Skip to main content
SpringerLink
Log in

Biodegradation of bisphenol A by an algal-bacterial system

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alexander HC, Dill DC, Smith LW, Guiney PD, Dorn P (1988) Bisphenol A: acute aquatic toxicity. Environ Toxicol Chem 7:19–26

    Article  CAS  Google Scholar 

  • 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 90:1527–1536

    Article  CAS  Google Scholar 

  • Benner R, Kaiser K (2011) Biological and photochemical transformations of amino acids and lignin phenols in riverine dissolved organic matter. Biogeochemistry 102:209–222

    Article  CAS  Google Scholar 

  • 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 86:293–300

    Article  Google Scholar 

  • Bordel S, Guieysse B, Muñoz R (2009) Mechanistic model for the reclamation of industrial wastewaters using algal-bacterial photobioreactors. Environ Sci Technol 43:3200–3207

    Article  CAS  Google Scholar 

  • 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 68:662–670

    Article  CAS  Google Scholar 

  • Cousins IT, Staples CA, Klecka GM, Mackay D (2002) A multimedia assessment of the environmental fate of bisphenol A. Hum Ecol Risk Assess 8:1107–1135

    Article  Google Scholar 

  • Croft MT, Lawrence AD, Raux-Deery E, Warrem MJ, Smith AG (2005) Algae acquire vitamin B-12 through a symbiotic relationship with bacteria. Nature 438:90–93

    Article  CAS  Google Scholar 

  • 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 36:2941–2948

    Article  CAS  Google Scholar 

  • 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 99:4980–4989

    Article  CAS  Google Scholar 

  • Eio EJ, Kawai M, Tsuchiya K, Yamamoto S, Toda T (2014) Biodegradation of bisphenol A by bacterial consortia. Int Biodeterior Biodegrad 96:166–173

    Article  Google Scholar 

  • 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 64:324–330

    Article  CAS  Google Scholar 

  • 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 66:1527–1531

    Article  CAS  Google Scholar 

  • Hill R, Bendall F (1960) Function of the two cytochrome components in chloroplasts-A Working Hypothesis. Nature 186:136–137

    Article  CAS  Google Scholar 

  • 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 24:1896–1901

    Article  CAS  Google Scholar 

  • Ike M, Chen MY, Jin CS, Fujita M (2002) Acute toxicity, mutagenicity, and estrogenicity of biodegradation products of bisphenol A. Environ Toxicol 17:457–461

    Article  CAS  Google Scholar 

  • 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 73:4776–4784

    Article  CAS  Google Scholar 

  • Krishnan AV, Stathis P, Permuth SF, Tokes L, Feldman D (1993) Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 132:2279–2286

    CAS  Google Scholar 

  • 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 114:224–230

    Article  CAS  Google Scholar 

  • Li T, Zheng Y, Yu L, Chen S (2013) High productivity cultivation of a heatresistantmicroalga Chlorella sorokiniana for biofuel production. Bioresour Technol 131:60–67

    Article  CAS  Google Scholar 

  • Lobos JH, Leib TK, Su TM (1992) Biodegradation of bisphenol A and other bisphenols by a gram-negative aerobic bacterium. Appl Environ Microbiol 58:1823–1831

    CAS  Google Scholar 

  • 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 64:688–694

    CAS  Google Scholar 

  • Mohapatra DP, Brar SK, Tyagi RD, Surampalli RY (2011) Occurrence of bisphenol A in wastewater and wastewater sludge of CUQ treatment plant. J Xenobiot 1:9–16

    Article  CAS  Google Scholar 

  • Morita M, Watanabe Y, Saiki H (2000) High photosynthetic productivity of green microalga Chlorella sorokiniana. Appl Biochem Biotechnol 87:203–218

    Article  CAS  Google Scholar 

  • Muñoz R, Kollner C, Guieysse B, Mattiasson B (2003) Salicylate biodegradation by various algal-bacterial consortia under photosynthetic oxygenation. Biotechnol Lett 25:1905–1911

