Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Physiological responses of Morus alba L. in heavy metal(loid)–contaminated soil and its associated improvement of the microbial diversity

Abstract

Woody plants have considerable application potential in the phytoremediation schemes, owing to their long-lived large biomass and prosperous root systems in heavy metal(loid)–contaminated soil. Under greenhouse conditions, the physiological response characteristics and phytoremediation possibility of Morus alba L. and its associated improvement of the bacterial and arbuscular mycorrhizal fungal (AMF) diversities in heavy metal(loid) co-contaminated soils were investigated. The results showed that the cultivated M. alba L. plant exhibited significant tolerance against the heavy metal(loid)s in co-contaminated soil and that the microbial diversities were improved notably. The contents of malondialdehyde (MDA) in M. alba L. leaves decreased with cultivation from 90 to 270 days, while the superoxide dismutase, peroxidase and catalase activities were maintained at normal levels to eliminate the production of lipid peroxides. The chemical compositions (e.g. amino acids, carbohydrates and proteins) in the root of M. alba L. fluctuated slightly throughout the cultivation period. Meanwhile, Cd, Pb and Zn were majorly concentrated in the M. alba L. roots, and the maximum contents were 23.4, 7.40 and 615.5 mg/kg, respectively. According to the polymerase chain reaction–denaturing gradient gel electrophoresis (PCR-DGGE) analysis results, the influence of M. alba L. on the rhizosphere AMF community was greater than that on the bacteria community. Meanwhile, the bacterial and AMF Shannon diversity indexes in the contaminated soil were enhanced by 18.7–22.0% and 7.14–16.4%, respectively, with the presence of M. alba L. Furthermore, the correlations between the availability of As, Cd, Pb, and Zn and Shannon diversity indexes of the bacterial and AMF communities were significantly (p < 0.05) positive with the phytoremediation of M. alba L. Therefore, M. alba L. can be suggested as a potential plant candidate for ecological remediation and for simultaneously improving the activity and diversity of microorganisms in contaminated soils.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Abbreviations

Cd:

Cadmium

Zn:

Zinc

Pb:

Lead

As:

Arsenic

MDA:

Malondialdehyde

SOD:

Superoxide dismutase

POD:

Peroxidase

CAT:

Catalase

FTIR:

Fourier transform infrared

BF:

Bioaccumulation factor

TF:

Transferring coefficient

PCR-DGGE:

Polymerase chain reaction–denaturing gradient gel electrophoresis

AMF:

Arbuscular mycorrhizal fungi

CCA:

Canonical correlation analysis

References

  1. Antoniadis V, Levizou E, Shaheen SM, Ok YS, Sebastian A, Baum C, Prasad MNV, Wenzel WW, Rinklebe J (2017) Trace elements in the soil-plant interface: phytoavailability, translocation, and phytoremediation–A review. Earth-Sci Rev 171:621–645

  2. Bączek-Kwinta R, Juzoń K, Borek M, Antonkiewicz J (2019) Photosynthetic response of cabbage in cadmium-spiked soil. Photosynthetica 57(3):731–739

  3. Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256(1):67–83

  4. Chang FC, Ko CH, Tsai MJ, Wang YN, Chung CY (2014) Phytoremediation of heavy metal contaminated soil by Jatropha curcas. Ecotoxicology 10(23):1969–1978

  5. Chen Z, Zheng Y, Ding C, Ren X, Yuan J, Sun F, Li Y (2017) Integrated metagenomics and molecular ecological network analysis of bacterial community composition during the phytoremediation of cadmium-contaminated soils by bioenergy crops. Ecotox Environ Safe 145:111–118

  6. Chen XW, Wu L, Luo N, Mo CH, Wong MH, Li H (2019) Arbuscular mycorrhizal fungi and the associated bacterial community influence the uptake of cadmium in rice. Geoderma 337:749–757

  7. Chowdhary P, Yadav A, Singh R, Chandra R, Singh DP, Raj A, Bharagava RN (2018) Stress response of Triticum aestivum L. and Brassica juncea L. against heavy metals growing at distillery and tannery wastewater contaminated site. Chemosphere 206:122–131

  8. De Oliveira VH, Tibbett M (2018) Tolerance, toxicity and transport of Cd and Zn in Populus trichocarpa. Environ Exp Bot 155:281–292

  9. Deng L, Zeng G, Fan C, Lu L, Chen X, Chen M, Wu H, He X, He Y (2015) Response of rhizosphere microbial community structure and diversity to heavy metal co-pollution in arable soil. Appl Microbiol Biotechnol 99(19):8259–8269

  10. Fan K, Hsi H, Chen C, Lee H, Hseu Z (2011) Cadmium accumulation and tolerance of mahogany (Swietenia macrophylla) seedlings for phytoextraction applications. J Environ Manag 92(10):2818–2822

