Environmental Science and Pollution Research

, Volume 26, Issue 6, pp 5564–5576 | Cite as

Occurrence, fate, and transport of potentially toxic metals (PTMs) in an alkaline rhizosphere soil-plant (Maize, Zea mays L.) system: the role of Bacillus subtilis

  • Xiaoping LiEmail author
  • Yue Cai
  • Dongying Liu
  • Yuwei Ai
  • Meng Zhang
  • Yu Gao
  • Yuchao Zhang
  • Xu Zhang
  • Xiangyang Yan
  • Bin Liu
  • Hongtao Yu
  • Howard W. Mielke
Research Article


Utilization of microbes is one of the most promising methods to remediate potentially toxic metals (PTMs) from soil. In this study, a systematic investigation was conducted to study the influence of Bacillus subtilis on PTMs occurrence, fractionation, translocation, and accumulation in the rhizosphere soil of Maize (Zea mays L.) in pot experiments. B. subtilis showed strong effects on the fate and mobility of Pb, Sb, Ni, Zn, Cu, and Cr, and it also affected PTMs’ distribution in the rhizosphere soil, maize growth, and microbial community structure. Results showed that it was easier for Zn to accumulate in maize roots than other PTMs. According to chemical fractionation, B. subtilis tended to immobilize Pb, Sb, Ni, Zn, and Cu in the rhizosphere soil. Compared with other PTMs, Cr tended to be more available and more mobile, which indicated a higher health risk to the eco-environment. These findings suggested that B. subtilis could be used as a geomicrobiological stabilizer to immobilize PTMs (Pb, Sb, Ni, Cu, Zn) in alkaline soils and decrease their uptake by plants, thus reducing the risks of a potential transfer into the food chain.


Bacillus subtilis Fate Maize (Zea mays Zhengdan 958) Potentially toxic metals (PTMs) Rhizosphere soil 


Authors’ contributions

Xiaoping Li conceived and designed the experiments. Dongying Liu performed the experiments, and Yue Cai organized and wrote the manuscript, Howard W. Mielke revised the manuscript. Yuwei Ai, Meng Zhang, Yu Gao, Yuchao Zhang, Xu Zhang, Xiangyang Yan, Bin Liu, and Hongtao Yu contributed the sampling, reagents, materials, and data analysis.

Funding information

The authors received financial support from the National Natural Science Foundation of China (41471420, 41877517), the project of International Science and Technology Innovation and Cooperation Base of Shaanxi Province (2018GHJD-16), the Natural Science Foundation of Shaanxi Province (2015JM4124), and the Fundamental Research Funds for the Central Universities (GK201701010, GK 200902024, and GK201402032).

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflict of interest.

Supplementary material

11356_2018_4031_MOESM1_ESM.docx (133 kb)
ESM 1 (DOCX 133 kb)
11356_2018_4031_MOESM2_ESM.docx (14 kb)
ESM 2 (DOCX 14.4 kb)


