Browse > Article

Humic Substances Act as Electron Acceptor and Redox Mediator for Microbial Dissimilatory Azoreduction by Shewanella decolorationis S12  

Hong, Yi-Guo (South China Botanical Garden, Chinese Academy of Sciences)
Guo, Jun (Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Institute of Microbiology)
Xu, Zhi-Cheng (Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Institute of Microbiology)
Xu, Mei-Ying (Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Institute of Microbiology)
Sun, Guo-Ping (Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Institute of Microbiology)
Publication Information
Journal of Microbiology and Biotechnology / v.17, no.3, 2007 , pp. 428-437 More about this Journal
Abstract
The potential for humic substances to serve as terminal electron acceptors in microbial respiration and the effects of humic substances on microbial azoreduction were investigated. The dissimilatory azoreducing microorganism Shewanella decolorationis S12 was able to conserve energy to support growth from electron transport to humics coupled to the oxidation of various organic substances or $H_2$. Batch experiments suggested that when the concentration of anthraquinone-2-sulfonate (AQS), a humics analog, was lower than 3 mmol/l, azoreduction of strain S12 was accelerated under anaerobic condition. However, there was obvious inhibition to azoreduction when the concentration of the AQS was higher than 5 mmol/l. Another humics analog, anthraquinone-2-sulfonate (AQDS), could still prominently accelerate azoreduction, even when the concentration was up to 12 mmol/l, but the rate of acceleration gradually decreased with the increasing concentration of the AQDS. Toxic experiments revealed that AQS can inhibit growth of strain S12 if the concentration past a critical one, but AQDS had no effect on the metabolism and growth of strain S12 although the concentration was up to 20 mmol/l. These results demonstrated that a low concentration of humic substances not only could serve as the terminal electron acceptors for conserving energy for growth, but also act as redox mediator shuttling electrons for the anaerobic azoreduction by S. decolorationis S12. However, a high concentration of humic substances could inhibit the bacterial azoreduction, resulting on the one hand from the toxic effect on cell metabolism and growth, and on the other hand from competion with azo dyes for electrons as electron acceptor.
Keywords
Shewanella decolorationis S12; humic reduction; azoreduction; electron acceptor; redox mediator;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
Times Cited By Web Of Science : 16  (Related Records In Web of Science)
연도 인용수 순위
1 Dubin, P. and K. L. Wright. 1975. Reduction of azo food dyes in cultures of Proteus vulgaris. Xenobiotica 5: 563- 571   DOI   ScienceOn
2 Hong, Y., X. Chen, J. Guo, Z. Xu, M. Xu, and G. Sun. 2006. Effects of electron donors and acceptors on anaerobic azo dyes reduction by Shewanella decolorationis S12. Appl. Microbiol. Biotechnol. published online, DOI 10.1007/s00253- 006-0657-2
3 Khehra, M. S., H. S. Saini, D. K. Sharma, B. S. Chadha, and S. S. Chimni. 2006. Biodegradation of azo dye C. I. Acid Red 88 by an anoxic-aerobic sequential bioreactor. Dyes Pigments 7: 1-7   DOI   ScienceOn
4 Miller, T. L. and M. L. Wolin. 1974. A serum bottle modofication of the hungate technique for cultivating obligate anaerobes. Appl. Microbiol. 27: 985-987
