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Arbuscular Mycorrhizal Fungi Induced Changes of Pb Migration and Bacterial Community in Both the Rhizosphere and Non-rhizosphere Soils of Paspalum notatum

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Abstract

Arbuscular mycorrhizal fungi (AMF) can form symbiosis with many plants and the effect of AMF on phytoremediation of heavy metal has been a hot topic. But the effects of AMF on pollutants and microbes in rhizosphere and non-rhizosphere soil are still scarce. Therefore, the effects of AMF on plant growth, Pb translocation, and bacteria community in rhizosphere and non-rhizosphere soils spiked with Pb were investigated. It was found that AMF could significantly increase the uptake of Pb by Paspalum notatum, and Pb content was about 11 to 197 times higher in the root than that in the leaves. Besides, concentration of soil exchangeable Pb was significantly reduced after plant cultivation, and application of AMF increased the reduction (the exchangeable Pb concentrations of Pb300M and Pb3000M in the rhizosphere were 26.3% and 23.6% lower than that of Pb300 and Pb3000, respectively). The reduction was generally higher in the rhizosphere soil than that in the non-rhizosphere soil. The amount of Pb uptake by plants only accounted for a small part (4.9–21.7%) of the soil decreased exchangeable Pb, irrespective of AMF application, and most of the original exchangeable Pb was transformed into stabilized forms. Although bacteria community exhibited some differences between rhizosphere and non-rhizosphere soils, PCoA analysis indicated that both AMF and Pb were stronger impact factors affecting the beta-diversity of soil bacteria community than rhizosphere. The results of this study can help to clarify the impacts of AMF on phytoremediation of heavy metal.

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Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Abdelhameed, R. E., & Metwally, R. A. (2019). Alleviation of cadmium stress by arbuscular mycorrhizal symbiosis. International Journal of Phytoremediation, 21(7), 663–671.

    Article  CAS  Google Scholar 

  • Ancona, V., Barra Caracciolo, A., Grenni, P., Di Lenola, M., Campanale, C., Calabrese, A., UricchioMascolo, V. F. G., & Massacci, A. (2017). Plant-assisted bioremediation of a historically PCB and heavy metal-contaminated area in Southern Italy. New Biotechnology, 38(Pt B), 65–73.

    Article  CAS  Google Scholar 

  • Andrade, S. A. L. D., Jorge, R. A., & Silveira, A. P. D. D. (2005). Cadmium effect on the association of jackbean (Canavalia ensiformis) and arbuscular mycorrhizal fungi. Scientia Agricola, 62(4), 389–394.

    Article  Google Scholar 

  • Chen, X., Wu, C., Tang, J., & Hu, S. (2005). Arbuscular mycorrhizae enhance metal lead uptake and growth of host plants under a sand culture experiment. Chemosphere, 60(5), 665–671.

    Article  CAS  Google Scholar 

  • Chen, Y., Jiang, Y., Huang, H., Mou, L., Ru, J., Zhao, J., & Xiao, S. (2018). Long-term and high-concentration heavy-metal contamination strongly influences the microbiome and functional genes in Yellow River sediments. Science of the Total Environment, 637, 1400–1412.

    Article  Google Scholar 

  • De Andrade, S. A., Da Silveira, A. P., Jorge, R. A., & De Abreu, M. F. (2008). Cadmium accumulation in sunflower plants influenced by arbuscular mycorrhiza. International Journal of Phytoremediation, 10(1), 1–13.

    Article  Google Scholar 

  • Deveau, A., Bonito, G., Uehling, J., Paoletti, M., Becker, M., Bindschedler, S., Hacquard, S., Herve, V., Labbe, J., Lastovetsky, O. A., Mieszkin, S., Millet, L. J., Vajna, B., Junier, P., Bonfante, P., Krom, B. P., Olsson, S., Van Elsas, J. D., & Wick, L. Y. (2018). Bacterial-fungal interactions: Ecology, mechanisms and challenges. FEMS Microbiology Review, 42(3), 335–352.

    Article  CAS  Google Scholar 

  • Entry, J., Watrud, L., & Reeves, M. (1999). Accumulation of 137Cs and 90Sr from contaminated soil by three grass species inoculated with mycorrhizal fungi. Environmental Pollution, 104(3), 449–457.