  1. Alagic SC, Tosic SB, Dimitrijevic MD, Antonijevic MM, Nujkic MM (2015) Assessment of the quality of polluted areas based on the content of heavy metals in different organs of the grapevine (Vitis vinifera) cv Tamjanika. Environ Sci Pollut Res Int 22(9):7155–7175Google Scholar
  2. Alford ÉR, Pilon-Smits EAH, Paschke MW (2010) Metallophytes—a view from the rhizosphere. Plant Soil 337(1–2):33–50Google Scholar
  3. Anjum SA, Tanveer M, Hussain S, Bao M, Wang L, Khan I, Ullah E, Tung SA, Samad RA, Shahzad B (2015) Cadmium toxicity in Maize (Zea mays L.): consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environ Sci Pollut Res Int 22(21):17022–17030Google Scholar
  4. Ayangbenro AS, Babalola OO (2017) A new strategy for heavy metal polluted environments: a review of microbial biosorbents. Int J Environ Res Public Health 14(1):e94.
  5. Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant-microbe interactions. Curr Opin Biotechnol 20(6):642–650Google Scholar
  6. Bahram M, Hildebrand F, Forslund SK, Anderson JL, Soudzilovskaia NA, Bodegom PM, Bengtsson-Palme J, Anslan S, Coelho LP, Harend H, Huerta-Cepas J, Medema MH, Maltz MR, Mundra S, Olsson PA, Pent M, Põlme S, Sunagawa S, Ryberg M, Tedersoo L, Bork P (2018) Structure and function of the global topsoil microbiome. Nature 560:233–237Google Scholar
  7. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57(1):233–266Google Scholar
  8. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17(8):478–486Google Scholar
  9. Beveridge TJ (1989) Role of cellular design in bacterial metal accumulation and mineralization. Annu Rev of Microbiol 43(1):147–171Google Scholar
  10. Bonanno G (2011) Trace element accumulation and distribution in the organs of Phragmites australis (common reed) and biomonitoring applications. Ecotoxicol Environ Saf 74(4):1057–1064Google Scholar
  11. Bonanno G (2013) Comparative performance of trace element bioaccumulation and biomonitoring in the plant species Typha domingensis, Phragmites australis and Arundo donax. Ecotoxicol Environ Saf 97:124–130Google Scholar
  12. Bonanno G, Lo Giudice R (2010) Heavy metal bioaccumulation by the organs of Phragmites australis (common reed) and their potential use as contamination indicators. Ecol Indic 10(3):639–645Google Scholar
  13. Burt RL, Hernandez R, Shaw R, Tunstead R, Ferguson PS (2014) Trace element concentration and speciation in selected urban soils in New York City. Environ Monit Assess 186(1):195–215Google Scholar
  14. Cai L, Xu Z, Bao P, He M, Dou L, Chen L, Zhou Y, Zhu YG (2015) Multivariate and geostatistical analyses of the spatial distribution and source of arsenic and heavy metals in the agricultural soils in Shunde, Southeast China. J Geochem Explor 148:189–195Google Scholar
  15. Çolak F, Atar N, Yazıcıoğlu D, Olgun A (2011) Biosorption of lead from aqueous solutions by Bacillus strains possessing heavy-metal resistance. Chem Eng J 173(2):422–428Google Scholar
  16. Cornu JY, Huguenot D, Jezequel K, Lollier M, Lebeau T (2017) Bioremediation of copper-contaminated soils by bacteria. World J Microbiol Biotechnol 33(2):26Google Scholar
  17. Costa ACAD (1999) Chemical interactions between mercurial species and surface biomolecules from structural components of some biological systems, in mercury contaminated sites: characterization, risk assessment and remediation. Springer, Berlin HeidelbergGoogle Scholar
  18. Cram S, Sommer I, Fernández P, Galicia L, Ríos C, Barois I (2015) Soil natural capital modification through landuse and cover change in a tropical forest landscape. J Trop For Sci 27:189–201Google Scholar
  19. Dassen SR, Cortois H, Martens M, de Hollander GA, Kowalchuk WH, van der Putten DDGB (2017) Differential responses of soil bacteria, fungi, archaea and protists to plant species richness and plant functional group identity. Mol Ecol 26(15):4085–4098Google Scholar
