Response of soil microbial communities to red mud-based stabilizer remediation of cadmium-contaminated farmland

  • Hui Li
  • Lemian Liu
  • Lin Luo
  • Yan Liu
  • Jianhong Wei
  • Jiachao Zhang
  • Yuan Yang
  • Anwei Chen
  • Qiming Mao
  • Yaoyu Zhou
Research Article
  • 43 Downloads

Abstract

In this work, a field test was conducted to investigate the effects of heavy metal stabilizer addition on brown rice and microbial variables in a cadmium (Cd)-contaminated farmland from April to October in 2016. Compared with the control, red mud-based stabilizer (RMDL) effectively reduced the concentration of Cd in brown rice (with the removal rate of 48.14% in early rice, 20.24 and 47.62% in late rice). The results showed that adding 0.3 kg m−2 RDML in early rice soil or soil for both early and late rice increased the microbial biomass carbon (MBC), the number of culturable heterotrophic bacteria and fungi, and the catalase activity in soil at different stages of paddy rice growth. Furthermore, there was no notable difference in the diversity of the bacterial species, community composition, and relative abundance at phylum (or class) or operational taxonomic unit (OTU) levels between the control and treatment (RMDL addition) groups. In a word, RMDL could be highly recommended as an effective remediation stabilizer for Cd-contaminated farmland, since its continuous application in paddy soil cultivating two seasons rice soil could effectively decrease the Cd content in brown rice and had no negative impact on soil microorganisms.

Keywords

Cd-contaminated farmland Brown rice Red mud Stabilizer Microbial biomass carbon Enzyme activity Microbial community 

Notes

Acknowledgements

The study was financially supported by National Natural Science Foundation of China (NSFC; Grant Nos. 51709103, 51409024, 51222805, 51408219, 51579096, 51521006, and 51508175), The Special Environmental Protection Foundation for Public Welfare Project (201509032), Project of Science and Technology of Hunan Province (2015WK3016), and Project of Science and Technology of Hunan Province (2016WK2010).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11356_2018_1409_MOESM1_ESM.docx (1.6 mb)
ESM 1 (DOCX 1616 kb)

