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Phytoremediation of triphenylmethane dyes by overexpressing a Citrobacter sp. triphenylmethane reductase in transgenic Arabidopsis

  • Environmental biotechnology
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Abstract

Triphenylmethane dyes are extensively utilized in textile industries, medicinal products, biological stains, and food processing industries, etc. They are generally considered as xenobiotic compounds, which are very recalcitrant to biodegradation. The widespread persistence of such compounds has generated concerns with regard to remediation of them because of their potential carcinogenicity, teratogenicity, and mutagenicity. In this study, we present a system of phytoremediation by Arabidopsis plants developed on the basis of overexpression of triphenylmethane reductase (TMR) from the Citrobacter sp. The morphology and growth of TMR transgenic Arabidopsis plants showed significantly enhanced tolerances to crystal violet (CV) and malachite green (MG). Further, HPLC and HPLC–MS analyses of samples before and after dye decolorization in culture media revealed that TMR transgenic plants exhibited strikingly higher capabilities of removing CV from their media and high efficiencies of converting CV to non-toxic leucocrystal violet (LCV). This work indicates that microbial degradative gene may be transgenically exploited in plants for bioremediation of triphenylmethane dyes in the environment.

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References

  • Aksu Z (2005) Application of biosorption for the removal of organic pollutants: a review. Process Biochem 40:997–1026

    Article  CAS  Google Scholar 

  • Alhassani HA, Rauf MA, Ashraf SS (2007) Efficient microbial degradation of Toluidine Blue dye by Brevibacillus sp. Dyes Pigments 75:395–400

    Article  CAS  Google Scholar 

  • Ayed L, Chaieb K, Cheref A, Bakhrouf A (2009) Biodegradation of triphenylmethane dye malachite green by Sphingomonas paucimobilis. World J Microbiol Biotechnol 25:705–711

    Article  CAS  Google Scholar 

  • Azmi W, Sani RK, Banerjee UC (1998) Biodegradation of triphenylmethane dyes. Enzyme Microb Technol 22:185–191

    Article  CAS  Google Scholar 

  • Banat IM, Nigam P, Singh D, Marchant R (1996) Microbial decolorization of textile-dye-containing effluents: a review. Bioresour Technol 58:217–227

    Article  CAS  Google Scholar 

  • Baxi NN, Shah AK (2007) The use of solid waste of a nylon-6 plant as a nutrient for bacterial decolourisation of dyes. World J Microbiol Biotechnol 23:1321–1326

    Article  CAS  Google Scholar 

  • Bumpus JA, Brock BJ (1988) Biodegradation of crystal violet by the white rot fungus Phanerochaete chrysosporium. Appl Environ Microbiol 54:1143–1150

    CAS  Google Scholar 

  • Cha CJ, Doerge DR, Cerniglia CE (2001) Biotransformation of malachite green by the fungus Cunninghamella elegans. Appl Environ Microbiol 67:4358–4360

    Article  CAS  Google Scholar 

  • Chander M, Arora DS (2007) Evaluation of some white-rot fungi for their potential to decolourise industrial dyes. Dyes Pigments 72:192–198

    Article  CAS  Google Scholar 

  • Culp SJ, Beland FA (1996) Malachite green: a toxicological review. Int J Toxicol 15:219–238

    Article  Google Scholar 

  • Daneshvar N, Ayazloo M, Khataee AR, Pourhassan M (2007) Biological decolorization of dye solution containing malachite green by microalgae Cosmarium sp. Biores Technol 98:1176–1182

    Article  CAS  Google Scholar 

  • Eichlerová I, Homolka L, Nerud F (2006) Ability of industrial dyes decolorization and ligninolytic enzymes production by different Pleurotus species with special attention on Pleurotus calyptratus, strain CCBAS 461. Process Biochem 39:855–859

    Google Scholar 

  • Gandia-Herrero F, Lorenz A, Larson T, Graham IA, Bowles DJ, Rylott EL, Bruce NC (2008) Detoxfication of the explosive 2,4,6-trinitrotoluene in Arabidopsis: discovery of bifunctional O- and C-glucosyltransferases. Plant J 56:963–974

    Article  CAS  Google Scholar 

  • Gregory P (1993) Dyes and dyes intermediates. In: Kroschwitz JI (ed) Encyclopedia of chemical technology. Wiley, New York, pp 544–545

    Google Scholar 

  • Hajdukiewicz P, Svab Z, Maliga P (1994) The small versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol Biol 25:989–994

    Article  CAS  Google Scholar 

  • Jadhav JP, Govindwar SP (2006) Biotransformation of malachite green by Saccharomyces cerevisiae MTCC 463. Yeast 23:315–323

    Article  CAS  Google Scholar 

  • Jang MS, Lee YM, Kim CH, Lee JH, Kang DW, Kim SJ, Lee YC (2005) Triphenylmethane reductase from Citrobacter sp. strain KCTC 18061P: purification, characterization, gene cloning, and overexpression of a functional protein in Escherichia coli. Appl Environ Microbiol 71:7955–7960

    Article  CAS  Google Scholar 

  • Kim MH, Kim YJ, Park HJ, Lee JS, Kwak SN, Jung WH, Lee SG, Kim D, Lee YC, Oh TK (2008) Structural insight into bioremediation of triphenylmethane dyes by Citrobacter sp. triphenylmethane reductase. J Biol Chem 283:31981–31990