  20. Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-González A, Eldridge DJ, Bardgett RD, Maestre FT, Singh BK, Fierer N (2018) A global atlas of the dominant bacteria found in soil. Science 359:320–325Google Scholar
  21. Dessaux Y, Grandclément C, Faure D (2016) Engineering the rhizosphere. Trends Plant Sci 21(3):266–278Google Scholar
  22. Dhanakumar S, Solaraj G, Mohanraj R (2015) Heavy metal partitioning in sediments and bioaccumulation in commercial fish species of three major reservoirs of river Cauvery delta region, India. Ecotoxicol Environ Saf 113:145–151Google Scholar
  23. Dormeyer MR, Egelkamp MJ, Thiele E, Hammer K et al (2015) A novel engineering tool in the Bacillus subtilis toolbox: inducer-free activation of gene expression by selection-driven promoter decryptification. Microbiology 161(Pt 2):354–361Google Scholar
  24. Evangelou MWH, Kutschinski-Klöss S, Ebel M, Schaeffer A (2007) Potential of Borago officinalis, Sinapis alba L. and Phacelia boratus for Phytoextraction of Cd and Pb from soil. Water Air Soil Poll 182(1–4):407–416Google Scholar
  25. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. P Natl Acade of Sci USA 103(3), 626–631Google Scholar
  26. Foucault Y, Leveque T, Xiong T, Schreck E, Austruy A, Shahid M, Dumat C (2013) Green manure plants for remediation of soils polluted by metals and metalloids: ecotoxicity and human bioavailability assessment. Chemosphere 93(7):1430–1435Google Scholar
  27. Gadd GM (2004) Microbial influence on metal mobility and application for bioremediation. Geoderma 122(2–4):109–119Google Scholar
  28. Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156(Pt 3):609–643Google Scholar
  29. Guo Y, Du W, Wang S, Tan L (2016) The biosorption of Sr(II) on Bacillus subtilis: a combined batch and modeling study. J Mol Liq 220:762–767Google Scholar
  30. Halim M, Conte P, Piccolo A (2003) Potential availability of heavy metals to phytoextraction from contaminated soils induced by exogenous humic substances. Chemosphere 52(1):265–275Google Scholar
  31. Hiltner L (1904) Uber neuer Erfahrungen und Probleme auf dem Gebiet der Bodenbakteriologie unter besonderer. Berücksichtigung der Gründüngung und Brache 32:1405–1417Google Scholar
  32. Hofman J, Stokkaer I, Snauwaert L, Samson R (2013) Spatial distribution assessment of particulate matter in an urban street canyon using biomagnetic leaf monitoring of tree crown deposited particles. Environ Pollut 183:123–132Google Scholar
  33. 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(10):5675–5684Google Scholar
  34. Jong T, Parry DL (2004) Heavy metal speciation in solid-phase materials from a bacterial sulfate reducing bioreactor using sequential extraction procedure combined with acid volatile sulfide analysis. J Environ Monit 6(4):278–285Google Scholar
  35. Khan AS, Khan M, Khan A, Qamar Z, Waqas M (2015) The uptake and bioaccumulation of heavy metals by food plants, their effects on plants nutrients, and associated health risk: a review. Environ Sci Pollut Res Int 22(18):13772–13799Google Scholar
  36. Kısa D, Elmastaş M, Öztürk L, Kayır Ö (2016) Responses of the phenolic compounds of Zea mays under heavy metal stress. Appl Biol Chem 59(6):813–820Google Scholar
  37. Li S, Peng M, Liu Z, Shah SS (2017a) The role of soil microbes in promoting plant growth. Mol Microbiol Res.
  38. Li H, Yang Q, Fan N, Zhang M, Zhai H, Ni Z, Zhang Y (2017b) Quantitative trait locus analysis of heterosis for plant height and ear height in an elite maize hybrid zhengdan 958 by design III. BMC Genet 18:36. Google Scholar
  39. Liu L, Chen H, Cai P, Liang W, Huang Q (2009) Immobilization and phytotoxicity of Cd in contaminated soil amended with chicken manure compost. J Hazard Mater 163(2):563–567Google Scholar
  40. Lockwood CL, Stewart DI, Mortimer RJG, Mayes WM, Jarvis AP, Gruiz K, Burke IT (2015) Leaching of copper and nickel in soil-water systems contaminated by bauxite residue (red mud) from Ajka, Hungary: the importance of soil organic matter. Environ Sci Pollut R 22(14):10800–10810Google Scholar
