Environmental Science and Pollution Research

, Volume 22, Issue 19, pp 15145–15153 | Cite as

Biodegradation of bisphenol A by an algal-bacterial system

  • Er Jin Eio
  • Minako Kawai
  • Chiaki Niwa
  • Masato Ito
  • Shuichi Yamamoto
  • Tatsuki Toda
Research Article


The degradation of bisphenol A (BPA) by Chlorella sorokiniana and BPA-degrading bacteria was investigated. The results show that BPA was partially removed by a monoculture of C. sorokiniana, but the remaining BPA accounted for 50.2, 56.1, and 60.5 % of the initial BPA concentrations of 10, 20, and 50 mg L−1, respectively. The total algal BPA adsorption and accumulation were less than 1 %. C. sorokiniana-bacterial system effectively removed BPA with photosynthetic oxygen provided by the algae irrespective of the initial BPA concentration. The growth of C. sorokiniana in the algal system was inhibited by BPA concentrations of 20 and 50 mg L−1, but not in the algal-bacterial system. This observation indicates that bacterial growth in the algal-bacterial system reduced the BPA-inhibiting effect on algae. A total of ten BPA biodegradation intermediates were identified by GC-MS. The concentrations of the biodegradation intermediates decreased to a low level at the end of the experiment. The hypothetical carbon mass balance analysis showed that the amounts of oxygen demanded by the bacteria are insufficient for effective BPA degradation. However, adding an external carbon source could compensate for the oxygen shortage. This study demonstrates that the algal-bacterial system has the potential to remove BPA and its biodegradation intermediates.


Algal-bacterial system Bacterial consortium Biodegradation Bisphenol A Inhibition Photosynthetic oxygen 



We would like to express our gratitude to Kenji Tsuchiya, Masatoshi Kishi, Yukiko Sasakawa, and Xia Yuan Jun from Soka University, for their assistance in this study. We are grateful to the Hachioji Kitano Wastewater Treatment Plant of Japan for the preparation of the seed sludge. The present study was financially supported by “The Environment Research and Technology Development Fund” from the Ministry of the Environment, Japan (4-1406).


