aims to investigate the effects of plant growth-promoting rhizobacteria (PGPR) Enterobacter sp. Zm-123 and a heavy metal adsorption biomass spent mushroom substrate (SMS) on the growth promotion of rape and reduction of cadmium (Cd) toxicity in contaminated soil.

Materials and methods

The Zm-123 fermentation broth (Zm-123) and SMS were made into three kinds of solid microbial agents by spray-mixing granulation (SG), coating granulation (CG), and semi-solid fermentation (SSF), then Zm-123, SMS, and the three kinds of solid microbial agents were applied to the rapes growing in simulated Cd-contaminated soil pots, respectively.

Results and discussion

All treatment groups significantly recovered soil physical–chemical properties and decreased exchangeable Cd (SE-Cd) in the soil (P < 0.05). All five treatment groups significantly increased the biomass and chlorophyll content of rape compared with the CK group (P < 0.05). In addition, all treatments effectively increased the activities of antioxidant enzymes catalase (CAT) and peroxidase (POD), reduced the accumulation of proline and malondialdehyde (MDA), and reduced the Cd content of the edible parts of rape. Among the five treatment groups, the SSF group showed the strongest effect, reducing soil SE-Cd by 19.56–21.94% and the Cd content in the edible part by 30.53–49.06%.

Conclusions

SMS as the substrate of the semi-solid fermentation Zm-123 treatment group can effectively remediate soil Cd contamination and promote the growth of rape.

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References

  • Abdelkrim S, Jebara SH, Saadani O, Abid G, Taamalli W, Zemni H, Mannai K, Louati F, Jebara M (2020) In situ effects of Lathyrus sativus- PGPR to remediate and restore quality and fertility of Pb and Cd polluted soils. Ecotoxicol Environ Saf 192

  • Abei H (1984) Catalase in vitro. Meth Enzymol 105:121–126

    Article  Google Scholar 

  • Ali J, Ali F, Ahmad I, Rafique M, Munis MFH, Hassan SW, Sultan T, Iftikhar M, Chaudhary HJ (2021) Mechanistic elucidation of germination potential and growth of Sesbania sesban seedlings with Bacillus anthracis PM21 under heavy metals stress: An in vitro study. Ecotoxicol Environ Saf 208

  • Ambrosini A, de Souza R, Passaglia LMP (2016) Ecological role of bacterial inoculants and their potential impact on soil microbial diversity. Plant Soil 400:193–207

    Article  CAS  Google Scholar 

  • Bao SD (2007) Soil agro-chemistrical analysis [M], vol 268–270, 3rd edn. China Agriculture Press, Beijing, pp 30–34;76–78;106–108;154–159 in Chinese

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of proline for water stress studies. Plant Soil 39:305–307

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Braud A, Jezequel K, Bazot S, Lebeau T (2009) Enhanced phytoextraction of an agricultural Cr- and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74:280–286

    Article  Google Scholar 

  • Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil - ScienceDirect. Soil Biol Biochem 17:837–842

    Article  CAS  Google Scholar 

  • Cui H, Zhou J, Zhao Q, Si Y, Mao J, Fang G, Liang J (2013) Fractions of Cu, Cd, and enzyme activities in a contaminated soil as affected by applications of micro- and nanohydroxyapatite. J Soils Sediments 13:742–752

    Article  CAS  Google Scholar 

  • Cuypers A, Plusquin M, Remans T, Jozefczak M, Keunen E, Gielen H, Opdenakker K, Nair AR, Munters E, Artois TJ, Nawrot T, Vangronsveld J, Smeets K (2010) Cadmium stress: an oxidative challenge. Biometals 23:927–940

    Article  CAS  Google Scholar 

  • Dabrowska G, Hrynkiewicz K, Trejgell A, Baum C (2017) The effect of plant growth-promoting rhizobacteria on the phytoextraction of Cd and Zn by Brassica napus L. Int J Phytorem 19:597–604

    Article  CAS  Google Scholar 

  • Dai M, Lu H, Liu W, Jia H, Hong H, Liu J, Yan C (2017) Phosphorus mediation of cadmium stress in two mangrove seedlings Avicennia marina and Kandelia obovata differing in cadmium accumulation. Ecotoxicol Environ Saf 139:272–279