    Article  CAS  Google Scholar 

  • Feng, G. D., Yang, S. Z., Li, H. P., & Zhu, H. H. (2016). Massilia putida sp. Nov., a dimethyl disulfide-producing bacterium isolated from wolfram mine tailing. International Journal of Systematic and Evolutionary Microbiology, 66(1), 50–55.

    Article  CAS  Google Scholar 

  • Garbaye, J. (1994). Helper bacteria: A new dimension to the mycorrhizal symbiosis. New Phytologist, 128(2), 197–210.

    Article  CAS  Google Scholar 

  • Gonzalez-Guerrero, M., Oger, E., Benabdellah, K., Azcon-Aguilar, C., Lanfranco, L., & Ferrol, N. (2010). Characterization of a CuZn superoxide dismutase gene in the arbuscular mycorrhizal fungus Glomus intraradices. Current Genetics, 56(3), 265–274.

    Article  CAS  Google Scholar 

  • Hanping, X., & Wensheng, S. (2001). Resistance to and uptoke of heavy metals by Vetiveria zizanioides and Paspalum notatum from lead/zinc mine tailings. Acta Ecologica Sinica, 21(7), 1121–1129.

    Google Scholar 

  • Hao, X., Zhu, J., Rensing, C., Liu, Y., Gao, S., Chen, W., Huang, Q., & Liu, Y.-R. (2021). Recent advances in exploring the heavy metal (loid) resistant microbiome. Computational and Structural Biotechnology Journal, 19, 94–109.

    Article  CAS  Google Scholar 

  • Hinsinger, P., Bengough, A. G., Vetterlein, D., & Young, I. M. (2009). Rhizosphere: Biophysics, biogeochemistry and ecological relevance. Plant and Soil, 321(1–2), 117–152.

    Article  CAS  Google Scholar 

  • Huang, Y., Tao, S., & Chen, Y.-J. (2005). The role of arbuscular mycorrhiza on change of heavy metal speciation in rhizosphere of maize in wastewater irrigated agriculture soil. Journal of Environmental Sciences, 17(2), 276–280.

    CAS  Google Scholar 

  • Huang, G., Zhou, X., Guo, G., Ren, C., Rizwan, M. S., Islam, M. S., & Hu, H. (2020). Variations of dissolved organic matter and Cu fractions in rhizosphere soil induced by the root activities of castor bean. Chemosphere, 254, 126800.

    Article  CAS  Google Scholar 

  • Ishii, T., Narutaki, A., Sawada, K., Aikawa, J., Matsumoto, I., & Kadoya, K. (1997). Growth stimulatory substances for vesicular-arbuscular mycorrhizal fungi in Bahia grass (Paspalum notatum Flügge.) roots. Plant and Soil, 196(2), 301–304.

    Article  CAS  Google Scholar 

  • Janeeshma, E., & Puthur, J. T. (2020). Direct and indirect influence of arbuscular mycorrhizae on enhancing metal tolerance of plants. Archives of Microbiology, 202(1), 1–16.

    Article  CAS  Google Scholar 

  • Janoušková, M., Vosátka, M., Rossi, L., & Lugon-Moulin, N. (2007). Effects of arbuscular mycorrhizal inoculation on cadmium accumulation by different tobacco (Nicotiana tabacum L.) types. Applied Soil Ecology, 35(3), 502–510.

    Article  Google Scholar 

  • Krishnamoorthy, R., Kim, C. G., Subramanian, P., Kim, K. Y., Selvakumar, G., & Sa, T. M. (2015). Arbuscular mycorrhizal fungi community structure, abundance and species richness changes in soil by different levels of heavy metal and metalloid concentration. PLoS One, 10(6), e0128784.

    Article  Google Scholar 

  • Lee, G., Suonan, Z., Kim, S. H., Hwang, D. W., & Lee, K. S. (2019). Heavy metal accumulation and phytoremediation potential by transplants of the seagrass Zostera marina in the polluted bay systems. Marine Pollution Bulletin, 149, 110509.

    Article  CAS  Google Scholar 

  • Li, X., Huang, S., & McBride, M. B. (2021). Rhizosphere effect on Pb solubility and phytoavailability in Pb-Contaminated soils. Environmental Pollution, 268(Pt B), 115840.