References

  1. Araujo RP, Almeida AAF, Peeira LS, Mangabeira PAO, Souza JO, Pirovani CP, Ahnert D, Baligar VC (2017) Photosynthetic, antioxidative, molecular and ultrastructural responses of young cacao plants to Cd toxicity in the soil. Ecotoxicol Environ Saf 144:148–157.  https://doi.org/10.1016/j.ecoenv.2017.06.006 CrossRefGoogle Scholar
  2. Bian R, Li L, Bao D, Zheng J, Zhang X, Zheng J, Liu X, Cheng K, Pan G (2016) Cd immobilization in a contaminated rice paddy by inorganic stabilizers of calcium hydroxide and silicon slag and by organic stabilizer of biochar. Environ Sci Pollut Res 23(10):10028–10036.  https://doi.org/10.1007/s11356-016-6214-3 CrossRefGoogle Scholar
  3. 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(5):335–336.  https://doi.org/10.1038/nmeth.f.303 CrossRefGoogle Scholar
  4. Cappuyns V (2015) Use of red mud in soil remediation: review of applications and challenges, Proceedings of the Bauxite Residue Valorisation and Best Practices conference. Acco, 1: 81-87Google Scholar
  5. Chaney RL (2015) How does contamination of rice soils with Cd and Zn cause high incidence of human Cd disease in subsistence rice farmers. Curr Pollut Rep 1(1):13–22.  https://doi.org/10.1007/s40726-015-0002-4 CrossRefGoogle Scholar
  6. Colin VL, Villegas LB, Abate CM (2012) Indigenous microorganisms as potential bioremediators for environments contaminated with heavy metals. Int Biodeter Biodegrad 69:28–37.  https://doi.org/10.1016/j.ibiod.2011.12.001 CrossRefGoogle Scholar
  7. de Mora AP, Ortega-Calvo JJ, Cabrera F, Madejón E (2005) Changes in enzyme activities and microbial biomass after “in situ” remediation of a heavy metal-contaminated soil. Appl Soil Ecol 28(2):125–137.  https://doi.org/10.1016/j.apsoil.2004.07.006 CrossRefGoogle Scholar
  8. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072.  https://doi.org/10.1128/AEM.03006-05 CrossRefGoogle Scholar
  9. dos Santos EdC, Silva IS, Simoes TH, Simioni KC, Oliveira VM, Grossman MJ, Durrant LR (2012) Correlation of soil microbial community responses to contamination with crude oil with and without chromium and copper. Int Biodeterior Biodegradation 70:104–110Google Scholar
  10. Du Y, Hu X-F, Wu X-H, Shu Y, Jiang Y, Yan X-J (2013) Affects of mining activities on Cd pollution to the paddy soils and rice grain in Hunan province, central South China. Environ Monit Assess 185(12):9843–9856.  https://doi.org/10.1007/s10661-013-3296-y CrossRefGoogle Scholar
  11. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998.  https://doi.org/10.1038/nmeth.2604 CrossRefGoogle Scholar
  12. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200.  https://doi.org/10.1093/bioinformatics/btr381 CrossRefGoogle Scholar
  13. Feigl V, Ujaczki É, Vaszita E, Molnár M (2017) Influence of red mud on soil microbial communities: application and comprehensive evaluation of the Biolog EcoPlate approach as a tool in soil microbiological studies. Sci Total Environ 595:903–911.  https://doi.org/10.1016/j.scitotenv.2017.03.266 CrossRefGoogle Scholar
  14. Feki-Tounsi M, Olmedo P, Gil F, Khlifi R, Mhiri MN, Rebai A, Hamza-Chaffai A (2013) Cadmium in blood of Tunisian men and risk of bladder cancer: interactions with arsenic exposure and smoking. Environ Sci Pollut Res 20:7204–7213CrossRefGoogle Scholar
  15. Feng R, Qiu W, Lian F, Yu Z, Yang Y, Song Z (2013) Field evaluation of in situ remediation of Cd-contaminated soil using four additives, two foliar fertilisers and two varieties of pakchoi. J Environ Manag 124:17–24.  https://doi.org/10.1016/j.jenvman.2013.03.037 CrossRefGoogle Scholar
  16. Feng Y, Yu Y, Tang H, Zu Q, Zhu J, Lin X (2015) The contrasting responses of soil microorganisms in two rice cultivars to elevated ground-level ozone. Environ Pollut 197:195–202.  https://doi.org/10.1016/j.envpol.2014.11.032 CrossRefGoogle Scholar
  17. Ferreira RR, Fornazier RF, Vitória AP, Lea PJ, Azevedo RA (2002) Changes in antioxidant enzyme activities in soybean under cadmium stress. J Plant Nutr 25(2):327–342.  https://doi.org/10.1081/PLN-100108839 CrossRefGoogle Scholar
