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Improvement of cadmium phytoremediation after soil inoculation with a cadmium-resistant Micrococcus sp.

Environmental Science and Pollution Research volume 23, pages 756–764 (2016)Cite this article

Abstract

Cadmium-resistant Micrococcus sp. TISTR2221, a plant growth-promoting bacterium, has stimulatory effects on the root lengths of Zea mays L. seedlings under toxic cadmium conditions compared to uninoculated seedlings. The performance of Micrococcus sp. TISTR2221 on promoting growth and cadmium accumulation in Z. mays L. was investigated in a pot experiment. The results indicated that Micrococcus sp. TISTR2221significantly promoted the root length, shoot length, and dry biomass of Z. mays L. transplanted in both uncontaminated and cadmium-contaminated soils. Micrococcus sp. TISTR2221 significantly increased cadmium accumulation in the roots and shoots of Z. mays L. compared to uninoculated plants. At the beginning of the planting period, cadmium accumulated mainly in the shoots. With a prolonged duration of cultivation, cadmium content increased in the roots. As expected, little cadmium was found in maize grains. Soil cadmium was significantly reduced with time, and the highest percentage of cadmium removal was found in the bacterial-inoculated Z. mays L. after transplantation for 6 weeks. We conclude that Micrococcus sp. TISTR2221 is a potent bioaugmenting agent, facilitating cadmium phytoextraction in Z. mays L.

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References

  • Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181

    Article  CAS  Google Scholar 

  • Ahmad I, Akhtar MJ, Zahir ZA, Naveed M, Mitter B, Sessitsch A (2014) Cadmium-tolerant bacteria induce metal stress tolerance in cereals. Environ Sci Pollut Res 21:11054–11065

    Article  CAS  Google Scholar 

  • Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals: concepts and applications. Chemosphere 91:869–881

    Article  CAS  Google Scholar 

  • Anjum NA, Umar S, Iqbal M (2014) Assessment of cadmium accumulation, toxicity, and tolerance in Brassicaceae and Fabaceae plants: implications for phytoremediation. Environ Sci Pollut Res 21:10286–10293

    Article  CAS  Google Scholar 

  • Barocsi A, Csintalan Z, Kocsanyi L, Dushenkov S, Kuperberg JM, Kucharski R, Richter PI (2003) Optimizing phytoremediation of heavy metal-contaminated soil by exploiting plants’ stress adaptation. Int J Phytoremediation 5:13–23

    Article  CAS  Google Scholar 

  • Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plant. Braz J Plant Physiol 17:21–34

    Article  CAS  Google Scholar 

  • Chaney RL, Malik M, Lim YM, Brown SL, Brewer EP, Angle JS, Baker AJM (1997) Phytoremediation of soil metals. Curr Opin Biotechnol 8:279–284

    Article  CAS  Google Scholar 

  • Chanprasert M, Prapagdee B, Wongthanate J, Eiamphungporn W (2011) Isolation and screening of IAA-producing rhizobacteria from heavy metal contaminated areas, Proceedings in the 8th KU-KPS conference. Kasetsart University, Bangkok, pp 737–744

    Google Scholar 

  • Chen YX, He YF, Luo YM, Yu YL, Lin Q, Wong MH (2003) Physiological mechanism of plant roots exposed to cadmium. Chemosphere 50:789–793

    Article  CAS  Google Scholar 

  • Chen ZJ, Sheng XF, He LY, Huang Z, Zhang WH (2013) Effects of root inoculation with bacteria on the growth, Cd uptake and bacterial communities associated with rape grown in Cd-contaminated soil. J Hazard Mater 244–245:709–717

    Article  CAS  Google Scholar 

  • Chiu KK, Ye ZH, Wong MH (2005) Enhanced uptake of As, Zn, and Cu by Vetiveria zizanioides and Zea mays using chelating agents. Chemosphere 60:1365–1375

    Article  CAS  Google Scholar 

  • Faust MB, Christians NE (2000) Copper reduces shoot growth and root development of creeping bent grass. Crop Sci 40:498–502

    Article  CAS  Google Scholar 

  • Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374

    Article  CAS  Google Scholar 

  • Guo J, Feng R, Ding Y, Wang R (2014) Applying carbon dioxide, plant growth-promoting rhizobacterium and EDTA can enhance the phytoremediation efficiency of ryegrass in a soil polluted with zinc, arsenic, cadmium and lead. J Environ Manag 141:1–8

