Skip to main content

Advertisement

SpringerLink
Log in

Nitrogen fertilizer management affects remobilization of the immobilized cadmium in soil and its accumulation in crop tissues

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Immobilization of soil cadmium (Cd) has been the strategy mostly used in remediation of Cd-contaminated arable soil. However, Cd might be remobilized after the immobilization process through the acid-soluble and complexation effects. Development of agronomic management technologies to prevent soil Cd remobilization after the immobilization process was an important pathway to control the food safety of agricultural products in soils with the immobilized Cd. In this study, the ammonia (NH4+-N) and nitrate (NO3−-N) forms with concentrations of 60, 90, and 150 mg-N kg−1 soil were performed for evaluating their effects on Cd remobilization with planted or unplanted treatments and Cd accumulation in tissues of edible amaranth (Liuye). With an initial soil palygorskite-bound fraction Cd concentration of 0.6 mg kg−1, bioavailable Cd in rhizosphere soils and Cd in crop shoots respectively increased from 11.4 to 20.6 μg kg−1 (dry soil weight) and 6.92 to 14.92 mg kg−1 (dry plant weight) in planted NH4+-N treatments, while significantly lower concentrations of bioavailable Cd in rhizosphere soils and Cd in crop tissues were observed with planted NO3−-N treatments. Compared with that of planted NO3−-N treatments, decreasing pH value (i.e., 7.64 to 7.18) induced by root proton efflux during the absorption of NH4+-N, enhancive organic/amino acid (oxalic acid, lactic acid, l-proline, and so on) secretion from roots, and increasing abundance of bacteria distributed in phyla Proteobacteria, Cyanobacteria, and Bacteroidetes with Cd mobilization ability in rhizosphere soils were the main reasons found in this study for the higher Cd remobilization in soils and Cd accumulation in crop under NH4+-N treatments. Moreover, the direct effect of NH4+-N on remobilization of immobilized Cd by upregulating the expression abundances of genes associated with pyruvate metabolism and amino acids metabolism was more significant than that of NO3−-N. In summary, the use of NO3−-N as preferred N fertilizer was more efficient to ensure the food safety of agricultural products than that of NH4+-N in Cd-contaminated arable soil after immobilization process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The data used to support the findings of this study are available from the corresponding author upon request.

References

  • Abeywickrama CJ, Wansapala J (2019) Review of organic and conventional agricultural products: heavy metal availability, accumulation and safety. Int J Food Saf Nutr Public Health:31–43

  • Britto DT, Kronzucker HJ (2005) Nitrogen acquisition, PEP carboxylase, and cellular pH homeostasis: new views on old paradigms. Plant Cell Environ 28:1396–1409

    Article  CAS  Google Scholar 

  • Carvalhais LC, Dennis PG, Fedoseyenko D, Hajirezaei MR, Borriss R, von Wirén N (2011) Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. J Plant Nutr Soil Sci 174:3–11

    Article  CAS  Google Scholar 

  • Dai Y, Liu R, Zhou Y, Li N, Hou L, Ma Q, Gao B (2020) Fire Phoenix facilitates phytoremediation of PAH-Cd co-contaminated soil through promotion of beneficial rhizosphere bacterial communities. Environ Int 136:105421

    Article  CAS  Google Scholar 

  • De Quintero MR, Hanson JB (1984) Reactions of corn root tissue to calcium. Plant Physiol 76(2):403–408

    Article  Google Scholar 

  • Fan B, Carvalhais LC, Becker A, Fedoseyenko D, von Wirén N, Borriss R (2012) Transcriptomic profiling of Bacillus amyloliquefaciens FZB42 in response to maize root exudates. BMC Microbiol 12(1):116

  • Ferreira EC, Neto JAG, Milori DM, Ferreira EJ, Anzano JM (2015) Laser-induced breakdown spectroscopy: extending its application to soil pH measurements. Spectrochim Acta B At Spectrosc 110:96–99

    Article  CAS  Google Scholar 

  • Gao Q, Li Q-S, He B-Y, Yang J-Q, Wang L-L, Wang J-F, Jiang J-J, Wang D-S, Wang Y-F (2019) Phosphate-solubilizing bacteria will not significantly remobilize soil cadmium remediated by weathered coal. Environ Sci Pollut Res 26(28):29003–29011