  18. Fleck AT, Mattusch J, Schenk MK (2013) Silicon decreases the arsenic level in rice grain by limiting arsenite transport. J Plant Nutr Soil Sci 176:785–794Google Scholar
  19. Frieslhanl W, Platzer K, Horak O, Gerzabek MH, Baumgarten A, Steinnes E (2009) Immobilising of Cd, Pb, and Zn contaminated arable soils close to a former Pb/Zn smelter: a field study in Austria over 5 years. Environ Geochem Health 31(5):581–594.  https://doi.org/10.1007/s10653-009-9256-3 CrossRefGoogle Scholar
  20. Garau G, Castaldi P, Santona L, Deiana P, Melis P (2007) Influence of red mud, zeolite and lime on heavy metal immobilization, culturable heterotrophic microbial populations and enzyme activities in a contaminated soil. Geoderma 142:47–57CrossRefGoogle Scholar
  21. Garau G, Silvetti M, Deiana S, Deiana P, Castaldi P (2011) Long-term influence of red mud on As mobility and soil physico-chemical and microbial parameters in a polluted sub-acidic soil. J Hazard Mater 185:1241–1248CrossRefGoogle Scholar
  22. Garau G, Silvetti M, Castaldi P, Mele E, Deiana P, Deiana S (2014) Stabilising metal (loid) s in soil with iron and aluminium-based products: microbial, biochemical and plant growth impact. J Environ Manag 139:146–153.  https://doi.org/10.1016/j.jenvman.2014.02.024 CrossRefGoogle Scholar
  23. Han J, Liang X, Xu Y, Xu Y, Lei Y, Jiang R (2014) In-situ remediation of Cd-polluted paddy soil by clay minerals and their effects on nitrogen, phosphorus and enzymatic activities. Acta Sci Circumst 34:2853–2860Google Scholar
  24. Hmid A, Al Chami Z, Sillen W, De Vocht A, Vangronsveld J (2015) Olive mill waste biochar: a promising soil amendment for metal immobilization in contaminated soils. Environ Sci Pollut Res 22(2):1444–1456.  https://doi.org/10.1007/s11356-014-3467-6 CrossRefGoogle Scholar
  25. Hong C, Si Y, Xing Y, Li Y (2015) Illumina MiSeq sequencing investigation on the contrasting soil bacterial community structures in different iron mining areas. Environ Sci Pollut Res 22(14):10788–10799.  https://doi.org/10.1007/s11356-015-4186-3 CrossRefGoogle Scholar
  26. Igwe JC, Nnorom IC, Gbaruko BC (2010) Kinetics of radionuclides and heavy metals behaviour in soils: implications for plant growth. Afr J Biotechnol 4:1541–1547Google Scholar
  27. Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6:68–72CrossRefGoogle Scholar
  28. Kent M (2011) Vegetation description and data analysis: a practical approach. John Wiley & SonsGoogle Scholar
  29. Kumari D, Pan X, Lee D-J, Achal V (2014) Immobilization of cadmium in soil by microbially induced carbonate precipitation with Exiguobacterium undae at low temperature. Int Biodeterior Biodegrad 94:98–102.  https://doi.org/10.1016/j.ibiod.2014.07.007 CrossRefGoogle Scholar
  30. Lee SS, Lim JE, El-Azeem SAA, Choi B, Oh S-E, Moon DH, Ok YS (2013) Heavy metal immobilization in soil near abandoned mines using eggshell waste and rapeseed residue. Environ Sci Pollut Res 20(3):1719–1726.  https://doi.org/10.1007/s11356-012-1104-9 CrossRefGoogle Scholar
  31. Li J, Xu Y (2017) Use of clay to remediate cadmium contaminated soil under different water management regimes. Ecotoxicol Environ Saf 141:107–112.  https://doi.org/10.1016/j.ecoenv.2017.03.021 CrossRefGoogle Scholar
  32. Li B, Yang J, Wei D, Chen S, Li J, Ma Y (2014) Field evidence of cadmium phytoavailability decreased effectively by rape straw and/or red mud with zinc sulphate in a cd-contaminated calcareous soil. PLoS One 9(10):e109967.  https://doi.org/10.1371/journal.pone.0109967 CrossRefGoogle Scholar
  33. Li P, Peng X, Luan Z, Zhao T, Zhang C, Liu B (2016) Effects of red mud addition on cadmium accumulation in cole (Brassica campestris L.) under high fertilization conditions. J Soils Sediments 16(8):2097–2104.  https://doi.org/10.1007/s11368-016-1392-7 CrossRefGoogle Scholar
  34. Liang X, Han J, Xu Y, Sun Y, Wang L, Tan X (2014) In situ field-scale remediation of Cd polluted paddy soil using sepiolite and palygorskite. Geoderma 235:9–18CrossRefGoogle Scholar
  35. Lim J-M, You Y, Kamala-Kannan S, Oh S-G, Oh B-T (2014) Stabilization of metals-contaminated farmland soil using limestone and steel refining slag. J Soil Groundw Environ 19(5):1–8.  https://doi.org/10.7857/JSGE.2014.19.5.001 CrossRefGoogle Scholar