    Article  CAS  Google Scholar 

  • He LY, Chen ZJ, Ren GD, Zhang YF, Qian M, Sheng XF (2009) Increased cadmium and lead uptake of a cadmium hyperaccumulator tomato by cadmium-resistant bacteria. Ecotoxicol Environ Saf 72:1343–1348

    Article  CAS  Google Scholar 

  • Jeong S, Moon HS, Nam K, Kim JY, Kim TS (2012) Application of phosphate solubilizing bacteria for enhancing bioavailability and phytoextraction of cadmium (Cd) from polluted soil. Chemosphere 88:204–210

    Article  CAS  Google Scholar 

  • Jiang CY, Sheng XF, Qian M, Wang QY (2008) Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil. Chemosphere 72:157–164

    Article  CAS  Google Scholar 

  • Khaokaew S, Landrot G (2014) A field-scale study of cadmium phytoremediation in a contaminated agricultural soil at Mae Sot district, Tak province, Thailand: (1) Determination of Cd-hyperaccumulating plants. Chemosphere. doi:10.1016/j.chemosphere.2014.09.108

    Google Scholar 

  • Kumar P, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1232–1238

    Article  CAS  Google Scholar 

  • Lebeau T, Braud A, Jezequel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ Pollut 153:497–522

    Article  CAS  Google Scholar 

  • Liu DH, Jiang WS, Gao XZ (2003) Effects of cadmium on root growth, cell division and nucleoli in root tip cells of garlic. Biol Plant 47:79–83

    Article  CAS  Google Scholar 

  • Liu J, Qu W, Kadiiska MB (2009) Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol Appl Pharmacol 238:209–214

    Article  CAS  Google Scholar 

  • Liu Z, Ge H, Li C, Zhao Z, Song F, Hu S (2015) Enhanced phytoextraction of heavy metals from contaminated soil by plant co-cropping associated with PGPR. Water Air Soil Pollut 226:29

    Article  CAS  Google Scholar 

  • Ma Y, Rajkumar M, Freitas H (2009) Inoculation of plant growth promoting bacterium Achromobacter xylosoxidans strain Ax10 for the improvement of copper phytoextraction by Brassica juncea. J Environ Manag 90:831–837

    Article  Google Scholar 

  • Mattina MJI, Lannucci-Berger W, Musante C, White JC (2003) Concurrent plant uptake of heavy metals and persistent organic pollutants from soil. Environ Pollut 124:375–378

    Article  CAS  Google Scholar 

  • McGrath SP, Cunliffe CH (1985) A simplified method for the extraction of the metals Fe, Zn, Cu, Ni, Cd, Pb, Cr, Co and Mn from soils and sewage sludges. J Sci Food Agric 36:794–798

    Article  CAS  Google Scholar 

  • Meers E, Ruttens A, Hopgood M, Lesage E, Tack FMG (2005) Potential of Brassica rapa, Cannabis sativa, Helianthus annuus and Zea mays for phytoextraction of heavy metals from calcareous dredged sediment derived soils. Chemosphere 61:561–572

    Article  CAS  Google Scholar 

  • Moreira H, Marques APGC, Franco AR, Rangel AOSS, Castro PML (2014) Phytomanagement of Cd-contaminated soils using maize (Zea mays L.) assisted by plant growth-promoting rhizobacteria. Environ Sci Pollut Res 21:9742–9753

    Article  CAS  Google Scholar 

  • Murakami M, Ae N, Ishikawa S (2007) Phytoextraction of cadmium by rice (Oryza sativa L.), soybean (Glycine max (L.) Merr.), and maize (Zea mays L.). Environ Pollut 145:96–103

    Article  CAS  Google Scholar 

  • Phaenark C, Pokethitiyook P, Kruatrachue M, Ngernsansaruay C (2009) Cd and Zn accumulation in plants from the Padaeng zinc mine area. Int J Phytoremediation 11:479–495

    Article  CAS  Google Scholar 

  • Pongsakul P, Attajarusit S (1999) Assessment of heavy metal contaminations in soil. Thai J Soils Fertil 21:71–82 (in Thai)