  1. Alexander HC, Dill DC, Smith LW, Guiney PD, Dorn P (1988) Bisphenol A: acute aquatic toxicity. Environ Toxicol Chem 7:19–26CrossRefGoogle Scholar
  2. Bahr M, Stams AJM, De la Rosa F, Garcia-Encina PA, Muñoz R (2011) Assessing the influence of the carbon oxidation-reduction state on organic pollutant biodegradation in algal-bacterial photobioreactors. Appl Microbiol Biotechnol 90:1527–1536CrossRefGoogle Scholar
  3. Benner R, Kaiser K (2011) Biological and photochemical transformations of amino acids and lignin phenols in riverine dissolved organic matter. Biogeochemistry 102:209–222CrossRefGoogle Scholar
  4. Borde X, Guieysse B, Delgado O, Muñoz R, Hatti-Kaul R, Nugier-Chauvin C, Patin H, Mattiasson B (2003) Synergistic relationships in algal-bacterial microcosms for the treatment of aromatic pollutants. Bioresour Technol 86:293–300CrossRefGoogle Scholar
  5. Bordel S, Guieysse B, Muñoz R (2009) Mechanistic model for the reclamation of industrial wastewaters using algal-bacterial photobioreactors. Environ Sci Technol 43:3200–3207CrossRefGoogle Scholar
  6. Correa-Reyes G, Viana MT, Marquez-Rocha FJ, Licea AF, Ponce E, VazquezDuhalt R (2007) Nonylphenol algal bioaccumulation and its effect through the trophic chain. Chemosphere 68:662–670CrossRefGoogle Scholar
  7. Cousins IT, Staples CA, Klecka GM, Mackay D (2002) A multimedia assessment of the environmental fate of bisphenol A. Hum Ecol Risk Assess 8:1107–1135CrossRefGoogle Scholar
  8. Croft MT, Lawrence AD, Raux-Deery E, Warrem MJ, Smith AG (2005) Algae acquire vitamin B-12 through a symbiotic relationship with bacteria. Nature 438:90–93CrossRefGoogle Scholar
  9. de-Bashan LE, Moreno M, Hernandez JP, Bashan Y (2002) Removal of ammonium and phosphorus ions from synthetic wastewater by the microalgae Chlorella vulgaris coimmobilized in alginate beads with the microalgae growth promoting bacterium Azospirillum brasilense. Water Res 36:2941–2948CrossRefGoogle Scholar
  10. de-Bashan LE, Trejo A, Huss VAR, Hernandez JP, Bashan Y (2008) Chlorella sorokiniana UTEX 2805, a heat and intense, sunlight-tolerant microalga with potential for removing ammonium from wastewater. Bioresour Technol 99:4980–4989CrossRefGoogle Scholar
  11. Eio EJ, Kawai M, Tsuchiya K, Yamamoto S, Toda T (2014) Biodegradation of bisphenol A by bacterial consortia. Int Biodeterior Biodegrad 96:166–173CrossRefGoogle Scholar
  12. Fischer J, Kappelmeyer U, Kastner M et al (2010) The degradation of bisphenol A by the newly isolated bacterium Cupriavidus basilensis JF1 can be enhanced by biostimulation with phenol. Int Biodeterior Biodegrad 64:324–330CrossRefGoogle Scholar
  13. Gonzalez LE, Bashan Y (2000) Increased growth of the microalga Chlorella vulgaris when coimmobilized and cocultured in alginate beads with the plant-growth-promoting bacterium Azospirillum brasilense. Appl Environ Microbiol 66:1527–1531CrossRefGoogle Scholar
  14. Hill R, Bendall F (1960) Function of the two cytochrome components in chloroplasts-A Working Hypothesis. Nature 186:136–137CrossRefGoogle Scholar
  15. Hirooka T, Nagase H, Uchida K, Hiroshige Y, Ehara Y, Nishikawa J, Nishihara T, Miyamoto K, Hirata Z (2005) Biodegradation of bisphenol A and disappearance of its estrogenic activity by the green alga Chlorella fusca var. vacuolata. Environ Toxicol Chem 24:1896–1901CrossRefGoogle Scholar
  16. Ike M, Chen MY, Jin CS, Fujita M (2002) Acute toxicity, mutagenicity, and estrogenicity of biodegradation products of bisphenol A. Environ Toxicol 17:457–461CrossRefGoogle Scholar
  17. Kolvenbach B, Schlaich N, Raoui Z, Prell J, Zuhlke S, Schaffer A, Guengerich FP, Corvini PF (2007) Degradation pathway of bisphenol A: does ipso substitution apply to phenols containing a quaternary alpha-carbon structure in the para position? Appl Environ Microbiol 73:4776–4784CrossRefGoogle Scholar
  18. Krishnan AV, Stathis P, Permuth SF, Tokes L, Feldman D (1993) Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 132:2279–2286Google Scholar
  19. Li G, Zu L, Wong P-K et al (2012) Biodegradation and detoxification of bisphenol A with one newly-isolated strain Bacillus sp. GZB: Kinetics, mechanism and estrogenic transition. Bioresour Technol 114:224–230CrossRefGoogle Scholar
  20. Li T, Zheng Y, Yu L, Chen S (2013) High productivity cultivation of a heatresistantmicroalga Chlorella sorokiniana for biofuel production. Bioresour Technol 131:60–67CrossRefGoogle Scholar
  21. Lobos JH, Leib TK, Su TM (1992) Biodegradation of bisphenol A and other bisphenols by a gram-negative aerobic bacterium. Appl Environ Microbiol 58:1823–1831Google Scholar
  22. Loferer-Krossbacher M, Klima J, Psenner R (1998) Determination of bacterial cell dry mass by transmission electron microscopy and densitometric image analysis. Appl Environ Microbiol 64:688–694Google Scholar
  23. Mohapatra DP, Brar SK, Tyagi RD, Surampalli RY (2011) Occurrence of bisphenol A in wastewater and wastewater sludge of CUQ treatment plant. J Xenobiot 1:9–16CrossRefGoogle Scholar