  36. Liu J, Qu P, Zhang W, Dong Y, Li L, Wang M (2014) Variations among rice cultivars in subcellular distribution of Cd: the relationship between translocation and grain accumulation. Environ Exp Bot 107:25–31.  https://doi.org/10.1016/j.envexpbot.2014.05.004 CrossRefGoogle Scholar
  37. Liu Z, Yang J, Wan X, Peng Y, Liu J, Wang X, Zeng M (2016) How red mud-induced enhancement of iron plaque formation reduces cadmium accumulation in rice with different radial oxygen loss. Pol J Environ Stud 25:1603–1613CrossRefGoogle Scholar
  38. Lombi E, Zhao F-J, Wieshammer G, Zhang G, McGrath SP (2002) In situ fixation of metals in soils using bauxite residue: biological effects. Environ Pollut 118(3):445–452.  https://doi.org/10.1016/S0269-7491(01)00295-0 CrossRefGoogle Scholar
  39. Lombi E, Hamon RE, McGrath SP, McLaughlin MJ (2003) Lability of Cd, Cu, and Zn in polluted soils treated with lime, beringite, and red mud and identification of a non-labile colloidal fraction of metals using isotopic techniques. Environ Sci Technol 37(5):979–984.  https://doi.org/10.1021/es026083w CrossRefGoogle Scholar
  40. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963.  https://doi.org/10.1093/bioinformatics/btr507 CrossRefGoogle Scholar
  41. 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(2):327–341.  https://doi.org/10.1016/j.soilbio.2005.05.010 CrossRefGoogle Scholar
  42. Pinna MV, Castaldi P, Deiana P, Pusino A, Garau G (2012) Sorption behavior of sulfamethazine on unamended and manure-amended soils and short-term impact on soil microbial community. Ecotoxicol Environ Saf 84:234–242.  https://doi.org/10.1016/j.ecoenv.2012.07.006 CrossRefGoogle Scholar
  43. Rao Z, Huang D, Zhu Q, Liu S, Luo Z, Cao X, Ren X, Wang J, Wang S (2013) Effects of amendments on the availability of Cd in contaminated paddy soil: a three-year field experiment. J Food Agr Environ 11:2009–2014Google Scholar
  44. Rizwan M, Ali S, Adrees M, Rizvi H, Rehman MZ, Hannan F, Qayyum MF, Hafeez F, Ok YS (2016) Cadmium stress in rice: toxic effects, tolerance mechanisms, and management: a critical review. Environ Sci Pollut Res 23:17859–17879CrossRefGoogle Scholar
  45. Singh BK, Quince C, Macdonald CA, Khachane A, Thomas N, Al-Soud WA, Sørensen SJ, He Z, White D, Sinclair A (2014) Loss of microbial diversity in soils is coincident with reductions in some specialized functions. Environ Microbiol 16(8):2408–2420.  https://doi.org/10.1111/1462-2920.12353 CrossRefGoogle Scholar
  46. Su JQ, Ding LJ, Xue K, Yao HY, Quensen J, Bai SJ, Wei WX, Wu JS, Zhou J, Tiedje JM (2015) Long-term balanced fertilization increases the soil microbial functional diversity in a phosphorus-limited paddy soil. Mol Ecol 24(1):136–150.  https://doi.org/10.1111/mec.13010 CrossRefGoogle Scholar
  47. Sun Y, Li Y, Xu Y, Liang X, Wang L (2015) In situ stabilization remediation of cadmium (Cd) and lead (Pb) co-contaminated paddy soil using bentonite. Appl Clay Sci 105:200–206CrossRefGoogle Scholar
  48. Sun Y, Sun G, Xu Y, Liu W, Liang X, Wang L (2016) Evaluation of the effectiveness of sepiolite, bentonite, and phosphate amendments on the stabilization remediation of cadmium-contaminated soils. J Environ Manag 166:204–210.  https://doi.org/10.1016/j.jenvman.2015.10.017 CrossRefGoogle Scholar
  49. Tang X, Li Q, Wu M, Lin L, Scholz M (2016) Review of remediation practices regarding cadmium-enriched farmland soil with particular reference to China. J Environ Manag 181:646–662.  https://doi.org/10.1016/j.jenvman.2016.08.043 CrossRefGoogle Scholar
  50. Team RC (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  51. Tripathy S, Bhattacharyya P, Mohapatra R, Som A, Chowdhury D (2014) Influence of different fractions of heavy metals on microbial ecophysiological indicators and enzyme activities in century old municipal solid waste amended soil. Ecol Eng 70:25–34CrossRefGoogle Scholar
  52. Vásquez-Murrieta M, Migueles-Garduño I, Franco-Hernández O, Govaerts B, Dendooven L (2006) C and N mineralization and microbial biomass in heavy-metal contaminated soil. Eur J Soil Biol 42:89–98CrossRefGoogle Scholar