  41. Luo Z, Wadhawan A, Bouwer EJ (2010) Sorption behavior of nine chromium (III) organic complexes in soil. Int J Environ Sci T 7(1):1–10Google Scholar
  42. Małecka M, Wójcik J, Sierota Z (2014) Chemical composition of soils on post-agricultural and forest sites before and after sawdust addition against the background of weather elements. For Res Papers 75(2):139–148Google Scholar
  43. Martínez-Sánchez MJ, García-Lorenzo ML, Pérez-Sirvent C, Bech J (2012) Trace element accumulation in plants from an aridic area affected by mining activities. J Geochem Explor 123:8–12Google Scholar
  44. Matyar F, Kaya A, Dincer S (2008) Antibacterial agents and heavy metal resistance in Gram-negative bacteria isolated from seawater, shrimp and sediment in Iskenderun Bay, Turkey. Sci Total Environ 407(1):279–285Google Scholar
  45. McCauley A, Jones C, Jacobsen J (2009) Soil pH and organic matter. Nutrient management. Montana State University Extension Service, BozemanGoogle Scholar
  46. Mustapha MU, Halimoon N (2015) Microorganisms and biosorption of heavy metals in the environment: a review paper. J Microbial Biochem Technol 07(05).
  47. Niemeyer JC, Lolata GB, de Carvalho GM, Da Silva EM, Sousa JP, Nogueira MA (2012) Microbial indicators of soil health as tools for ecological risk assessment of a metal contaminated site in Brazil. Appl Soil Ecol 59:96–105Google Scholar
  48. Oburger E, Schmidt H (2016) New methods to unravel rhizosphere processes. Trends Plant Sci 21(3):243–255Google Scholar
  49. Pagnanelli F, Esposito A, Toro L, Vegliò F (2003) Metal speciation and pH effect on Pb, Cu, Zn and Cd biosorption onto Sphaerotilus natans: Langmuir-type empirical model. Water Res 37(3):627–633Google Scholar
  50. Petr K, Bernd S, Astrid R, Ursula H, Reza K, Norbert C (2011) Citramalic acid and salicylic acid in sugar beet root exudates solubilize soil phosphorus. BMC Plant Biol 11(1):121Google Scholar
  51. Petriacq P, Williams A, Cotton A, McFarlane AE, Rolfe SA, Ton J (2017) Metabolite profiling of non-sterile rhizosphere soil. Plant J 92(1):147–162Google Scholar
  52. Phillips DP, Human LRD, Adams JB (2015) Wetland plants as indicators of heavy metal contamination. Mar Pollut Bull 92(1–2):227–232Google Scholar
  53. Pinheiro JP, Mota AM, Benedetti MF (1999) Lead and calcium binding to fulvic acids: salt effect and competition. Environ Sci Technol 33(19):3398–3404Google Scholar
  54. Rafati M, Khorasani N, Moattar F, Shirvany A, Moraghebi F, Hosseinzadeh S (2011) Phytoremediation potential of Populus alba and Morus alba for cadmium, chromuim and nickel absorption from polluted soil. Int J Environ Res 5(4):961–970Google Scholar
  55. Rai AK, Singh DP, Prabha R, Kumar M, Sharma L (2016) Microbial Inoculants: identification, characterization, and applications in the field. In: Singh DP, Singh HB, Prabha R (eds) Microbial Inoculants in Sustainable Agricultural Productivity, Vol. 1: Research Perspectives. Springer India, New Delhi, pp 103–115Google Scholar
  56. Roesch LFW, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD, Daroub SH, Camargo FAO, Farmerie WG, Triplett EW (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. Isme J 1:283–290Google Scholar
  57. Schloss PD, Handelsman J (2006) Toward a census of Bacteria in soil. PLoS Comput Biol 2(7):e92Google Scholar
  58. Shahid M, Pinelli E, Dumat C (2012) Review of Pb availability and toxicity to plants in relation with metal speciation: role of synthetic and natural organic ligands. J Hazard Mater 219-220:1–12Google Scholar
  59. Shrestha R, Fischer R, Sillanpää M (2007) Investigations on different positions of electrodes and their effects on the distribution of Cr at the water sediment interface. Int J Environ Sci Technol 4(4):413–420Google Scholar
  60. Simon E, Braun M, Vidic A, Bogyó D, Fábián I, Tóthmérész B (2011) Air pollution assessment based on elemental concentration of leaves tissue and foliage dust along an urbanization gradient in Vienna. Environ Pollut 159(5):1229–1233Google Scholar