    Article  CAS  Google Scholar 

  • Ling, N., Wang, T., & Kuzyakov, Y. (2022). Rhizosphere bacteriome structure and functions. Nature Communications, 13(1), 836.

    Article  CAS  Google Scholar 

  • Liu, X., Guo, D., Ren, C., Li, R., Du, J., Guan, W., Li, Y., & Zhang, Z. (2020). Performance of Streptomyces pactum-assisted phytoextraction of Cd and Pb: In view of soil properties, element bioavailability, and phytoextraction indices. Environmental Science and Pollution Research International, 27(35), 43514–43525.

    Article  CAS  Google Scholar 

  • Motaghian, H. R., & Hosseinpur, A. R. (2015). Rhizosphere effects on Cu availability and fractionation in sewage sludge-amended calcareous soils. Journal of Plant Nutrition and Soil Science, 178(5), 713–721.

    Article  CAS  Google Scholar 

  • Posta, K., Marschner, H., & Römheld, V. (1994). Manganese reduction in the rhizosphere of mycorrhizal and nonmycorrhizal maize. Mycorrhiza, 5(2), 119–124.

    Article  CAS  Google Scholar 

  • Qin, Y., Zhang, W., Feng, Z., Feng, G., Zhu, H., & Yao, Q. (2022). Arbuscular mycorrhizal fungus differentially regulates P mobilizing bacterial community and abundance in rhizosphere and hyphosphere. Applied Soil Ecology, 170, 104294.

    Article  Google Scholar 

  • Riaz, M., Kamran, M., Fang, Y., Wang, Q., Cao, H., Yang, G., Deng, L., Wang, Y., Zhou, Y., & Anastopoulos, I. (2021). Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: A critical review. Journal of Hazardous Materials, 402, 123919.

    Article  CAS  Google Scholar 

  • Shah, V., & Daverey, A. (2020). Phytoremediation: A multidisciplinary approach to clean up heavy metal contaminated soil. Environmental Technology & Innovation, 18, 100774.

    Article  Google Scholar 

  • Stephenson, C., & Black, C. R. (2014). One step forward, two steps back: the evolution of phytoremediation into commercial technologies. Bioscience Horizons, 7, hzu009-hzu009.

  • Subramanian, K. S., Tenshia, V., Jayalakshmi, K., & Ramachandran, V. (2009). Biochemical changes and zinc fractions in arbuscular mycorrhizal fungus (Glomus intraradices) inoculated and uninoculated soils under differential zinc fertilization. Applied Soil Ecology, 43(1), 32–39.

    Article  Google Scholar 

  • Vodnik, D., Grcman, H., Macek, I., van Elteren, J. T., & Kovacevic, M. (2008). The contribution of glomalin-related soil protein to Pb and Zn sequestration in polluted soil. Science of the Total Environment, 392(1), 130–136.

    Article  CAS  Google Scholar 

  • Wang, G., Wang, L., Ma, F., You, Y., Wang, Y., & Yang, D. (2020). Integration of earthworms and arbuscular mycorrhizal fungi into phytoremediation of cadmium-contaminated soil by Solanum nigrum L. Journal of Hazardous Materials, 389, 121873.

    Article  CAS  Google Scholar 

  • Whitfield, L., Richards, A. J., & Rimmer, D. L. (2004). Relationships between soil heavy metal concentration and mycorrhizal colonisation in Thymus polytrichus in northern England. Mycorrhiza, 14(1), 55–62.

    Article  CAS  Google Scholar 

  • Wiangkham, N., & Prapagdee, B. (2018). Potential of Napier grass with cadmium-resistant bacterial inoculation on cadmium phytoremediation and its possibility to use as biomass fuel. Chemosphere, 201, 511–518.

    Article  CAS  Google Scholar 

  • Wu, S., Zhang, X., Sun, Y., Wu, Z., Li, T., Hu, Y., Su, D., Lv, J., Li, G., Zhang, Z., Zheng, L., Zhang, J., & Chen, B. (2015). Transformation and Immobilization of chromium by arbuscular mycorrhizal fungi as revealed by SEM-EDS, TEM-EDS, and XAFS. Environmental Science and Technology, 49(24), 14036–14047.

    Article  CAS  Google Scholar 

  • Wu, S., Zhang, X., Huang, L., & Chen, B. (2019). Arbuscular mycorrhiza and plant chromium tolerance. Soil Ecology Letters, 1(3–4), 94–104.