    Article  CAS  Google Scholar 

  • Demiral T, Turkan I (2005) Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp Bot 53:247–257

    Article  CAS  Google Scholar 

  • El-Esawi MA, Elkelish A, Soliman M, Elansary HO, Zaid A, Wani SH (2020) Serratia marcescens BM1 enhances cadmium stress tolerance and phytoremediation potential of soybean through modulation of osmolytes, leaf gas exchange, antioxidant machinery, and stress-responsive genes expression. Antioxidants 9

  • Fang L, Cai P, Chen W, Liang W, Hong Z, Huang Q (2009) Impact of cell wall structure on the behavior of bacterial cells in the binding of copper and cadmium. Colloids Surf A 347:50–55

    Article  CAS  Google Scholar 

  • Fang XZ, Tian WH, Liu XX, Lin XY, Jin CW, Zheng SJ (2016) Alleviation of proton toxicity by nitrate uptake specifically depends on nitrate transporter 1.1 in Arabidopsis. New Phytol 211:149–158

    Article  CAS  Google Scholar 

  • Ghosh A, Pramanik K, Bhattacharya S, Mondal S, Ghosh SK, Maiti TK (2022) A potent cadmium bioaccumulating Enterobacter cloacae strain displays phytobeneficial property in Cd-exposed rice seedlings. Current Research in Microbial Sciences 3:100101–100101

    Article  CAS  Google Scholar 

  • Guo J, Lv X, Jia H, Hua L, Ren X, Muhammad H, Wei T, Ding Y (2020) Effects of EDTA and plant growth-promoting rhizobacteria on plant growth and heavy metal uptake of hyperaccumulator Sedum alfredii Hance. J Environ Sci 88:361–369

    Article  CAS  Google Scholar 

  • Guo X, Wei Z, Penn CJ, Xu T, Wu Q (2013) Effect of soil washing and liming on bioavailability of heavy metals in acid contaminated soil. Soil Sci Soc Am J 77:432–441

    Article  CAS  Google Scholar 

  • Gupta P, Rani R, Chandra A, Kumar V (2018) Potential applications of Pseudomonas sp (strain CPSB21) to ameliorate Cr6+ stress and phytoremediation of tannery effluent contaminated agricultural soils. Sci Rep 8

  • Hassan W, Bano R, Bashir F, David J (2014) Comparative effectiveness of ACC-deaminase and/or nitrogen-fixing rhizobacteria in promotion of maize (Zea mays L.) growth under lead pollution. Environ Sci Pollut Res 21:10983–10996

    Article  CAS  Google Scholar 

  • He X, Xu M, Wei Q, Tang M, Guan L, Lou L, Xu X, Hu Z, Chen Y, Shen Z, Xia Y (2020) Promotion of growth and phytoextraction of cadmium and lead in Solanum nigrum L. mediated by plant-growth-promoting rhizobacteria. Ecotoxicol Environ Saf 205

  • Jin CW, Liu Y, Mao QQ, Wang Q, Du ST (2013) Mild Fe-deficiency improves biomass production and quality of hydroponic-cultivated spinach plants (Spinacia oleracea L.). Food Chem 138:2188–2194

    Article  CAS  Google Scholar 

  • Jin K, Sleutel S, Buchan D, De Neve S, Cai DX, Gabriels D, Jin JY (2009) Changes of soil enzyme activities under different tillage practices in the Chinese Loess Plateau. Soil Tillage Res 104:115–120

    Article  Google Scholar 

  • Ju W, Liu L, Fang L, Cui Y, Duan C, Wu H (2019) Impact of co-inoculation with plant-growth-promoting rhizobacteria and rhizobium on the biochemical responses of alfalfa-soil system in copper contaminated soil. Ecotoxicol Environ Saf 167:218–226

    Article  CAS  Google Scholar 

  • Kanu AS, Ashraf U, Mo Z, Sabir SuR, Baggie I, Charley CS, Tang X (2019) Calcium amendment improved the performance of fragrant rice and reduced metal uptake under cadmium toxicity. Environ Sci Pollut Res 26:24748–24757