    Article  CAS  Google Scholar 

  • Gassama UM, Puteh AB, Abd-Halim MR, Kargbo B (2015) Influence of municipal wastewater on rice seed germination, seedling performance, nutrient uptake, and chlorophyll content. J Crop Sci Biotechnol 18:9–19

    Article  Google Scholar 

  • Gaxiola RA, Palmgren MG, Schumacher K (2007) Plant proton pumps. FEBS Lett 581:2204–2214

    Article  CAS  Google Scholar 

  • Guo SH, Hu N, Li QS, Yang P, Wang LL, Xu ZM, Chen HJ, He BY, Zeng EY (2018) Response of edible amaranth cultivar to salt stress led to Cd mobilization in rhizosphere soil: a metabolomic analysis. Environ Pollut 241:422–431

    Article  CAS  Google Scholar 

  • He BY, Yu DP, Chen Y, Shi JL, Xia Y, Li QS, Wang LL, Ling L, Zeng EY (2017) Use of low-calcium cultivars to reduce cadmium uptake and accumulation in edible amaranth (Amaranthus mangostanus L.). Chemosphere 171:588–594

    Article  CAS  Google Scholar 

  • Hu J, Zhou Y, Lei Z, Liu G, Hua Y, Zhou W, Wan X, Zhu D, Zhao J (2020) Effects of Potamogeton crispus decline in the rhizosphere on the abundance of anammox bacteria and nirS denitrifying bacteria. Environ Pollut 260:114018

    Article  CAS  Google Scholar 

  • Jiang N, Juan Y, Tian L, Chen X, Sun W, Chen L (2018) Modification of the composition of dissolved nitrogen forms, nitrogen transformation processes, and diversity of bacterial communities by freeze–thaw events in temperate soils. Pedobiologia 71:41–49

    Article  Google Scholar 

  • Jiang J-J, Wang J-F, Yang P, Xu Z-M, He T, Gao Q, Wang L-L, Li Q-S (2019) Interactive effects between cadmium stabilized by palygorskite and mobilized by siderophores from Pseudomonas fluorescens. Ecotoxicol Environ Saf 181:265–273

    Article  CAS  Google Scholar 

  • Kumari A, Parida AK (2018) Metabolomics and network analysis reveal the potential metabolites and biological pathways involved in salinity tolerance of the halophyte Salvadora persica. Environ Exp Bot 148:85–99

    Article  CAS  Google Scholar 

  • Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821

    Article  CAS  Google Scholar 

  • Li WL, Wang JF, Lv Y, Dong HJ, Wang LL, He T, Li QS (2020) Improving cadmium mobilization by phosphate-solubilizing bacteria via regulating organic acids metabolism with potassium. Chemosphere 244:125475

    Article  CAS  Google Scholar 

  • Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry–based metabolite profiling in plants. Nat Protoc 1:387–396

    Article  CAS  Google Scholar 

  • Liu T, Yu L, Xu J, Yan X, Li H, Whalen JK, Hu F (2017) Bacterial traits and quality contribute to the diet choice and survival of bacterial-feeding nematodes. Soil Biol Biochem 115:467–474

    Article  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Senthilkumar M, Pragatheswari D, Lee JS, Lee KC (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(2):578–586

    Article  CAS  Google Scholar 

  • Malviya R, Chaudhary R (2006) Factors affecting hazardous waste solidification/stabilization: A review. J Hazard Mater 137:267–276

    Article  CAS  Google Scholar 

  • Maurer F, Christl I, Hoffmann M, Kretzschmar R (2012) Reduction and reoxidation of humic acid: influence on speciation of cadmium and silver. Environ Sci Technol 46:8808–8816

    Article  CAS  Google Scholar 

  • Mei X, Li S, Li Q, Yang Y, Luo X, He B, Li H, Xu Z (2014) Sodium chloride salinity reduces Cd uptake by edible amaranth (Amaranthus mangostanus L.) via competition for Ca channels. Ecotoxicol Environ Saf 105:59–64