    Article  Google Scholar 

  • Muñoz R, Kollner C, Guieysse B, Mattiasson B (2004) Photosynthetically oxygenated salicylate biodegradation in a continuous stirred tank photobioreactor. Biotechnol Bioeng 87:797–803

    Article  Google Scholar 

  • 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 69:934–941

    Article  CAS  Google Scholar 

  • 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 148:234–241

    Article  CAS  Google Scholar 

  • 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 46:282–298

    Article  CAS  Google Scholar 

  • 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 52:8–15

    Article  CAS  Google Scholar 

  • Oswald WJ (1988) Micro-algae and waste-water treatment. In: Borowitzka MBL (ed) Micro-algal Biotechnology. Cambridge University Press, Cambridge

    Google Scholar 

  • 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 23:1337–1355

    Google Scholar 

  • 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 York

    Google Scholar 

  • Roh H, Subramanya N, Zhao F, Yu CP, Sandt J, Chu KH (2009) Biodegradation potential of wastewater micropollutants by ammonia-oxidizing bacteria. Chemosphere 77:1084–1089

    Article  CAS  Google Scholar 

  • 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 43:223–231

    Article  Google Scholar 

  • Sorokin C, Krauss RW (1958) The effects of light intensity on the growth rates of green algae. Plant Physiol 33:109–113

    Article  CAS  Google Scholar 

  • 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 269:7323–7329

    CAS  Google Scholar 

  • 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 36:2149–2173

    Article  CAS  Google Scholar 

  • Suzuki R, Ishimaru T (1990) An improved method for the determination of phytoplankton chlorophyll using N, N-dimethylformamide. J Oceanogr Soc Jpn 46:190–194

    Article  CAS  Google Scholar 

  • 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 38:2389–2396

    Article  CAS  Google Scholar 

  • Welschmeyer NA (1994) Fluorometric analysis of chlorophyll-a in the presence of chlorophyll-b and pheopigments. Limnol Oceanogr 39:1985–1992

    Article  CAS  Google Scholar 

  • Yamamoto T, Yasuhara A, Shiraishi H, Nakasugi O (2001) Bisphenol A in hazardous waste landfill leachates. Chemosphere 42:415–418

    Article  CAS  Google Scholar 

  • Yoshihara S, Makishima M, Suzuki N, Ohta S (2001) Metabolic activation of bisphenol A by rat liver S9 fraction. Toxicol Sci 62:221–227

    Article  CAS  Google Scholar 

  • Zhang W, Yin K, Chen L (2013) Bacteria-mediated bisphenol A degradation. Appl Microbiol Biotechnol 97:5681–5689

    Article  CAS  Google Scholar 

  • 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 6:714–722

    Article  Google Scholar 

  • Zhao J, Li Y, Zhang C, Zeng Q, Zhou Q (2008) Sorption and degradation of bisphenol A by aerobic activated sludge. J Hazard Mater 155:305–311

    Article  CAS  Google Scholar 

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

  1. Graduate School of Engineering, Soka University, 1-236 Tangi-cho, Hachioji, Tokyo, 192-8577, Japan

    Er Jin Eio

  2. Asian People’s Exchange, Inoue Building, 1-5-12 Negishi, Taitou-ku, Tokyo, 110-0003, Japan

    Minako Kawai

  3. Department of Environmental Engineering for Symbiosis, Faculty of Engineering, Soka University, 1-236 Tangi-cho, Hachioji, Tokyo, 192-8577, Japan

    Minako Kawai, Chiaki Niwa, Masato Ito, Shuichi Yamamoto & Tatsuki Toda

Authors
  1. Er Jin Eio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Minako Kawai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chiaki Niwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Masato Ito
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shuichi Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tatsuki Toda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Er Jin Eio.

Additional information

Responsible editor: Gerald Thouand

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eio, E.J., Kawai, M., Niwa, C. et al. Biodegradation of bisphenol A by an algal-bacterial system. Environ Sci Pollut Res 22, 15145–15153 (2015). https://doi.org/10.1007/s11356-015-4693-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-4693-2

Keywords

Search

Navigation