  61. Song W, Kim M, Tripathi BM, Kim H, Adams JM (2016) Predictable communities of soil bacteria in relation to nutrient concentration and successional stage in a laboratory culture experiment. Environ Microbiol 18(6):1740–1753Google Scholar
  62. Spain AV, Isbell RF, , Probert ME (1983) Soil organic matter. In: ‘Soils—an Australian viewpoint’, pp 551–563. CSIRO, Melbourne Australia. Academic Press, London UKGoogle Scholar
  63. Thomasi SS, Fernandes RBA, Fontes RLF, Jordão CP (2014) Sequential extraction of copper, nickel, zinc, lead and cadmium from Brazilian Oxysols: metal leaching and metal distribution in soil fractions. Int J Environ Stud 72(1):41–55Google Scholar
  64. Tiquia SM, Lloyd J, Herms DA, Hoitink HAJ, Michel FC (2002) Effects of mulching and fertilization on soil nutrients, microbial activity and rhizosphere bacterial community structure determined by analysis of TRFLPs of PCR-amplified 16S rRNA genes. Appl Soil Ecol 21(1):31–48Google Scholar
  65. Van Dam NM, Bouwmeester HJ (2016) Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci 21(3):256–265Google Scholar
  66. Vijayaraghavan K, Yun YS (2008) Bacterial biosorbents and biosorption. Biotechnol Adv 26(3):266–291Google Scholar
  67. Vijayaraghavan K, Padmesh TV, Palanivelu K, Velan M (2006) Biosorption of nickel(II) ions onto Sargassum wightii: application of two-parameter and three-parameter isotherm models. J Hazard Mater 133(1):304–308Google Scholar
  68. Yao AV, Bochow H, Karimov S, Boturov U, Sanginboy S, Sharipov AK (2006) Effect of FZB 24®Bacillus subtilis as a biofertilizer on cotton yields in field tests. Arch Phytopathol Plant Prot 39(4):323–328Google Scholar
  69. You M, Huang Y, Lu J, Li C (2015) Fractionation characterizations and environmental implications of heavy metal in soil from coal mine in Huainan, China. Environ Earth Sci 75(1)Google Scholar
  70. Zeng F, Ali S, Zhang H, Ouyang Y, Qiu B, Wu F, Zhang G (2011) The influence of pH and organic matter content in paddy soil on heavy metal availability and their uptake by rice plants. Environ Pollut 159(1):84–91Google Scholar
  71. Zhang T, Zou H, Ji M, Li X, Li L, Tang T (2014) Enhanced electrokinetic remediation of lead-contaminated soil by complexing agents and approaching anodes. Environ Sci Pollut Res Int 21(4):3126–3133Google Scholar
  72. Ziegler J, Schmidt S, Chutia R, Müller J, Böttcher C, Strehmel N, Scheel D, Abel S (2016) Non-targeted profiling of semi-polar metabolites in Arabidopsis root exudates uncovers a role for coumarin secretion and lignification during the local response to phosphate limitation. J Exp Bot 67(5):1421–1432Google Scholar
  73. Zou T, Li T, Zhang X, Yu H, Luo H (2011) Lead accumulation and tolerance characteristics of Athyrium wardii (Hook.) as a potential phytostabilizer. J Hazard Mater 186(1):683–689Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Xiaoping Li
    • 1
    • 2
    Email author
  • Yue Cai
    • 1
    • 2
  • Dongying Liu
    • 1
    • 2
  • Yuwei Ai
    • 1
    • 2
  • Meng Zhang
    • 1
    • 2
  • Yu Gao
    • 1
    • 2
  • Yuchao Zhang
    • 1
    • 2
  • Xu Zhang
    • 1
    • 2
  • Xiangyang Yan
    • 2
    • 3
  • Bin Liu
    • 1
    • 2
  • Hongtao Yu
    • 2
    • 4
  • Howard W. Mielke
    • 5
  1. 1.Department of Environmental Science, School of Geography and TourismShaanxi Normal UniversityXi’anPeople’s Republic of China
  2. 2.International Joint Research Centre of Shaanxi Province for Pollutant Exposure and Eco-environmental HealthXi’anPeople’s Republic of China
  3. 3.School of Chemistry & Chemical EngineeringShaanxi Normal UniversityXi’anPeople’s Republic of China
  4. 4.School of Computer, Mathematical and Natural SciencesMorgan State UniversityBaltimoreUSA
  5. 5.Department of Pharmacology, School of MedicineTulane UniversityNew OrleansUSA

Personalised recommendations