    Article  CAS  Google Scholar 

  • Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J 8:1577–1587

    Article  CAS  Google Scholar 

  • Narendrula-Kotha R, Nkongolo KK (2017) Bacterial and fungal community structure and diversity in a mining region under long-term metal exposure revealed by metagenomics sequencing. Ecol Genet Genom 2:13–24

    Google Scholar 

  • Nie Y, Wang M, Zhang W, Ni Z, Hashidoko Y, Shen W (2018) Ammonium nitrogen content is a dominant predictor of bacterial community composition in an acidic forest soil with exogenous nitrogen enrichment. Sci Total Environ 624:407–415

    Article  CAS  Google Scholar 

  • O'Brien JA, Vega A, Bouguyon E, Krouk G, Gojon A, Coruzzi G, Gutiérrez RA (2016) Nitrate transport, sensing, and responses in plants. Mol Plant 9:837–856

    Article  CAS  Google Scholar 

  • Parker JL, Newstead S (2014) Molecular basis of nitrate uptake by the plant nitrate transporter nrt1.1. Nature 507(7490):68–72

    Article  CAS  Google Scholar 

  • Riaz U, Aslam A, Zaman QU, Javeid S, Jamil M (2020) Cadmium contamination, bioavailability, uptake mechanism and remediation strategies in soil-plant-environment system: a critical review. Curr Anal Chem 17(1):1–12

    Article  CAS  Google Scholar 

  • Rudrappa T, Czymmek KJ, Paré PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148(3):1547–1556

    Article  CAS  Google Scholar 

  • Sasse J, Martinoia E, Northen T (2018) Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci 23:25–41

    Article  CAS  Google Scholar 

  • Scheible WR, Gonzalez FA, Lauerer M, Muller RB, Caboche M, Stitt M (1997) Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9:783–798

    Article  CAS  Google Scholar 

  • Song H, Peng L, Li Z, Deng X, Shao J, Gu J-d (2019) Metal distribution and biological diversity of crusts in paddy fields polluted with different levels of cadmium. Ecotoxicol Environ Saf 184:109620

    Article  CAS  Google Scholar 

  • Stein SE (1999) An integrated method for spectrum extraction and compound identification from gas chromatography/mass spectrometry data. J Am Soc Mass Spectrom 10:770–781

    Article  CAS  Google Scholar 

  • Su H, Fang Z, Tsang PE, Zheng L, Cheng W, Fang J, Zhao D (2016) Remediation of hexavalent chromium contaminated soil by biochar-supported zero-valent iron nanoparticles. J Hazard Mater 318:533–540

    Article  CAS  Google Scholar 

  • Tao Q, Zhao J, Li J, Liu Y, Luo J, Yuan S, Li B, Li Q, Xu Q, Yu X, Huang H, Li T, Wang C (2020) Unique root exudate tartaric acid enhanced cadmium mobilization and uptake in Cd-hyperaccumulator Sedum alfredii. J Hazard Mater 383:121177

    Article  CAS  Google Scholar 

  • Tegeder M (2012) Transporters for amino acids in plant cells: some functions and many unknowns. Curr Opin Plant Biol 15:315–321

    Article  CAS  Google Scholar 

  • Tegeder M, Tan Q, Grennan AK, Patrick JW (2007) Amino acid transporter expression and localisation studies in pea (Pisum sativum). Funct Plant Biol 34:1019–1028

    Article  CAS  Google Scholar 

  • Tian Y, Zhang X, Wang J, Gao L (2013) Soil microbial communities associated with the rhizosphere of cucumber under different summer cover crops and residue management: a 4-year field experiment. Sci Hortic 150:100–109

    Article  Google Scholar 

  • van Dam NM, Bouwmeester HJ (2016) Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci 21:256–265

    Article  Google Scholar 

  • Wang J, Zhou Y, Zhou C, Shen Q, Putheti R (2009) Effects of NH4+-N/NO3--N ratios on growth, nitrate uptake and organic acid levels of spinach (Spinacia oleracea L.). Afr J Biotechnol 8(15). https://doi.org/10.4314/ajb.v8i15.61860

  • Wångstrand H, Eriksson J, Öborn I (2007) Cadmium concentration in winter wheat as affected by nitrogen fertilization. Eur J Agron 26(3):209–214