  24. Morita M, Watanabe Y, Saiki H (2000) High photosynthetic productivity of green microalga Chlorella sorokiniana. Appl Biochem Biotechnol 87:203–218CrossRefGoogle Scholar
  25. Muñoz R, Kollner C, Guieysse B, Mattiasson B (2003) Salicylate biodegradation by various algal-bacterial consortia under photosynthetic oxygenation. Biotechnol Lett 25:1905–1911CrossRefGoogle Scholar
  26. Muñoz R, Kollner C, Guieysse B, Mattiasson B (2004) Photosynthetically oxygenated salicylate biodegradation in a continuous stirred tank photobioreactor. Biotechnol Bioeng 87:797–803CrossRefGoogle Scholar
  27. Nakajima N, Teramoto T, Kasai F, Sano T, Tamaoki M, Aono M, Kubo A, Kamada H, Azumi Y, Saji H (2007) Glycosylation of bisphenol A by freshwater microalgae. Chemosphere 69:934–941CrossRefGoogle Scholar
  28. Nguyen LN, Hai FI, Yang S, Kang J, Leusch FDL, Roddick F, Price WE, Nghiem LD (2013) Removal of trace organic contaminants by an MBR comprising a mixed culture of bacteria and white-rot fungi. Bioresour Technol 148:234–241CrossRefGoogle Scholar
  29. Nishihara T, Nishikawa J, Kanayama T, Dakeyama F, Saito K, Imagawa M, Takatori S, Kitagawa Y, Hori S, Utsumi H (2000) Estrogenic activities of 517 chemicals by yeast two-hybrid assay. J Health Sci 46:282–298CrossRefGoogle Scholar
  30. Nomiyama K, Tanizaki T, Koga T, Arizono K, Shinohara R (2007) Oxidative degradation of BPA using TiO2 in water, and transition of estrogenic activity in the degradation pathways. Arch Environ Contam Toxicol 52:8–15CrossRefGoogle Scholar
  31. Oswald WJ (1988) Micro-algae and waste-water treatment. In: Borowitzka MBL (ed) Micro-algal Biotechnology. Cambridge University Press, CambridgeGoogle Scholar
  32. Oswald WJ, Ludwig HF, Gotaas HB, Lynch V (1951) Algae symbiosis in oxidation ponds I. Growth characteristics of Euglena gracilis cultured in sewage. Sew Ind Wastes 23:1337–1355Google Scholar
  33. Porges N, Jasewicz L, Hoover SR (1956) Principles of biological oxidation. In: McCabe J, Eckenfelder WW Jr (eds) Biological Treatment of Sewage and Industrial Wastes, vol 1. Reinhold Publishing, New YorkGoogle Scholar
  34. Roh H, Subramanya N, Zhao F, Yu CP, Sandt J, Chu KH (2009) Biodegradation potential of wastewater micropollutants by ammonia-oxidizing bacteria. Chemosphere 77:1084–1089CrossRefGoogle Scholar
  35. Shibata A, Goto Y, Saito H, Kikuchi T, Toda T, Taguchi S (2006) Comparison of SYBR Green I and SYBR Gold stains for enumerating bacteria and viruses by epifluorescence microscopy. Aquat Microb Ecol 43:223–231CrossRefGoogle Scholar
  36. Sorokin C, Krauss RW (1958) The effects of light intensity on the growth rates of green algae. Plant Physiol 33:109–113CrossRefGoogle Scholar
  37. Spivack J, Leib TK, Lobos JH (1994) Novel pathway for bacterial metabolism of bisphenol A. Rearrangements and stilbene cleavage in bisphenol A metabolism. J Biol Chem 269:7323–7329Google Scholar
  38. Staples CA, Dorn PB, Klecka GM, O’Block ST, Harris LR (1998) A review of the environmental fate, effects, and exposures of bisphenol-A. Chemosphere 36:2149–2173CrossRefGoogle Scholar
  39. Suzuki R, Ishimaru T (1990) An improved method for the determination of phytoplankton chlorophyll using N, N-dimethylformamide. J Oceanogr Soc Jpn 46:190–194CrossRefGoogle Scholar
  40. Suzuki T, Nakagawa Y, Takano I, Yaguchi K, Yasuda K (2004) Environmental fate of bisphenol A and its biological metabolites in river water and their xeno-estrogenic activity. Environ Sci Technol 38:2389–2396CrossRefGoogle Scholar
  41. Welschmeyer NA (1994) Fluorometric analysis of chlorophyll-a in the presence of chlorophyll-b and pheopigments. Limnol Oceanogr 39:1985–1992CrossRefGoogle Scholar
  42. Yamamoto T, Yasuhara A, Shiraishi H, Nakasugi O (2001) Bisphenol A in hazardous waste landfill leachates. Chemosphere 42:415–418CrossRefGoogle Scholar
  43. Yoshihara S, Makishima M, Suzuki N, Ohta S (2001) Metabolic activation of bisphenol A by rat liver S9 fraction. Toxicol Sci 62:221–227CrossRefGoogle Scholar
  44. Zhang W, Yin K, Chen L (2013) Bacteria-mediated bisphenol A degradation. Appl Microbiol Biotechnol 97:5681–5689CrossRefGoogle Scholar
  45. Zhang W, Xiong B, Sun WF, An S, Lin KF, Guo MJ, Cui XH (2014) Acute chronic toxic effects of bisphenol A on Chlorella pyrenoidosa and Scenedesnus obliquus. Environ Toxicol 6:714–722CrossRefGoogle Scholar
  46. Zhao J, Li Y, Zhang C, Zeng Q, Zhou Q (2008) Sorption and degradation of bisphenol A by aerobic activated sludge. J Hazard Mater 155:305–311CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Er Jin Eio
    • 1
  • Minako Kawai
    • 2
    • 3
  • Chiaki Niwa
    • 3
  • Masato Ito
    • 3
  • Shuichi Yamamoto
    • 3
  • Tatsuki Toda
    • 3
  1. 1.Graduate School of EngineeringSoka UniversityTokyoJapan
  2. 2.Asian People’s ExchangeTokyoJapan
  3. 3.Department of Environmental Engineering for Symbiosis, Faculty of EngineeringSoka UniversityTokyoJapan

Personalised recommendations