Bioprocess and Biosystems Engineering

, Volume 37, Issue 2, pp 217–224 | Cite as

Exploring metal effects and synergistic interactions of ferric stimulation on azo-dye decolorization by new indigenous Acinetobacter guillouiae Ax-9 and Rahnella aquatilis DX2b

  • I-Son NgEmail author
  • Fangxin Xu
  • Chiming Ye
  • Bor-Yann ChenEmail author
  • Yinghua Lu
Original Paper


The first-attempt study deciphered metal-interacting effects on dye-decolorizing capabilities of indigenous bioelectricity-generating strains, Acinetobacter guillouiae Ax-9 and Rahnella aquatilis DX2b. Most of the metallic ions were inhibitory to color removal capabilities of these strains. However, with supplementation of 5 mM ferric chloride, specific decolorization rate (SDR) of Ax-9 increased by 55.48 % compared to Fe3+-free conditions. In contrast, SDR of DX2b decreased 75.35 % due to the inhibition of ferric chloride. On the other hand, ferric citrate could stimulate SDR of DX2b for 21.5 % at same dosage. Enzymatic assay indicated that Fe reductase activity was consistent with synergistic effects of ferric chloride on Ax-9, and ferric citrate on DX2b. Protein analysis via SDS-PAGE and identification of Tandem MS/MS afterwards showed that outer membrane protein (Omp) primarily deals with decolorization as a channeling regulation. Moreover, molecular modeling and bioinformatics data also provided detailed evidences to confirm the biological significance of Omp.


Acinetobacter guillouiae Rahnella aquatilis Decolorization Metal effect Ferric synergism 



The authors are grateful to the financial support by the Fundamental Research Funds for the Central Universities (2011121017), the Chinese National Natural Science Foundation (21206141) and the Fujian Provincial Department of Science & Technology (2012I0009). The authors also sincerely appreciate the academic connection program between Xiamen University (China) and National I-Lan University (Taiwan) in this study.