5 O'Neill, C., F. R. Hawkes, D. L. Hawkes, N. D. Lourenco, H. M. Pinheiro, and W. Delee. 1999. Colour in textile effluents - sources, measurement, discharge consents and simulation: A review. J. Chem. Technol. Biotechnol. 74: 1009-1018   DOI   ScienceOn
6 O'Neill, C., F. R. Hawkes, D. L. Hawkes, S. Esteves, and S. J. Wilcox. 2000. Anaerobic-aerobic biotreatment of simulated textile effluent containing varied ratios of starch and azo dye. Water. Res. 34: 2355-2361   DOI   ScienceOn
7 Rau, J., H.-J. Knackmuss, and A. Stolz. 2002. Effects of different quinoid redox mediators on the anaerobic reduction of azo dyes by bacteria. Environ. Sci. Technol. 36: 1497- 1504   DOI   ScienceOn
8 Seshadri, S., P. L. Bishop, and A. M. Agha. 1994. Anaerobic/ aerobic treatment of selected azo dyes in wastewater. Waste. Manag. 14: 127-137   DOI   ScienceOn
9 Slobodkin, A. I., T. P. Tourova, B. B. Kuznetsov, N. A. Kostrikina, N. A. Chernyh, and E. A. Bonch-Osmolovskaya. 1999. Thermoanaerobacter siderophilus sp. nov., a novel dissimilatory Fe(III)-reducing, anaerobic, thermophilic bacterium. Int. J. Syst. Bacteriol. 49: 1471-1478   DOI   ScienceOn
10 Stevenson, F. J. 1994. Humus Chemistry: Genesis, Composition, Reactions. New York: Wiley
11 Van der Zee, F. P., R. H. M. Bouwman, D. P. B. T. B. Strik, G. Lettinga, and J. A. Field. 2001. Application of redox mediators to accelerate the transformation of reactive azo dyes in anaerobic bioreactors. Biotechnol. Bioeng. 75: 691- 701   DOI   ScienceOn
12 Fultz, M. L. and R. A. Durst. 1982. Mediator compounds for the electrochemical study of biological redox systems. Anal. Chim. Acta 140: 1-18   DOI   ScienceOn
13 Lovley, D. R., J. D. Coates, E. L. Blunt-Harris, E. J. P. Phillips, and J. C. Woodward. 1996. Humic substances as electron acceptors for microbial respiration. Nature 382: 441-448
14 Padamavathy, S., S. Sandhya, K. Swaminathan, Y. V. Subrahmanyam, and S. N. Kaul. 2003. Comparison of decolorization of reactive azo dyes by Microorganisms isolated from various source. J. Environ. Sci. 15: 628-632
15 Field, J. A., F. J. Cervantes, F. P. Van der Zee, and G. Lettinga. 2000. Role of quinines in the biodegradation of priority pollutants: A review. Water Sci. Technol. 42: 215- 222
16 Kudlich, M., A. Keck, J. Klein, and A. Stolz. 1997. Localization of the enzyme system involved in the anaerobic degradation of azo dyes by Sphingomonas sp. BN6 and effect of artificial redox mediators on the rate of azo reduction. Appl. Environ. Microbiol. 63: 3691-3694
17 Stolz, A. 2001. Basic and applied aspects in the microbial degradation of azo dyes. Appl. Microbiol. Biotechnol. 56: 69-80   DOI
18 Park, E. H., M. S. Jang, I. H. Cha, Y. L. Choi, Y. S. Cho, C. H. Kim, and Y. C. Lee. 2005. Decolorization of a sulfonated azo dye, congo red, by Staphylococcus sp. EY-3. J. Microbiol. Biotechnol. 15: 221-225   과학기술학회마을
19 Chang, J. S. and Y. C. Lin. 2000. Fed-batch bioreactor strategies for microbial decolorization of azo dye using a Pseudomonas luteola strain. Biotechnol. Prog. 16: 979-985   DOI   ScienceOn
20 Chung, K. T. and C. E. Cerniglia. 1992. Mutagenicity of azo dyes: Structure-activity relationships. Mutat. Res. 77: 201- 220
21 Xu M., J. Guo, Y. Cen, X. Zhong, W. Cao, and G. Sun. 2005. Shewanella decolorationis sp. nov., a dye-decolorizing bacterium isolated from an activated-sludge of wastewater treatment plant. Int. J. Syst. Evol. Microbiol. 55: 363-368   DOI   ScienceOn
22 Cervantes, F. J., F. P. van der Zee, G. Lettinga, and J. A. Field. 2001. Enhanced decolourisation of acid orange 7 in a continuous UASB reactor with quinines as redox mediators. Water Sci. Technol. 44: 123-128