  53. Wang Y, Björn LO (2014) Heavy metal pollution in Guangdong Province, China, and the strategies to manage the situation. Front Environ Sci 2:9CrossRefGoogle Scholar
  54. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267.  https://doi.org/10.1128/AEM.00062-07 CrossRefGoogle Scholar
  55. Wang M, Peng C, Chen W (2015) Effects of rice cultivar and typical soil improvement measures on the uptake of Cd in rice grains. Huanjing kexue 36(11):4283–4290Google Scholar
  56. Wang M, Chen W, Peng C (2016) Risk assessment of Cd polluted paddy soils in the industrial and township areas in Hunan, southern China. Chemosphere 144:346–351CrossRefGoogle Scholar
  57. Witt C, Gaunt JL, Galicia CC, Ottow JC, Neue H-U (2000) A rapid chloroform-fumigation extraction method for measuring soil microbial biomass carbon and nitrogen in flooded rice soils. Biol Fertil Soils 30(5-6):510–519.  https://doi.org/10.1007/s003740050030 CrossRefGoogle Scholar
  58. Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. Isrn Ecology 2011:2090–2110CrossRefGoogle Scholar
  59. Xie Y, Ji X, Huang J, Liu Z, Guang D, Tian F (2015) Effect of organic manure, passivator and their complex on the bioavailability of soil Cd. Meteorol Environ Res 6:48–57Google Scholar
  60. Xin N, Hao J, Lu X, Liu H, Wu X (2017) Effect of modified bentonite on Cd accumulation in different organs and growth of rice under cadmium stress. DEStech Transactions on Engineering and Technology ResearchGoogle Scholar
  61. Xu Y, Zhao D, Xu Y, Sun Y (2017) Immobilization and remediation of low-level Cd contaminated soil using bentonite. J Agric Resour Environ 34:38–46Google Scholar
  62. Yang X, Liu J, McGrouther K, Huang H, Lu K, Guo X, He L, Lin X, Che L, Ye Z (2016) Effect of biochar on the extractability of heavy metals (Cd, Cu, Pb, and Zn) and enzyme activity in soil. Environ Sci Pollut Res 23(2):974–984.  https://doi.org/10.1007/s11356-015-4233-0 CrossRefGoogle Scholar
  63. Yao A, Wang Y, Ling X, Chen Z, Tang Y, Qiu H, Ying R, Qiu R (2017) Effects of an iron-silicon material, a synthetic zeolite and an alkaline clay on vegetable uptake of As and Cd from a polluted agricultural soil and proposed remediation mechanisms. Environ Geochem Health 39(2):353–367.  https://doi.org/10.1007/s10653-016-9863-8 CrossRefGoogle Scholar
  64. Yin P, Shi L (2014) Remediation of Cd, Pb, and Cu-contaminated agricultural soil using three modified industrial by-products. Water Air Soil Pollut 225(11):2194.  https://doi.org/10.1007/s11270-014-2194-4 CrossRefGoogle Scholar
  65. Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89(6):670–679.  https://doi.org/10.1002/bit.20347 CrossRefGoogle Scholar
  66. Zhao F-J, Ma Y, Zhu Y-G, Tang Z, McGrath SP (2014) Soil contamination in China: current status and mitigation strategies. Environ Sci Technol 49:750–759CrossRefGoogle Scholar
  67. Zhou Y, Tang L, Zeng G, Zhang C, Zhang Y, Xie X (2016) Current progress in biosensors for heavy metal ions based on DNAzymes/DNA molecules functionalized nanostructures: a review. Sensors Actuators B Chem 223:280–294.  https://doi.org/10.1016/j.snb.2015.09.090 CrossRefGoogle Scholar
  68. Zhou R, Liu X, Luo L, Zhou Y, Wei J, Chen A, Tang L, Wu H, Deng Y, Zhang F (2017) Remediation of Cu, Pb, Zn and Cd-contaminated agricultural soil using a combined red mud and compost amendment. Int Biodeterior Biodegrad 118:73–81.  https://doi.org/10.1016/j.ibiod.2017.01.023 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Hui Li
    • 1
  • Lemian Liu
    • 2
  • Lin Luo
    • 1
  • Yan Liu
    • 3
  • Jianhong Wei
    • 4
  • Jiachao Zhang
    • 1
  • Yuan Yang
    • 1
  • Anwei Chen
    • 1
  • Qiming Mao
    • 1
  • Yaoyu Zhou
    • 1
  1. 1.College of Resources and EnvironmentHunan Agriculture UniversityChangshaChina
  2. 2.College of Biological Science and EngineeringFuzhou UniversityFuzhouChina
  3. 3.Hunan Modern Environment Technology Co., LTDChangshaChina
  4. 4.College of Biological Science and TechnologyHunan Agricultural UniversityChangshaChina

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