  1. 1.
    Travis AS (2002) Contaminated earth and water: a legacy of the synthetic dyestuffs industry. Ambix 49:21–50Google Scholar
  2. 2.
    Kuhad RC, Sood N, Tripathi KK, Singh A, Ward OP (2004) Developments in microbial methods for the treatment of dye effluents. Adv Appl Microbiol 56:185–213CrossRefGoogle Scholar
  3. 3.
    Mu Y, Rabaey K, Rozendal RA, Yuan ZG, Keller J (2009) Decolorization of azo dyes in bioelectrochemical systems. Environ Sci Technol 43:5137–5143CrossRefGoogle Scholar
  4. 4.
    Zhang MM, Chen WM, Chen BY, Chang CT, Hsueh CC, Ding Y, Lin KL, Xu H (2010) Comparative study on characteristics of azo dye decolorization by indigenous decolorizers. Bioresour Technol 101:2651–2656CrossRefGoogle Scholar
  5. 5.
    Telke AA, Kalyani DC, Dawkar VV, Govindwar SP (2009) Influence of organic and inorganic compounds on oxidoreductive decolorization of sulfonated azo dye C.I. Reactive Orange 16. J Hazard Mater 172:298–309CrossRefGoogle Scholar
  6. 6.
    Hsueh CC, Chen BY (2007) Comparative study on reaction selectivity of azo dye decolorization by Pseudomonas luteola. J Hazard Mater 141:842–849CrossRefGoogle Scholar
  7. 7.
    Wesenberg D, Kyriakides I, Agathos SN (2003) White-rot fungi and their enzymes for the treatment of industrial dye effluents. Biotechnol Adv 22:161–187CrossRefGoogle Scholar
  8. 8.
    Mitter EK, Corso CR (2012) Acid Black 48 dye biosorption using Saccharomyces cerevisiae immobilized with treated sugarcane bagasse. Water Sci Technol 66:1431–1438CrossRefGoogle Scholar
  9. 9.
    Doshi H, Ray A, Kothari IL, Gami B (2006) Spectroscopic and scanning electron microscopy studies of bioaccumulation of pollutants by algae. Curr Microbiol 53:148–157CrossRefGoogle Scholar
  10. 10.
    Arora S, Saini HS, Singh K (2011) Biological decolorization of industrial dyes by Candida tropicalis and Bacillus firmus. Water Sci Technol 63:761–768CrossRefGoogle Scholar
  11. 11.
    Chengalroyen MD, Dabbs ER (2013) The microbial degradation of azo dyes: minireview. World J Microbiol Biotechnol 29:389–399CrossRefGoogle Scholar
  12. 12.
    Han JL, Ng IS, Wang Y, Zheng X, Chen WM, Hsueh CC, Liu SQ, Chen BY (2012) Exploring new strains of dye-decolorizing bacteria. J Biosci Bioeng 113:508–514CrossRefGoogle Scholar
  13. 13.
    Srinivasan A, Viraraghavan T (2010) Decolorization of dye wastewaters by biosorbents: a review. J Environ Manage 91:1915–1929CrossRefGoogle Scholar
  14. 14.
    Sarayu K, Sandhya S (2012) Current technologies for biological treatment of textile wastewater–a review. Appl Biochem Biotechnol 167:645–661CrossRefGoogle Scholar
  15. 15.
    Xiao X, Xu CC, Wu YM, Cai PJ, Li WW, Du DL, Yu HQ (2012) Biodecolorization of Naphthol Green B dye by Shewanella oneidensis MR-1 under anaerobic conditions. Bioresour Technol 110:86–90CrossRefGoogle Scholar
  16. 16.
    Qu Y, Cao X, Ma Q, Shi S, Tan L, Li X, Zhou H, Zhang X, Zhou J (2012) Aerobic decolorization and degradation of Acid Red B by a newly isolated Pichia sp. TCL. J Hazard Mater 223–224:31–38CrossRefGoogle Scholar
  17. 17.
    Dawkar VV, Jadhav UU, Ghodake GS, Govindwar SP (2009) Effect of inducers on the decolorization and biodegradation of textile azo dye Navy blue 2GL by Bacillus sp. VUS. Biodegradation 20:777–787CrossRefGoogle Scholar
  18. 18.
    Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201CrossRefGoogle Scholar
  19. 19.
    Hsueh CC, Chen BY (2008) Exploring effects of chemical structure on azo dye decolorization characteristics by Pseudomonas luteola. J Hazard Mater 154:703–710CrossRefGoogle Scholar
  20. 20.
    Hsueh CC, Chen BY, Yen CY (2009) Understanding effects of chemical structure on azo dye decolorization characteristics by Aeromonas hydrophila. J Hazard Mater 167:995–1001CrossRefGoogle Scholar
  21. 21.
    Xu M, Guo J, Sun G (2007) Biodegradation of textile azo dye by Shewanella decolorationis S12 under microaerophilic conditions. Appl Microbiol Biotechnol 76:719–726CrossRefGoogle Scholar
  22. 22.
    Chen CH, Chang CF, Liu SM (2010) Partial degradation mechanisms of malachite green and methyl violet B by Shewanella decolorationis NTOU1 under anaerobic conditions. J Hazard Mater 177:281–289CrossRefGoogle Scholar
  23. 23.
    Cai PJ, Xiao X, He YR, Li WW, Chu J, Wu C, He MX, Zhang Z, Sheng GP, Lam MH, Xu F, Yu HQ (2011) Anaerobic biodecolorization mechanism of methyl orange by Shewanella oneidensis MR-1. Appl Microbiol Biotechnol 93:1769–1776CrossRefGoogle Scholar
