Skip to main content

Advertisement

Log in

Bamboo-based agroforestry changes phytoremediation efficiency by affecting soil properties in rhizosphere and non-rhizosphere in heavy metal-polluted soil (Cd/Zn/Cu)

  • Soils, Sec 3 • Remediation and Management of Contaminated or Degraded Lands • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Bamboo forests are usually managed to create one-story canopies suitable for agroforestry practices. The aim of this study was to investigate the remediation effects of Lei bamboo (Phyllostachys praecox) in different planting systems, pure and agroforestry, on heavy metal–contaminated (Cd/Zn/Cu) soil.

Methods

Two different cultivation systems, i.e., a pure Lei bamboo stand and bamboo-based agroforestry system, were established in the field. Soil and plant samples were collected 5 years after planting bamboo in the experimental area. The soil nutrients, root exudates, heavy metals, microbial communities in the rhizosphere and non-rhizosphere soil, and metal uptake in the harvestable parts were determined.

Results

Amounts of both Cu and Cd removed from the soil per plant in agroforestry were 1.4 times greater than those in pure forest, but there was no difference in Zn in the harvestable parts of plants from the two systems. Compared with non-rhizosphere soil, the rhizosphere soil showed lower relative polysaccharide content and hydrophobicity. The most dominant phyla of bacteria were Proteobacteria, Acidobacteria, and Actinobacteria, with average relative abundances of 30.8%, 22.3%, and 11.8%, respectively. Agroforestry significantly reduced the microbial diversity in bamboo rhizosphere but significantly increased the diversity in the non-rhizosphere, compared with pure forest. There was a strong correlation between soil organic matter (SOM) and genera. Fourier transform infrared spectroscopy and root exudate analysis showed that bamboo planting systems changed the soil functional groups and chemical composition.

Conclusion

Bamboo roots remove heavy metals from rhizosphere soil and transfer them in large quantities to the stems. Gemmata, Kaistobacter, Arthrobacter, Anaeromyxobacter, Thiobacillus, and Candidatus Solibacter were found to be related to heavy metal soil remediation by bamboo. Rhizosphere processes are important drivers of SOM decomposition and nutrient recycling, contributing to increased heavy metal removal and microbial community diversity. These findings provide insights into the soil characterization of phytoremediation using a bamboo-based agroforestry system.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Abollino O, Aceto M, Malandrino M, Mentasti E, Sarzanini C, Petrella F (2002) Heavy metals in agricultural soils from Piedmont, Italy. Distribution, speciation and chemometric data treatment. Chemosphere 49:545–557

    CAS  Google Scholar 

  • Araujo R, Gupta VV, Reith F, Bissett A, Mele P, Franco CM (2020) Biogeography and emerging significance of Actinobacteria in Australia and Northern Antarctica soils. Soil Biol Biochem 146:107805

    CAS  Google Scholar 

  • Bhardwaj D, Krishan C (2007) Bamboo based agroforestry systems in India and their future potential. Agroforestry: systems and practices 551–562

  • Bian FY, Zhong ZK, Zhang XP, Yang CB, Gai X (2020) Bamboo–an untapped plant resource for the phytoremediation of heavy metal contaminated soils. Chemosphere 246:125750

    CAS  Google Scholar 

  • Bian FY, Zhong ZK, Li CZ, Zhang XP, Gu LJ, Huang ZC, Gai X, Huang ZY (2021) Intercropping improves heavy metal phytoremediation efficiency through changing properties of rhizosphere soil in bamboo plantation. J Hazard Mater 416:125898

    CAS  Google Scholar 

  • Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59

    CAS  Google Scholar 

  • Bremner J (1960) Determination of nitrogen in soil by the Kjeldahl method. J Agric Sci 55:11–33

    CAS  Google Scholar 

  • Cai X, Jiang M, Liao J, Yang Y, Li N, Cheng Q, Li X, Song H, Luo Z, Liu S (2021) Biomass allocation strategies and Pb-enrichment characteristics of six dwarf bamboos under soil Pb stress. Ecotoxicol Environ Saf 207:111500

    CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    CAS  Google Scholar 

  • Chen J, Li S, Liang C, Xu Q, Li Y, Qin H, Fuhrmann JJ (2017) Response of microbial community structure and function to short-term biochar amendment in an intensively managed bamboo (Phyllostachys praecox) plantation soil: effect of particle size and addition rate. Sci Total Environ 574:24–33