    Article  CAS  Google Scholar 

  • Khakimova L, Chubukova O, Vershinina Z, Maslennikova D (2023) Effects of Pseudomonas sp. OBA 2.4.1 on growth and tolerance to cadmium stress in Pisum sativum L. Biotech (Basel (Switzerland)) 12

  • Khan AR, Ullah I, Khan AL, Hong SJ, Waqas M, Park GS, Kwak Y, Choi J, Jung BK, Park M, Lee IJ, Shin JH (2014) Phytostabilization and physicochemical responses of korean ecotype Solanum nigrum L. to cadmium contamination. Water Air Soil Pollut 225

  • Li X, Ma H, Li L, Gao Y, Li Y, Xu H (2019) Subcellular distribution, chemical forms and physiological responses involved in cadmium tolerance and detoxification in Agrocybe Aegerita. Ecotoxicol Environ Saf 171:66–74

    Article  CAS  Google Scholar 

  • Li X, Zhang X, Yang Y, Li B, Wu Y, Sun H, Yang Y (2016) Cadmium accumulation characteristics in turnip landraces from China and assessment of their phytoremediation potential for contaminated soils. Front Plant Sci 7

  • Manoj SR, Karthik C, Kadirvelu K, Arulselvi PI, Shanmugasundaram T, Bruno B, Rajkumar M (2020) Understanding the molecular mechanisms for the enhanced phytoremediation of heavy metals through plant growth promoting rhizobacteria: a review. J Environ Manage 254

  • Maslennikova D, Nasyrova K, Chubukova O, Akimova E, Baymiev A, Blagova D, Ibragimov A, Lastochkina O (2022) Effects of Rhizobium leguminosarum Thy2 on the Growth and Tolerance to Cadmium Stress of Wheat Plants. Life-Basel 12

  • Mitra S, Pramanik K, Sarkar A, Ghosh PK, Soren T, Maiti TK (2018) Bioaccumulation of cadmium by Enterobacter sp. and enhancement of rice seedling growth under cadmium stress. Ecotoxicol Environ Saf 165:672–673

    Article  CAS  Google Scholar 

  • Moreira H, Pereira SIA, Marques APGC, Rangel AOSS, Castro PML (2016) Selection of metal resistant plant growth promoting rhizobacteria for the growth and metal accumulation of energy maize in a mine soil - Effect of the inoculum size. Geoderma 278:1–11

    Article  CAS  Google Scholar 

  • Neubauer U, Furrer G, Schulin R (2002) Heavy metal sorption on soil minerals affected by the siderophore desferrioxamine B: the role of Fe (III)(hydr) oxides and dissolved Fe (III). Eur J Soil Sci 53:45–55

    Article  CAS  Google Scholar 

  • Ngan NM, Riddech N (2021) Use of spent mushroom substrate as an inoculant carrier and an organic fertilizer and their impacts on roselle growth (Hibiscus sabdariffa L.) and soil quality. Waste Biomass Valorization 12:3801–3811

    Article  CAS  Google Scholar 

  • Pan F, Meng Q, Wang Q, Luo S, Chen B, Khan KY, Yang X, Feng Y (2016) Endophytic bacterium Sphingomonas SaMR12 promotes cadmium accumulation by increasing glutathione biosynthesis in Sedum alfredii Hance. Chemosphere 154:358–366

    Article  CAS  Google Scholar 

  • Patel M, Patel K, Al-Keridis LA, Alshammari N, Badraoui R, Elasbali AM, Abu Al-Soud W, Hassan M I, Yadav DK, Adnan M (2022) Cadmium-tolerant plant growth-promoting bacteria Curtobacterium oceanosedimentum improves growth attributes and strengthens antioxidant system in Chili (Capsicum frutescens). Sustainability 14

  • Podazza G, Arias M, Prado FE (2012) Cadmium accumulation and strategies to avoid its toxicity in roots of the citrus rootstock Citrumelo. J Hazard Mater 215:83–89