    Google Scholar 

  • Prapagdee B, Chanprasert M, Mongkolsuk S (2013) Bioaugmentation with cadmium-resistant plant growth-promoting rhizobacteria to assist cadmium phytoextraction by Helianthus annuus. Chemosphere 92:659–666

    Article  CAS  Google Scholar 

  • Sanità di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130

    Article  Google Scholar 

  • Sheng XF, Sun LN, Huang Z, He LY, Zhang WH, Chen ZJ (2012) Promotion of growth and Cu accumulation of bio-energy crop (Zea mays) by bacteria: implications for energy plant biomass production and phytoremediation. J Environ Manag 103:58–64

    Article  CAS  Google Scholar 

  • Simmons RW, Pongsakul P, Chaney L, Saiyasitpanich D, Klinphoklap S, Nobuntou W (2003) The relative exclusion of zinc and iron from rice grain in relation to rice grain cadmium as compared to soybean: implications for human health. Plant Soil 257:163–170

    Article  CAS  Google Scholar 

  • Simmons RW, Pongsakul P, Saiyasitpanich D, Klinphoklap S (2005) Elevated levels of cadmium and zinc in paddy soils and elevated levels of cadmium in rice grain downstream of a zinc mineralized area in Thailand: implications for public health. Environ Geochem Health 27:501–511

    Article  CAS  Google Scholar 

  • Sun Y, Zhou Q, Wang L, Liu W (2009) Cadmium tolerance and accumulation characteristics of Bidens pilosa L. as a potential Cd-hyperaccumulator. J Hazard Mater 161:808–814

    Article  CAS  Google Scholar 

  • Teixeira C, Almeida MR, da Silva MN, Bordalo AA, Mucha AP (2014) Development of autochthonous microbial consortia for enhanced phytoremediation of salt-marsh sediments contaminated with cadmium. Sci Total Environ 493:757–765

    Article  CAS  Google Scholar 

  • Thawornchaisit U, Polprasert C (2009) Evaluation of phosphate fertilizers for the stabilization of cadmium in highly contaminated soils. J Hazard Mater 165:1109–1113

    Article  CAS  Google Scholar 

  • Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E, Van der Lelie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794

    Article  CAS  Google Scholar 

  • Wang M, Zou J, Duan A, Jiang W, Liu D (2007) Cadmium accumulation and its effects on metal uptake in maize (Zea mays L.). Bioresour Technol 98:82–88

    Article  CAS  Google Scholar 

  • Wang Y, Yan A, Dai J, Wang NN, Wu D (2012) Accumulation and tolerance characteristics of cadmium in Chlorophytum comosum: a popular ornamental plant and potential Cd hyperaccumulator. Environ Monit Assess 184:929–937

    Article  CAS  Google Scholar 

  • Yokota A, Khamna S, Peberdy JF, Lumyong S (2010) Indole-3-acetic acid production by Streptomyces sp. isolated from some Thai medicinal plant rhizosphere soils. Eurasia J Biosci 4:23–32

    Google Scholar 

  • Yoon J, Cao X, Zhou Q, Ma L (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368:456–464

    Article  CAS  Google Scholar 

  • Zhang S, Li T, Huang H, Zou T, Zhang X, Yu H, Zheng Z, Wang Y (2012) Cd accumulation and phytostabilization potential of dominant plants surrounding mining tailings. Environ Sci Pollut Res 19:3879–3888

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research project was supported by the grant from Thailand Research Fund and Mahidol University (grant no. RSA5780026).

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Affiliations

  1. Faculty of Environment and Resource Studies, Mahidol University, Salaya, Nakhonpathom, 73170, Thailand

    Chirawee Sangthong, Kunchaya Setkit & Benjaphorn Prapagdee

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  1. Chirawee Sangthong
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  2. Kunchaya Setkit
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  3. Benjaphorn Prapagdee
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Correspondence to Benjaphorn Prapagdee.

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Responsible editor: Elena Maestri

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Sangthong, C., Setkit, K. & Prapagdee, B. Improvement of cadmium phytoremediation after soil inoculation with a cadmium-resistant Micrococcus sp.. Environ Sci Pollut Res 23, 756–764 (2016). https://doi.org/10.1007/s11356-015-5318-5

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  • DOI: https://doi.org/10.1007/s11356-015-5318-5

Keywords

  • Cadmium
  • Phytoextraction
  • Indole-3-acetic acid
  • Micrococcus sp.
  • Zea mays L.