    CAS  Google Scholar 

  • Chen L, Hu BX, Dai H, Zhang X, Xia C-A, Zhang J (2019) Characterizing microbial diversity and community composition of groundwater in a salt-freshwater transition zone. Sci Total Environ 678:574–584

    CAS  Google Scholar 

  • Chen X, Zhao Y, Zhao X, Wu J, Zhu L, Zhang X, Wei Z, Liu Y, He P (2020) Selective pressures of heavy metals on microbial community determine microbial functional roles during composting: sensitive, resistant and actor. J Hazard Mater 398:122858

    CAS  Google Scholar 

  • Dollinger J, Jose S (2018) Agroforestry for Soil Health Agrofor Syst 92:213–219

    Google Scholar 

  • Duan J, Wang L, Yang J, Yu C, Wang J, Liu ZT (2015) Chemical constituents in rhizospheric soil extracts of Pinus massoniana and Liquidambar formosana. Scientia Silvae Sinicae 51:8–15

    CAS  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    CAS  Google Scholar 

  • Elevitch CR, Mazaroli DN, Ragone D (2018) Agroforestry Standards for Regenerative Agriculture Sustainability 10:3337

    Google Scholar 

  • Emmett BD, Buckley DH, Drinkwater LE (2020) Plant growth rate and nitrogen uptake shape rhizosphere bacterial community composition and activity in an agricultural field. New Phytol 225:960–973

    CAS  Google Scholar 

  • FAO (2006) World reference base for soil resources. A framework for international classification, correlation and communication, food and agriculture organization for the United Nations, Rome

  • Gai X, Zhong Z, Zhang X, Bian F, Yang C (2021) Effects of chicken farming on soil organic carbon fractions and fungal communities in a Lei bamboo (Phyllostachys praecox) forest in subtropical China. For Ecol Manag 479:118603

    Google Scholar 

  • Gama-Rodrigues AC, Müller MW, Gama-Rodrigues EF, Mendes FAT (2021) Cacao-based agroforestry systems in the Atlantic Forest and Amazon Biomes: an ecoregional analysis of land use. Agric Sys 194:103270

    Google Scholar 

  • Gao J-J, Zhang Y, Gerhard M, Mejias-Luque R, Zhang L, Vieth M, Ma J-L, Bajbouj M, Suchanek S, Liu W-D (2018) Association between gut microbiota and Helicobacter pylori-related gastric lesions in a high-risk population of gastric cancer. Front Cell Infect Microbiol 8:202

    Google Scholar 

  • Hernández-Morcillo M, Burgess P, Mirck J, Pantera A, Plieninger T (2018) Scanning agroforestry-based solutions for climate change mitigation and adaptation in Europe. Environ Sci Policy 80:44–52

    Google Scholar 

  • Hong Y, Liao W, Yan Z, Bai Y, Feng C, Xu Z, Xu D (2020) Progress in the research of the toxicity effect mechanisms of heavy metals on freshwater organisms and their water quality criteria in China. J Chem 2020

  • Huang M, Li Z, Huang B, Luo N, Zhang Q, Zhai X, Zeng G (2018) Investigating binding characteristics of cadmium and copper to DOM derived from compost and rice straw using EEM-PARAFAC combined with two-dimensional FTIR correlation analyses. J Hazard Mater 344:539–548

    CAS  Google Scholar 

  • Kalam S, Basu A, Ahmad I, Sayyed R, El Enshasy HA, Dailin DJ, Suriani N (2020) Recent understanding of soil Acidobacteria and their ecological significance: a critical review. Front Microbiol 11:2712

    Google Scholar 

  • Kowalchuk GA, Stienstra AW, Heilig GHJ, Stephen JR, Woldendorp JW (2000) Molecular analysis of ammonia-oxidising bacteria in soil of successional grasslands of the Drentsche A (The Netherlands). FEMS Microbiol Ecol 31:207–215

    CAS  Google Scholar 

  • Latati M, Aouiche A, Tellah S, Laribi A, Benlahrech S, Kaci G, Ouarem F, Ounane SM (2017) Intercropping maize and common bean enhances microbial carbon and nitrogen availability in low phosphorus soil under Mediterranean conditions. Eur J Soil Biol 80:9–18