  11. Garate A, Ramos I, Manzanares M, Lucena JJ (1993) Cadmium uptake and distribution in three cultivars of Lactuca sp. Bull Environ Contam Toxicol 50(5):709–716

  12. Gleń-Karolczyk K, Boligłowa E, Antonkiewicz J (2018) Organic fertilization shapes the biodiversity of fungal communities associated with potato dry rot. Appl Soil Ecol 129:43–51

  13. Hou D, Wang K, Liu T, Wang H, Lin Z, Qian J, Lu L, Tian S (2017) Unique rhizosphere micro-characteristics facilitate phytoextraction of multiple metals in soil by the hyperaccumulating plant Sedum alfredii. Environ Sci Technol 51:5675–5684

  14. Jiang Y, Jiang S, Li Z, Yan X, Qin Z, Huang R (2019) Field scale remediation of Cd and Pb contaminated paddy soil using three mulberry (Morus alba L.) cultivars. Ecol Eng 129:38–44

  15. Kumar A, Majeti NVP (2014) Proteomic responses to lead-induced oxidative stress in Talinum triangulare Jacq. (Willd.) roots: identification of key biomarkers related to glutathione metabolisms. Environ Sci Pollut Res 21(14):8750–8764

  16. Leung H, Wang Z, Ye Z, Yung K, Peng X, Cheung K (2013) Interactions between arbuscular mycorrhizae and plants in phytoremediation of metal-contaminated soils: A review. Pedosphere 23(5):549–563

  17. Liang Y, Wang X, Guo Z, Xiao X, Peng C, Yang J, Zhou C, Zeng P (2019a) Chelator-assisted phytoextraction of arsenic, cadmium and lead by Pteris vittata L. and soil microbial community structure response. Int J Phytoremed 21(10):1032–1040

  18. Liang Y, Zhou C, Guo Z, Huang Z, Peng C, Zeng P, Xiao X, Xian Z (2019b) Removal of cadmium, lead, and zinc from multi-metal–contaminated soil using chelate-assisted Sedum alfredii Hance. Environ Sci Pollut Res 26:28319–28327. https://doi.org/10.1007/s11356-019-06041-w

  19. Liu C, Lin H, Dong Y, Li B, Liu Y (2018) Investigation on microbial community in remediation of lead-contaminated soil by Trifolium repens L. Ecotox Environ Safe 165:52–60

  20. Lu RK (1999) Analytical methods of soil agricultural chemistry (in Chinese). China Agricultural Science and Technology Press, Beijing

  21. Luo Z, He J, Polle A, Rennenberg H (2016) Heavy metal accumulation and signal transduction in herbaceous and woody plants: paving the way for enhancing phytoremediation efficiency. Biotechnol Adv 34(6):1131–1148

  22. Luo Y, Wu Y, Wang H, Xing R, Zheng Z, Qiu J, Yang L (2018) Bacterial community structure and diversity responses to the direct revegetation of an artisanal zinc smelting slag after 5 years. Environ Sci Pollut Res 25(15):14773–14788

  23. Marmiroli M, Pietrini F, Maestri E, Zacchini M, Marmiroli N, Massacci A (2011) Growth, physiological and molecular traits in Salicaceae trees investigated for phytoremediation of heavy metals and organics. Tree Physiol 31(12):1319–1334

  24. Mleczek M, Gąsecka M, Waliszewska B, Magdziak Z, Szostek M, Rutkowski P, Kaniuczak J, Zborowska M, Budzyńska S, Mleczek P, Niedzielski P (2018) Salix viminalis L.–a highly effective plant in phytoextraction of elements. Chemosphere 212:67–78

  25. Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164(5):601–610

  26. Pérez-de-Mora A, Burgos P, Madejón E, Cabrera F, Jaeckel P, Schloter M (2006) Microbial community structure and function in a soil contaminated by heavy metals: effects of plant growth and different amendments. Soil Biol Biochem 38:327–341

  27. Pilipović A, Zalesny RS, Rončević S, Nikolić N, Orlović S, Beljin J, Katanić M (2019) Growth, physiology, and phytoextraction potential of poplar and willow established in soils amended with heavy-metal contaminated, dredged river sediments. J Environ Manag 239:352–365

  28. Pulford I, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees–a review. Environ Int 29(4):529–540

  29. Rahoui S, Chaoui A, El Ferjani E (2010) Membrane damage and solute leakage from germinating pea seed under cadmium stress. J Hazard Mater 178(1-3):1128–1131