    Article  Google Scholar 

  • Wu, C., Li, F., Yi, S., & Ge, F. (2021). Genetically engineered microbial remediation of soils co-contaminated by heavy metals and polycyclic aromatic hydrocarbons: Advances and ecological risk assessment. Journal of Environmental Management, 296, 113185.

    Article  CAS  Google Scholar 

  • Yang, C., Ho, Y. N., Inoue, C., & Chien, M. F. (2020). Long-term effectiveness of microbe-assisted arsenic phytoremediation by Pteris vittata in field trials. Science of the Total Environment, 740, 140137.

    Article  CAS  Google Scholar 

  • Yang, Y., Dong, M., Cao, Y., Wang, J., Tang, M., & Ban, Y. (2017). Comparisons of soil properties, enzyme activities and microbial communities in heavy metal contaminated bulk and rhizosphere soils of Robinia pseudoacacia L. in the Northern Foot of Qinling Mountain. Forests, 8(11), 430.

  • Zhang, X., Lin, A., Zhang, X., & Guo, L. (2012). The effects of arbuscular mycorrhizal fungi (AMF) on forms of Pb in the upland rice rhizosphere. Chinese Agricultural Science Bulletin, 28, 24–29.

    Google Scholar 

  • Zhang, L., Shi, N., Fan, J., Wang, F., George, T. S., & Feng, G. (2018). Arbuscular mycorrhizal fungi stimulate organic phosphate mobilization associated with changing bacterial community structure under field conditions. Environmental Microbiology, 20(7), 2639–2651.

    Article  CAS  Google Scholar 

  • Zheng, B. X., Bi, Q. F., Hao, X. L., Zhou, G. W., & Yang, X. R. (2017). Massilia phosphatilytica sp. Nov., a phosphate solubilizing bacteria isolated from a long-term fertilized soil. International Journal of Systematic and Evolutionary Microbiology, 67(8), 2514–2519.

    Article  CAS  Google Scholar 

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Funding

The authors received support from the Shanxi Provincial Key Research and Development Program (201903D421002), Shanxi Provincial Open List Bidding Project (20191101007), and National Natural Science Foundation of China (21806092). Miroslav Vosatka received support from the Czech Academy of Sciences within the long-term research development program RVO 67985939.

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Authors and Affiliations

  1. Institute of Resources and Environmental Engineering, Collaborative Innovation Center of High Value-Added Utilization of Coal-Related Wastes, Shanxi University, Taiyuan, 030006, China

    Zhengjun Feng, Huiping Song & Fangqin Cheng

  2. Baowu Water Technology Co., Ltd. Shanxi Branch, Taiyuan, 030006, Shanxi, China

    Huizhi Ren

  3. Shanxi Qinghuan Nengchuang Environmental Protection Technology Company Limited, Taiyuan, 030006, China

    Yan Zou

  4. Department of Mycorrhizal Symbioses, Institute of Botany, Czech Academy of Sciences, 252 43, Pruhonice, Czech Republic

    Miroslav Vosatka

  5. School of Environment and Energy, South China University of Technology, Higher Education Mega Center, Guangzhou, 510006, China

    Shaobin Huang

  6. Shanghai Acad Environm Sci, Shanghai, 200233, China

    Hainan Lu

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  1. Zhengjun Feng
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Contributions

Zhengjun Feng: conceptualization; data curation; investigation; formal analysis; writing – review & editing.

Huizhi Ren: Data curation; formal analysis; methodology; writing – original draft.

huiping Song: funding acquisition; supervision; project administration.

Yan Zou: conceptualization; project administration.

Miroslav Vosatka: writing – review & editing; supervision.

Shaobin Huang: software; writing – review & editing.

Hainan Lu: formal analysis; methodology.

Fangqin Cheng: funding acquisition; project administration; supervision.

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Correspondence to Fangqin Cheng.

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Feng, Z., Ren, H., Song, H. et al. Arbuscular Mycorrhizal Fungi Induced Changes of Pb Migration and Bacterial Community in Both the Rhizosphere and Non-rhizosphere Soils of Paspalum notatum. Water Air Soil Pollut 234, 156 (2023). https://doi.org/10.1007/s11270-023-06082-5

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