  24. 24.
    Telke AA, Joshi SM, Jadhav SU, Tamboli DP, Govindwar SP (2010) Decolorization and detoxification of Congo red and textile industry effluent by an isolated bacterium Pseudomonas sp. SU-EBT. Biodegradation 21:283–296CrossRefGoogle Scholar
  25. 25.
    Kim JS, Ahn T, Yim SK, Yun CH (2002) Differential effect of copper (II) on the cytochrome P450 enzymes and NADPH-cytochrome P450 reductase: inhibition of cytochrome P450-catalyzed reactions by copper (II) ion. Biochemistry 41:9438–9447CrossRefGoogle Scholar
  26. 26.
    Mills DA, Schmidt B, Hiser C, Westley E, Ferguson-Miller S (2002) Membrane potential-controlled inhibition of cytochrome c oxidase by zinc. J Biol Chem 277:14894–14901CrossRefGoogle Scholar
  27. 27.
    Vijayaraghavan K, Yun YS (2008) Bacterial biosorbents and biosorption. Biotechnol Adv 26:266–291CrossRefGoogle Scholar
  28. 28.
    Chen X, Sun G, Xu M (2010) Role of iron in azoreduction by resting cells of Shewanella decolorationis S12. J Appl Microbiol 110:580–586CrossRefGoogle Scholar
  29. 29.
    Chen CH, Chang CF, Ho CH, Tsai TL, Liu SM (2008) Biodegradation of crystal violet by a Shewanella sp. NTOU1. Chemosphere 72:1712–1720CrossRefGoogle Scholar
  30. 30.
    Xu M, Guo J, Kong X, Chen X, Sun G (2007) Fe(III)-enhanced Azo Reduction by Shewanella decolorationis S12. Appl Microbiol Biotechnol 74:1342–1349CrossRefGoogle Scholar
  31. 31.
    Beveridge TJ (1999) Structures of Gram-negative cell walls and their derived membrane vesicles. J Bacteriol 181:4725–4733Google Scholar
  32. 32.
    Ng IS, Zheng X, Chen BY, Chi X, Lu Y, Chang CS (2013) Proteomics approach to decipher novel genes and enzymes characterization of a bioelectricity-generating and dye-decolorizing bacterium Proteus hauseri ZMd44. Biotechnol Bioprocess Eng 18:8–17CrossRefGoogle Scholar
  33. 33.
    Smith MG, Gianoulis TA, Pukatzki S, Mekalanos JJ, Ornston LN, Gerstein M, Snyder M (2007) New insights into Acinetobacter baumannii pathogenesis revealed by high-density pyrosequencing and transposon mutagenesis. Genes Dev 21:601–614CrossRefGoogle Scholar
  34. 34.
    Martinez RJ, Bruce D, Detter C, Goodwin LA, Han J, Han CS, Held B, Land ML, Mikhailova N, Nolan M and others (2012) Complete genome sequence of Rahnella aquatilis CIP 78.65. J Bacteriol 194:3020–3021Google Scholar
  35. 35.
    Hayashi K, Morooka N, Yamamoto Y, Fujita K, Isono K, Choi S, Ohtsubo E, Baba T, Wanner BL, Mori H, Horiuchi T (2006) Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110. Mol Syst Biol 2(2006):0007Google Scholar
  36. 36.
    Eren E, Vijayaraghavan J, Liu J, Cheneke BR, Touw DS, Lepore BW, Indic M, Movileanu L, van den Berg B (2012) Substrate specificity within a family of outer membrane carboxylate channels. PLoS Biol 10:e1001242CrossRefGoogle Scholar
  37. 37.
    Heidelberg JF, Paulsen IT, Nelson KE, Gaidos EJ, Nelson WC, Read TD, Eisen JA, Seshadri R, Ward N, Methe B and others (2002) Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat Biotechnol 20:1118–1123Google Scholar
  38. 38.
    Huang JH, Elzinga EJ, Brechbuehl Y, Voegelin A, Kretzschmar R (2011) Impacts of Shewanella putrefaciens strain CN-32 cells and extracellular polymeric substances on the sorption of As(V) and As(III) on Fe(III)-(hydr)oxides. Environ Sci Technol 45:2804–2810CrossRefGoogle Scholar
  39. 39.
    Seshadri R, Joseph SW, Chopra AK, Sha J, Shaw J, Graf J, Haft D, Wu M, Ren Q, Rosovitz MJ and others (2006) Genome sequence of Aeromonas hydrophila ATCC 7966T: jack of all trades. J Bacteriol 188:8272–8282Google Scholar
  40. 40.
    Galdiero S, Falanga A, Cantisani M, Tarallo R, Della Pepa ME, D’Oriano V, Galdiero M (2012) Microbe-host interactions: structure and role of gram-negative bacterial porins. Curr Protein Pept Sci 13:843–854CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Chemical and Biochemical Engineering, College of Chemistry and Chemical EngineeringXiamen UniversityXiamenChina
  2. 2.The Key Laboratory for Synthetic Biotechnology of Xiamen CityXiamen UniversityXiamenChina
  3. 3.Department of Chemical and Biological EngineeringZhejiang UniversityHangzhouChina
  4. 4.Department of Chemical and Materials EngineeringNational I-Lan UniversityI-LanTaiwan

Personalised recommendations