    Article  Google Scholar 

  • Pramanik K, Mitra S, Sarkar A, Maiti TK (2018) Alleviation of phytotoxic effects of cadmium on rice seedlings by cadmium resistant PGPR strain Enterobacter aerogenes MCC 3092. J Hazard Mater 351:317–329

    Article  CAS  Google Scholar 

  • Pramanik K, Mitra S, Sarkar A, Soren T, Maiti TK (2017) Characterization of cadmium-resistant Klebsiella pneumoniae MCC 3091 promoted rice seedling growth by alleviating phytotoxicity of cadmium. Environ Sci Pollut Res 24:24419–24437

    Article  CAS  Google Scholar 

  • Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends in Biotechnol 28:142–149

    Article  CAS  Google Scholar 

  • Ran J, Zheng W, Wang H, Wang H, Li Q (2020) Indole-3-acetic acid promotes cadmium (Cd) accumulation in a Cd hyperaccumulator and a non-hyperaccumulator by different physiological responsesy. Ecotoxicol Environ Saf 191

  • Ribas LCC, de Mendonca MM, Camelini CM, Soares CHL (2009) Use of spent mushroom substrates from Agaricus subrufescens (syn. A. blazei, A. brasiliensis) and Lentinula edodes productions in the enrichment of a soil-based potting media for lettuce (Lactuca sativa) cultivation: Growth promotion and soil bioremediation. Bioresour Technol 100:4750–4757

    Article  CAS  Google Scholar 

  • Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194

    Article  CAS  Google Scholar 

  • Sun Y, Zheng S, Wang L, Liang X, Xu Y (2020) Changes of enzymatic activities, substrate utilization pattern, and microbial community diversity in heavy metal-contaminated soils. Water Air Soil Pollut 231

  • Tapia Y, Cala V, Eymar E, Frutos I, Garate A, Masaguer A (2010) Chemical characterization and evaluation of composts as organic amendments for immobilizing cadmium. Bioresour Technol 101:5437–5443

    Article  CAS  Google Scholar 

  • Tessier AP, Campbell P, Bisson MX (1979) Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem 51:844–851

    Article  CAS  Google Scholar 

  • Ullah I, Al-Johny BO, Al-Ghamdi KMS, Al-Zahrani HAA, Anwar Y, Firoz A, Al-Kenani N, Almatry MAA (2019) Endophytic bacteria isolated from Solanum nigrum L., alleviate cadmium (Cd) stress response by their antioxidant potentials, including SOD synthesis by sodA gene. Ecotoxicol Environ Saf 174:197–207

    Article  CAS  Google Scholar 

  • Vance E (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19

  • Walker DJ, Clemente R, Roig A, Bernal MP (2003) The effects of soil amendments on heavy metal bioavailability in two contaminated Mediterranean soils. Environ Pollut 122:303–312

    Article  CAS  Google Scholar 

  • Wang F, Ouyang W, Hao F, Lin C, Song N (2014) In situ remediation of cadmium-polluted soil reusing four by-products individually and in combination. J Soils Sediments 14:451–461

    Article  CAS  Google Scholar 

  • Wei Y, Jin Z, Zhang M, Li Y, Huang S, Liu X, Jin Y, Wang H, Qu J (2020) Impact of spent mushroom substrate on Cd immobilization and soil property. Environ Sci Pollut Res 27:3007–3022

    Article  CAS  Google Scholar 

  • Wu F, Fan J, Ye X, Yang L, Hu R, Ma J, Ma S, Li D, Zhou J, Nie G, Zhang X (2022) Unraveling cadmium toxicity in Trifolium repens L. seedling: insight into regulatory mechanisms using comparative transcriptomics combined with physiological analyses. Int J Mol Sci 23

  • Xiao L, Yu Z, Liu H, Tan T, Yao J, Zhang Y, Wu J (2020) Effects of Cd and Pb on diversity of microbial community and enzyme activity in soil. Ecotoxicology 29:551–558