    CAS  Google Scholar 

  • Li B, Xu R, Sun X, Han F, Xiao E, Chen L, Qiu L, Sun W (2021a) Microbiome–environment interactions in antimony-contaminated rice paddies and the correlation of core microbiome with arsenic and antimony contamination. Chemosphere 263:128227

    CAS  Google Scholar 

  • Li J, Zhou L, Lin W (2019) Calla lily intercropping in rubber tree plantations changes the nutrient content, microbial abundance, and enzyme activity of both rhizosphere and non-rhizosphere soil and calla lily growth. Ind Crops Prod 132:344–351

    CAS  Google Scholar 

  • Li X, Yang Q, Wang L, Song C, Chen L, Zhang J, Liang Y (2021b) Using Caenorhabditis elegans to assess the ecological health risks of heavy metals in soil and sediments around Dabaoshan Mine, China. Environ Sci Pollut Res 1–14

  • Lin Y, Wang L, Li R, Hu S, Wang Y, Xue Y, Yu H, Jiao Y, Wang Y, Zhang Y (2018) How do root exudates of bok choy promote dibutyl phthalate adsorption on mollisol? Ecotoxicol Environ Saf 161:129–136

    CAS  Google Scholar 

  • Liu D, Li S, Islam E, Chen JR, Wu JS, Ye ZQ, Peng DL, Yan WB, Lu KP (2015) Lead accumulation and tolerance of moso bamboo (Phyllostachys pubescens) seedlings: applications of phytoremediation. J Zhejiang Univ Sci B 16:123–130

    CAS  Google Scholar 

  • Liu H, Xu F, Xie Y, Wang C, Zhang A, Li L, Xu H (2018) Effect of modified coconut shell biochar on availability of heavy metals and biochemical characteristics of soil in multiple heavy metals contaminated soil. Sci Total Environ 645:702–709

    CAS  Google Scholar 

  • Mansour H, Saber M, Awad F, Zaghloul A (2019) Dehydrogenase activity and zinc equivalent parameters as indicators for potential toxic elements remediation in polluted soil ecosystem. Bioremediat J 23:326–333

    CAS  Google Scholar 

  • Masella AP, Bartram AK, Truszkowski JM, Brown DG, Neufeld JD (2012) PANDAseq: paired-end assembler for illumina sequences. BMC Bioinformatics 13:31

    CAS  Google Scholar 

  • Nath AJ, Lal R, Das AK (2015) Ethnopedology and soil properties in bamboo (Bambusa sp.) based agroforestry system in North East India. Catena 135:92–99

    CAS  Google Scholar 

  • Oyedun AO, Gebreegziabher T, Hui CW (2013) Mechanism and modelling of bamboo pyrolysis. Fuel Process Technol 106:595–604

    CAS  Google Scholar 

  • Oyuela Leguizamo MA, Fernández Gómez WD, Sarmiento MCG (2017) Native herbaceous plant species with potential use in phytoremediation of heavy metals, spotlight on wetlands - a review. Chemosphere 168:1230–1247

    CAS  Google Scholar 

  • Pei P, Sun Y, Wang L, Liang X, Xu Y (2021) In-situ stabilization of Cd by sepiolite co–applied with organic amendments in contaminated soils. Ecotoxicol Environ Saf 208:111600

    CAS  Google Scholar 

  • Pei Y, Yu Z, Ji J, Khan A, Li X (2018) Microbial community structure and function indicate the severity of chromium contamination of the Yellow River. Front Microbiol 9:38

    Google Scholar 

  • Puthusseri RM, Nair HP, Johny TK, Bhat SG (2021) Insights into the response of mangrove sediment microbiomes to heavy metal pollution: Ecological risk assessment and metagenomics perspectives. J Environ Manage 298:113492

    CAS  Google Scholar 

  • Rodríguez L, Ruiz E, Alonso-Azcárate J, Rincón J (2009) Heavy metal distribution and chemical speciation in tailings and soils around a Pb–Zn mine in Spain. J Environ Manage 90:1106–1116

    Google Scholar 

  • Schmidt MW, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DA (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56

    CAS  Google Scholar 

  • Schwabe R, Dittrich C, Kadner J, Senges CHR, Bandow JE, Tischler D, Schlömann M, Levicán G, Wiche O (2021) Secondary metabolites released by the rhizosphere bacteria Arthrobacter oxydans and Kocuria rosea enhance plant availability and soil–plant transfer of germanium (Ge) and rare earth elements (REEs). Chemosphere 285:131466