  30. Rahoui S, Chaoui A, Ben C, Rickauer M, Gentzbittel L, El Ferjani E (2015) Effect of cadmium pollution on mobilization of embryo reserves in seedlings of six contrasted Medicago truncatula lines. Phytochemistry 111:98–106

  31. Ran H, Guo Z, Shi L, Feng W, Xiao X, Peng C, Xue Q (2019) Effects of mixed amendments on the phytoavailability of Cd in contaminated paddy soil under a rice-rape rotation system. Environ Sci Pollut Res 26(14):14128–14136

  32. Renella G, Mench M, van der Lelie D, Pietramellara G, Ascher J, Ceccherini MT, Landi L, Nannipieri P (2004) Hydrolase activity, microbial biomass and community structure in long-term Cd-contaminated soils. Soil Biol Biochem 36(3):443–451

  33. Salam MMA, Kaipiainen E, Mohsin M, Villa A, Kuittinen S, Pulkkinen P, Pelkonen P, Mehtätalo L, Pappinen A (2016) Effects of contaminated soil on the growth performance of young Salix (Salix schwerinii E. L. Wolf) and the potential for phytoremediation of heavy metals. J Environ Manag 183:467–477

  34. Sarwar N, Imran M, Shaheen MR, Ishaque W, Kamran MA, Matloob A, Rehim A, Hussain S (2017) Phytoremediation strategies for soils contaminated with heavy metals: modifications and future perspectives. Chemosphere 171:710–721

  35. Shukla OP, Juwarkar AA, Singh SK, Khan S, Rai UN (2011) Growth responses and metal accumulation capabilities of woody plants during the phytoremediation of tannery sludge. Waste Manag 31:115–123

  36. Singh J, Lee B (2016) Influence of nano-TiO2 particles on the bioaccumulation of Cd in soybean plants (Glycine max): a possible mechanism for the removal of Cd from the contaminated soil. J Environ Manag 170:88–96

  37. Tauqeer HM, Ali S, Rizwan M, Ali Q, Saeed R, Iftikhar U, Ahmad R, Farid M, Abbasi GH (2016) Phytoremediation of heavy metals by Alternanthera bettzickiana: growth and physiological response. Ecotox Environ Safe 126:138–146

  38. Tong J, Miaowen C, Juhui J, Jinxian L, Baofeng C (2017) Endophytic fungi and soil microbial community characteristics over different years of phytoremediation in a copper tailings dam of Shanxi, China. Sci Total Environ 574:881–888

  39. Unterbrunner R, Puschenreiter M, Sommer P, Wieshammer G, Tlusto P, Zupan M, Wenzel WW (2007) Heavy metal accumulation in trees growing on contaminated sites in Central Europe. Environ Pollut 148:107–114

  40. Wan X, Lei M, Chen T, Tan Y, Yang J (2017) Safe utilization of heavy-metal-contaminated farmland by mulberry tree cultivation and silk production. Sci Total Environ 599–600:1867–1873

  41. Wang K, Huang H, Zhu Z, Li T, He Z, Yang X, Alva A (2013) Phytoextraction of metals and rhizoremediation of PAHs in co-contaminated soil by co-planting of Sedum alfredii with ryegrass (Lolium Perenne) or castor (Ricinus communis). Int J Phytoremediation 15(3):283–298

  42. Wang L, Ji B, Hu Y, Liu R, Sun W (2017) A review on in situ phytoremediation of mine tailings. Chemosphere 184:594–600

  43. Wang J, Ye S, Xue S, Hartley W, Wu H, Shi L (2018) The physiological response of Mirabilis jalapa Linn. to lead stress and accumulation. Int Biodeterior Biodegradation 128:11–14

  44. Wu Q, Wang XF, Li Y, Zhao HB, Peng S (2014) Response of rhizosphere bacterial diversity to phytoremediation of Ni contaminated sediments. Ecol Eng 73:311–318

  45. Xin L, Guo Z, Xiao X, Peng C, Zeng P, Feng W, Xu W (2019) Feasibility of anaerobic digestion on the release of biogas and heavy metals from rice straw pretreated with sodium hydroxide. Environ Sci Pollut Res 26(19):19434–19444

  46. Xu ZY, Tang M, Chen H, Ban YH, Zhang HH (2012) Microbial community structure in the rhizosphere of Sophora viciifolia grown at a lead and zinc mine of northwest China. Sci Total Environ 435-436:453–464

  47. Xu X, Yang B, Qin G, Wang H, Zhu Y, Zhang K, Yang H (2019) Growth, accumulation, and antioxidative responses of two Salix genotypes exposed to cadmium and lead in hydroponic culture. Environ Sci Pollut Res 26(19):19770–19784