    Article  CAS  Google Scholar 

  • Xu Q, Pan W, Zhang R, Lu Q, Xue W, Wu C, Song B, Du S (2018) Inoculation with Bacillus subtilis and Azospirillum brasilense produces abscisic acid that reduces Irt1-mediated cadmium uptake of roots. J Agric Food Chem 66:5229–5236

    Article  CAS  Google Scholar 

  • Yang W, Wang S, Ni W, Rensing C, Xing S (2019) Enhanced Cd-Zn-Pb-contaminated soil phytoextraction by Sedum alfredii and the rhizosphere bacterial community structure and function by applying organic amendments. Plant Soil 444:101–118

    Article  CAS  Google Scholar 

  • Yang X, Feng Y, He ZL, Stoffella PJ (2005) Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. J Trace Elem Med Biol 18:339–353

    Article  CAS  Google Scholar 

  • Yu S, Liang J, Bai X, Dong L, Liu X, Wei Y, Li Y, Huang S, Qu J (2018) Inoculation of plant growth-promoting bacteria Bacillus sp YM-1 alleviates the toxicity of Pb to pakchoi. Environ Sci Pollut Res 25:28216–28225

    Article  CAS  Google Scholar 

  • Yu Z, Zhou Q (2009) Growth responses and cadmium accumulation of Mirabilis jalapa L. under interaction between cadmium and phosphorus. J Hazard Mater 167:38–43

    Article  CAS  Google Scholar 

  • Zeng X, Xu H, Lu J, Chen Q, Li W, Wu L, Tang J, Ma L (2020) The immobilization of soil cadmium by the combined amendment of bacteria and hydroxyapatite. Sci Rep 10

  • Zhang C, Xue S, Liu GB, Song ZL (2011) A comparison of soil qualities of different revegetation types in the Loess Plateau, China. Plant Soil 347:163–178

    Article  CAS  Google Scholar 

  • Zhang M, Jin Z, Zhang X, Wang G, Li R, Qu J, Jin Y (2020) Alleviation of Cd phytotoxicity and enhancement of rape seedling growth by plant growth-promoting bacterium Enterobacter sp. Zm-123. Environ Sci Pollut Res 27:33192–33203

    Article  CAS  Google Scholar 

  • Zhang YJ, Xie M, Li CY, Wu G, Peng DL (2014) Impacts of the transgenic CrylAc and CpTI insect-resistant cotton SGK321 on selected soil enzyme activities in the rhizosphere. Plant Soil Environ 60:401–406

    Article  CAS  Google Scholar 

  • Zhao H, Sun S, Zhang L, Yang J, Wang Z, Ma F, Li M (2020) Carbohydrate metabolism and transport in apple roots under nitrogen deficiency. Plant Physiol Biochem 155:455–463

    Article  CAS  Google Scholar 

  • Zhu HJ, Sun LF, Zhang YF, Zhang XL, Qiao JJ (2012) Conversion of spent mushroom substrate to biofertilizer using a stress-tolerant phosphate-solubilizing Pichia farinose FL7. Bioresour Technol 111:410–416

    Article  CAS  Google Scholar 

  • Zhu X, Lv B, Shang X, Wang J, Li M, Yu X (2019) The immobilization effects on Pb, Cd and Cu by the inoculation of organic phosphorus-degrading bacteria (OPDB) with rapeseed dregs in acidic soil. Geoderma 350:1–10

    Article  CAS  Google Scholar 

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Funding

This research was financially supported by the Natural Science Foundation of Heilongjiang Province, China (Grant No. LH2020D002).

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Authors and Affiliations

  1. School of Resources and Environment, Northeast Agricultural University, Harbin, 150030, China

    Yu Jin, Rui Yang, Yongduo Guan, Xiaochen Liu, JiaHui Fu, Xuesheng Liu & Juanjuan Qu

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  1. Yu Jin
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  2. Rui Yang
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Correspondence to Juanjuan Qu.

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Jin, Y., Yang, R., Guan, Y. et al. Effects of Enterobacter sp. Zm-123 and spent mushroom substrate on rape growth promotion and cadmium toxicity reduction in cadmium-contaminated soil. J Soils Sediments 23, 2783–2797 (2023). https://doi.org/10.1007/s11368-023-03515-w

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