    Article  CAS  Google Scholar 

  • Littlefield NA, Blackwell BN, Hewitt CC, Gaylor DW (1985) Chronic toxicity and carcinogenicity studies of Gentian violet in mice. Fund Appl Toxicol 5:902–912

    Article  CAS  Google Scholar 

  • Liu W, Chao Y, Yang X, Bao H, Qian Sh (2004) Biodecolorization of azo, anthraquinonic and triphenylmethane dyes by white-rot fungi and a laccase-secreting engineered strain. J Ind Microbiol Biotechnol 31:127–132

    Article  CAS  Google Scholar 

  • Macek T, Macková M, Káš J (2000) Exploitation of plants for the removal of organics in environmental remediation. Biotechnol Adv 18(1):23–34

    Article  CAS  Google Scholar 

  • Manal MA, El-Naggar S, El-Aasar A, Khlood IB (2005) Bioremediation of crystal violet using Hubble bioreactor packed with Pseudomonas aeruginosa. Water Res 39:5045–5054

    Article  CAS  Google Scholar 

  • Misra S, Gedamu L (1989) Heavy-metal tolerant transgenic Brassica napus L. and Nicotiana tabacum L. plants. Theor Appl Genet 78:161–168

    Article  CAS  Google Scholar 

  • Murashige SF (1962) A revised medium for rapid growth and bioassays with tobacco cultures. Plant Physiol 5:473–497

    Google Scholar 

  • Murray EE, Lotzer J, Eberle M (1989) Codon usage in plant genes. Nucleic Acids Res 17:477–498

    Article  CAS  Google Scholar 

  • Nelson CR, Hites RA (1982) Aromatic amines in and near the Buffalo River. Environ Sci Technol 14:1147–1149

    Article  Google Scholar 

  • Novakova M, Mackova M, Chrastilova Z, Viktorova J, Szekeres M, Demnerova K, Macek T (2009) Cloning of the bacterial bphC gene into Nicotiana tabacum to improve the efficiency of PCB phytoremediation. Biotechnol Bioeng 102:29–37

    Article  CAS  Google Scholar 

  • Novotny C, Rawal B, Bhatt M, Patel M, Sasek V, Molitoris HP (2001) Capacity of Irpex lacteus and Pleurotus ostreatus for decolorization of chemically different dyes. J Biotechnol 89:113–122

    Article  CAS  Google Scholar 

  • Peng RH, Xiong AS, Yao QH (2006) A direct and efficient PAGE-mediated overlap extension PCR method for gene multiple-site mutagenesis. Appl Microbiol Biotechnol 73:234–240

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 1.53–1.70

    Google Scholar 

  • Sani RK, Banerjee UC (1999) Decolorization of triphenylmethane dyes and textile and dye-stuff effluent by Kurthia sp. Enz Microbiol Technol 24:433–437

    Article  CAS  Google Scholar 

  • Sharma DK, Saini HS, Singh M, Chimni SS, Chadha BS (2004) Biotreatment of simulated textile dye effluent containing malachite green by an up-flow immobilized cell bioreactor. World J Microbiol Biotechnol 20:431–434

    Article  CAS  Google Scholar 

  • Tekere M, Mswaka AY, Zvauya R, Read JS (2001) Growth, dye degradation and ligninolytic activity studies on Zimbabwean white rot fungi. Enz Microbiol Technol 28:420–426

    Article  CAS  Google Scholar 

  • Xiong AS, Yao QH, Peng RH, Duan H, Li X, Fan HQ, Cheng ZM, Li Y (2006) PCR-based accurate synthesis of long DNA sequences. Nat Protoc 1:791–797

    Article  CAS  Google Scholar 

  • Zhang X, Henriques R, Lin SS, Niu QW, Chua NH (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1:641–646

    Article  CAS  Google Scholar 

  • Zille A, Górnacka B, Rehorek A, Cavaco-Paulo A (2005) Degradation of azo dyes by Trametes villosa laccase over long periods of oxidative conditions. Appl Environ Microbiol 71:6711–6718

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Professor Nigel Halford, Rothamsted Research, United Kingdom, for critical reading of the manuscript. The research was supported by the National Natural Science Foundation of China (31071486), The Key Project Fund of the Shanghai Municipal Committee of Agriculture (No. 2009-6-4 and No. 2011-1-8), and International Scientific and Technological Cooperation (2010DFA62320).

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Authors and Affiliations

  1. Shanghai Key Laboratory of Agricultural Genetics and Breeding, Biotechnology Research Institute, Shanghai Academy of Agricultural Sciences, 2901 Beidi Road, Shanghai, People’s Republic of China

    Xiao-Yan Fu, Wei Zhao, Ai-Sheng Xiong, Yong-Sheng Tian, Bo Zhu, Ri-He Peng & Quan-Hong Yao

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  1. Xiao-Yan Fu
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  2. Wei Zhao
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  3. Ai-Sheng Xiong
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  4. Yong-Sheng Tian
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  5. Bo Zhu
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  6. Ri-He Peng
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  7. Quan-Hong Yao
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Corresponding authors

Correspondence to Ri-He Peng or Quan-Hong Yao.

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Xiao-Yan Fu and Wei Zhao contributed equally to this article.

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Fu, XY., Zhao, W., Xiong, AS. et al. Phytoremediation of triphenylmethane dyes by overexpressing a Citrobacter sp. triphenylmethane reductase in transgenic Arabidopsis . Appl Microbiol Biotechnol 97, 1799–1806 (2013). https://doi.org/10.1007/s00253-012-4106-0

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  • DOI: https://doi.org/10.1007/s00253-012-4106-0

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