    Article  Google Scholar 

  • Wei S, Wang S, Zhou Q, Zhan J, Ma L, Wu Z, Sun T, Prasad MNV (2010) Potential of Taraxacum mongolicum Hand-Mazz for accelerating phytoextraction of cadmium in combination with eco-friendly amendments. J Hazard Mater 181:480–484

    Article  CAS  Google Scholar 

  • Wei J, Li Q, Xu Z, Zhou X, Yang Y, Chen K, Lin X (2017) Mobilization effects of various organic acids on cadmium carbonate in soil (in Chinese). Chin J Environ Eng 11:5298–5306

    Google Scholar 

  • Wu W, Wu J, Liu X, Chen X, Wu Y, Yu S (2017) Inorganic phosphorus fertilizer ameliorates maize growth by reducing metal uptake, improving soil enzyme activity and microbial community structure. Ecotoxicol Environ Saf 143:322–329

    Article  CAS  Google Scholar 

  • Yan W, Zhongqiang W, Xinyu Z, Hao Y, Xiyu L, Wenjing L (2017) Enzyme activities and microbial communities in subtropical forest soil aggregates to ammonium and nitrate-nitrogen additions. J Resour Ecol 8(3):258–267

    Google Scholar 

  • Yang B, Wang M, Wang J, Song X, Wang Y, Xu H, Bai J (2018a) Mechanism of high contaminant removal performance in the expanded granular sludge blanket (EGSB) reactor involved with granular activated carbon for low-strength wastewater treatment. Chem Eng J 334:1176–1185

    Article  CAS  Google Scholar 

  • Yang P, Zhou X-F, Wang L-L, Li Q-S, Zhou T, Chen Y-K, Zhao Z-Y, He B-Y (2018b) Effect of phosphate-solubilizing bacteria on the mobility of insoluble cadmium and metabolic analysis. Int J Environ Res Public Health 15:1330

    Article  Google Scholar 

  • Yang Y, Xiong J, Tao L, Cao Z, Tang W, Zhang J, Yu X, Fu G, Zhang X, Lu Y (2020) Regulatory mechanisms of nitrogen (N) on cadmium (Cd) uptake and accumulation in plants: a review. Sci Total Environ 708:135186

    Article  CAS  Google Scholar 

  • Zeng J, Liu X, Song L, Lin X, Zhang H, Shen C, Chu H (2016) Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition. Soil Biol Biochem 92:41–49

    Article  CAS  Google Scholar 

  • Zhu S, Vivanco JM, Manter DK (2016) Nitrogen fertilizer rate affects root exudation, the rhizosphere microbiome and nitrogen-use-efficiency of maize. Appl Soil Ecol 107:324–333

    Article  Google Scholar 

  • Zhu X, Yan Y, Liu M et al (2018) Effects of different nitrogen form ratios on growth and total organic acids in Lactuca sativa L (in Chinese). Chin J Trop Crops 39(7):1324–1331

    Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (No. 41977265) and the Key Project of National Natural Science Foundation (U1901212).

Author information

Authors and Affiliations

  1. Guangdong Key Laboratory of Environmental Pollution and Health, School of Environment, Jinan University, Guangzhou, 510632, China

    Jun-Feng Wang, Wan-Li Li, Qu-Sheng Li, Li-Li Wang, Tao He & Fo-Peng Wang

  2. College of Resources and Environment, Zhongkai University of Agriculture and Engineering, Guangzhou, 510225, China

    Zhi-Min Xu

Authors
  1. Jun-Feng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wan-Li Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qu-Sheng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Li-Li Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tao He
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fo-Peng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhi-Min Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

QL designed the experiment and was responsible for administration and reviewing of project; JW was responsible for editing and reviewing of the original draft; LW and ZX gave guidance during the experiment; JW, WL, TH, and FW measured relevant indicators in this study.

Corresponding author

Correspondence to Qu-Sheng Li.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Kitae Baek

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, JF., Li, WL., Li, QS. et al. Nitrogen fertilizer management affects remobilization of the immobilized cadmium in soil and its accumulation in crop tissues. Environ Sci Pollut Res 28, 31640–31652 (2021). https://doi.org/10.1007/s11356-021-12868-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-12868-z

Keywords

Search

Navigation