  48. Yang Y, Liang Y, Ghosh A, Song Y, Chen H, Tang M (2015a) Assessment of arbuscular mycorrhizal fungi status and heavy metal accumulation characteristics of tree species in a lead–zinc mine area: potential applications for phytoremediation. Environ Sci Pollut Res 22(17):13179–13193

  49. Yang Z, Liu L, Chai L, Liao Y, Yao W, Xiao R (2015b) Arsenic immobilization in the contaminated soil using poorly crystalline Fe-oxyhydroxy sulfate. Environ Sci Pollut Res 22(16):12624–12632

  50. Yang LP, Zhu J, Wang P, Zeng J, Tan R, Yang YZ, Liu ZM (2018) Effect of Cd on growth, physiological response, Cd subcellular distribution and chemical forms of Koelreuteria paniculata. Ecotox Environ Safe 160:10–18

  51. Yu S, Sheng L, Zhang C, Deng H (2018) Physiological response of Arundo donax to cadmium stress by Fourier transform infrared spectroscopy. Spectrochim Acta A Mol Biomol Spectrosc 198:88–91

  52. Zeng P, Guo Z, Cao X, Xiao X, Liu Y, Shi L (2018a) Phytostabilization potential of ornamental plants grown in soil contaminated with cadmium. Int J Phytoremediation 20(4):311–320

  53. Zeng P, Guo Z, Xiao X, Cao X, Peng C (2018b) Response to cadmium and phytostabilization potential of Platycladus orientalis in contaminated soil. Int J Phytoremediation 20(13):1337–1345

  54. Zeng P, Guo Z, Xiao X, Peng C, Feng W, Xin L, Xu Z (2019a) Phytoextraction potential of Pteris vittata L. co-planted with woody species for As, Cd, Pb and Zn in contaminated soil. Sci Total Environ 650:594–603

  55. Zeng P, Guo Z, Xiao X, Peng C, Huang B, Feng W (2019b) Complementarity of co-planting a hyperaccumulator with three metal(loid)-tolerant species for metal(loid)-contaminated soil remediation. Ecotox Environ Safe 169:306–315

  56. Zeng P, Guo Z, Xiao X, Peng C (2019c) Effects of tree-herb co-planting on the bacterial community composition and the relationship between specific microorganisms and enzymatic activities in metal(loid)-contaminated soil. Chemosphere 220:237–248

  57. Zeng P, Guo Z, Xiao X, Peng C (2019d) Dynamic response of enzymatic activity and microbial community structure in metal(loid)-contaminated soil with tree-herb intercropping. Geoderma 345:5–16

  58. Zeng P, Guo Z, Xiao X, Peng C, Liu L, Yan D, He Y (2019e) Physiological stress responses, mineral element uptake and phytoremediation potential of Morus alba L. in cadmium-contaminated soil. Ecotoxicol Environ Safe:109973. https://doi.org/10.1016/j.ecoenv.2019.109973

  59. Zhang L, Ding X, Chen S, He X, Zhang F, Feng G (2014) Reducing carbon: Phosphorus ratio can enhance microbial phytin mineralization and lessen competition with maize for phosphorus. J Plant Interact 9(1):850–856

  60. Zhang X, Li M, Yang H, Li X, Cui Z (2018) Physiological responses of Suaeda glauca and Arabidopsis thaliana in phytoremediation of heavy metals. J Environ Manag 223:132–139

  61. Zhao S, Shang X, Duo L (2013) Accumulation and spatial distribution of Cd, Cr, and Pb in mulberry from municipal solid waste compost following application of EDTA and (NH4)2SO4. Environ Sci Pollut Res 20(2):967–975

  62. Zhao X, Huang J, Lu J, Sun Y (2019) Study on the influence of soil microbial community on the long-term heavy metal pollution of different land use types and depth layers in mine. Ecotox Environ Safe 170:218–226

  63. Zhou L, Zhao Y, Wang S, Han S, Liu J (2015) Lead in the soil-mulberry (Morus alba L.)-silkworm (Bombyx mori) food chain: translocation and detoxification. Chemosphere 128:171–177

Download references

Funding

This study received financial support from the National Key R&D Program of China (2018YFC1800400) and the National Natural Science Foundation of China (41271330, 21577176).

Author information

Correspondence to Zhaohui Guo.

Additional information

Publisher’s note

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

Responsible editor: Gangrong Shi

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zeng, P., Huang, F., Guo, Z. et al. Physiological responses of Morus alba L. in heavy metal(loid)–contaminated soil and its associated improvement of the microbial diversity. Environ Sci Pollut Res 27, 4294–4308 (2020). https://doi.org/10.1007/s11356-019-07124-4

Download citation

Keywords

  • Morus alba L.
  • Heavy metal(loid)s
  • Physiological responses
  • Phytoremediation
  • Soil microbial diversity