    CAS  Google Scholar 

  • Smith LG, Westaway S, Mullender S, Ghaley BB, Xu Y, Lehmann LM, Pisanelli A, Russo G, Borek R, Wawer R, Borzęcka M, Sandor M, Gliga A, Smith J (2022) Assessing the multidimensional elements of sustainability in European agroforestry systems. Agric Sys 197:103357

    Google Scholar 

  • Solanki MK, Wang Z, Wang F-Y, Li C-N, Gupta CL, Singh RK, Malviya MK, Singh P, Yang L-T, Li Y-R (2020) Assessment of diazotrophic Proteobacteria in sugarcane rhizosphere when intercropped with legumes (peanut and soybean) in the field. Front Microbiol 11:1814

    Google Scholar 

  • Staton T, Breeze TD, Walters RJ, Smith J, Girling RD (2022) Productivity, biodiversity trade-offs, and farm income in an agroforestry versus an arable system. Ecol Econ 191:107214

    Google Scholar 

  • Sun D, Li K, Bi Q, Zhu J, Zhang Q, Jin C, Lu L, Lin X (2017) Effects of organic amendment on soil aggregation and microbial community composition during drying-rewetting alternation. Sci Total Environ 574:735–743

    CAS  Google Scholar 

  • Sun L, Cao X, Tan C, Deng Y, Cai R, Peng X, Bai J (2020) Analysis of the effect of cadmium stress on root exudates of Sedum plumbizincicola based on metabolomics. Ecotoxicol Environ Saf 205:111152

    CAS  Google Scholar 

  • Tang X, Zou L, Su S, Lu Y, Zhai W, Manzoor M, Liao Y, Nie J, Shi J, Ma LQ (2021) Long-term manure application changes bacterial communities in rice rhizosphere and arsenic speciation in rice grains. Environ Sci Technol 55:1555–1565

    CAS  Google Scholar 

  • Wen J, Li Z, Luo N, Huang M, Yang R, Zeng G (2018) Investigating organic matter properties affecting the binding behavior of heavy metals in the rhizosphere of wetlands. Ecotoxicol Environ Saf 162:184–191

    CAS  Google Scholar 

  • Yang B, Meng X, Singh AK, Wang P, Song L, Zakari S, Liu W (2020) Intercrops improve surface water availability in rubber-based agroforestry systems. Agr Ecosyst Environ 298:106937

    Google Scholar 

  • Yang C, Ni H, Zhong Z, Zhang X, Bian F (2019) Changes in soil carbon pools and components induced by replacing secondary evergreen broadleaf forest with Moso bamboo plantations in subtropical China. CATENA 180:309–319

    CAS  Google Scholar 

  • Zhang R, Huang Q, Yan T, Yang J, Zheng Y, Li H, Li M (2019a) Effects of intercropping mulch on the content and composition of soil dissolved organic matter in apple orchard on the loess plateau. J Environ Manage 250:109531

    CAS  Google Scholar 

  • Zhang X, Bian F, Zhong Z, Gai X, Yang C (2020) Deciphering the rhizosphere microbiome of a bamboo plant in response to different chromium contamination levels. J Hazard Mater 399:123107

    CAS  Google Scholar 

  • Zhang X, Gao G, Wu Z, Wen X, Zhong H, Zhong Z, Bian F, Gai X (2019b) Agroforestry alters the rhizosphere soil bacterial and fungal communities of moso bamboo plantations in subtropical China. Appl Soil Ecol 143:192–200

    Google Scholar 

  • Zhong B, An X, An W, Xiao X, Li H, Xia X, Zhang Q (2021) Effect of bioaugmentation on lignocellulose degradation and antibiotic resistance genes removal during biogas residues composting. Bioresour Technol 340:125742

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Talent Development Program of China National Bamboo Research Center (ZXYC202202).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zheke Zhong.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Responsible editor: Girish Choppala

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 81 KB)

Rights and permissions

Springer Nature or its licensor 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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bian, F., Zhong, Z., Zhang, X. et al. Bamboo-based agroforestry changes phytoremediation efficiency by affecting soil properties in rhizosphere and non-rhizosphere in heavy metal-polluted soil (Cd/Zn/Cu). J Soils Sediments 23, 368–378 (2023). https://doi.org/10.1007/s11368-022-03303-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-022-03303-y

Keywords

Navigation