23 Cervantes, F. J., F. A. M. de Bok, T. Duong-Dac, A. J. M. Stams, G. Lettinga, and J. A. Field. 2002. Reduction of humic substances by halorespiring, sulphate-reducing and nmethanogenic microorganisms. Environ. Microbiol. 4: 51- 57   DOI   ScienceOn
24 Scott, D. T., D. M. McKnight, E. L. Blunt-Harris, S. E. Kolesar, and D. R. Lovley. 1998. Quinone moieties act as electron acceptors in the reduction of humic substances by humics reducing microorganisms. Environ. Sci. Technol. 32: 2984-2989   DOI   ScienceOn
25 Newman, D. K. and R. Kolter. 2000. A role for excreted quinones in extracellular electron transfer. Nature 405: 94- 97   DOI   ScienceOn
26 Brown, M. A. and S. C. DeVito. 1993. Predicting azo dye toxicity. Crit. Rev. Environ. Sci. Technol. 23: 249-324   DOI   ScienceOn
27 Wesenberg, D., I. Kyriakides, and S. N. Agathos. 2003. White-rot fungi and their enzymes for the treatment of industrial dye effluents. Biotechnol. Adv. 22: 161-187   DOI   ScienceOn
28 Haug, W., A. Schmid, B. Nortemann, D. C. Hempel, A. Stolz, and H.-J. Knackmuss. 1991. Mineralization of the sulfonated azo dye mortant yellow 3 by a 6-aminonaphthalene- 2-sulfonate-degrading bacterial consortium. Appl. Environ. Microbiol. 57: 3144-3149
29 O'Neill, C., A. Lopez, S. Esteves, F. R. Hawkes, D. L. Hawkes, and S. Wilcox. 2000. Azo-dye degradation in an anaerobic-aerobic treatment system operating on simulated textile effluent. Appl. Microbiol. Biotechnol. 53: 249-254   DOI   ScienceOn
30 Chung, K. T. and S. E. J. Stevens. 1993. Degradation of azo dyes by environmental microorganisms and helminths. Environ. Toxicol. Chem. 12: 2121-2132
31 Coates, J. D., D. J. Ellis, E. Roden, K. Gaw, E. L. Blunt-Harris, and D. R. Lovley. 1998. Recovery of humics reducing bacteria from a diversity of sedimentary environments. Appl. Environ. Microbiol. 64: 1504-1509
32 Park, M. R., S. Lee, T.-H. Han, B.-T. Oh, J. H. Shim, and I. S. Kim. 2006. A new intermediate in the degradation of carbofuran by Sphingomonas sp. strain SB5. J. Microbiol. Biotechnol. 16: 1306-1310   과학기술학회마을
33 Rajaguru, P., K. Kalaiselvi, M. Palanivel, and V. Subburam. 2000. Biodegradation of azo dyes in a sequential anaerobicaerobic system. Appl. Microbiol. Biotechnol. 54: 268-273   DOI   ScienceOn
34 Francis, C. A., A. Y. Obraztsova, and B. M. Tebo. 2000. Dissimilatory metal reduction by the facultative anaerobe Pantoea agglomerans SP1. Appl. Environ. Microbiol. 66: 543-548   DOI   ScienceOn
35 Lovley, D. R., J. L. Fraga, E. L. Blunt-Harris, L. A. Hayes, E. J. P. Phillips, and J. D. Coates. 1998. Humic substances as a mediator for microbially catalyzed metal reduction. Acta. Hydrochem. Hydrbiol. 26: 152-157   DOI   ScienceOn
36 Coates, J. D., V. K. Bhupathiraju, L. A. Achenbach, M. J. Mclnerney, and D. R. Lovley. 2001. Geobacter hydrogenophilus. Geobacter chapellei and Geobacter grbicie, three new, strictly anaerobic, dissimilatory Fe(III)-reducers. Int. J. Syst. Evol. Microbiol. 51: 581-588   DOI
37 Tan, N., F. X. Prenafeta-Boldu, J. L. Opsteeg, G. Lettinga, and J. Field. 1999. Biodegradation of azo dyes in cocultures of anaerobic granular sludge with aerobic aromatic amine degrading enrichment cultures. Appl. Microbiol. Biotechnol. 51: 865-871   DOI   ScienceOn
38 Lovley, D. R. and J. D. Coates. 2000. Novel forms of anaerobic respiration of environmental relevance. Curr. Opin. Microbiol. 3: 252-256   DOI   ScienceOn
39 Wolin, E. A., M. J. Wolin, and R. S. Wolfe. 1963. Formation of methane by bacterial extracts. J. Biol. Chem. 238: 2882- 2886