Advertisement

Isolation of Bisphenol A-Tolerating/degrading Shewanella haliotis Strain MH137742 from an Estuarine Environment

  • Felipe Silva de SantanaEmail author
  • Louise Hase Gracioso
  • Bruno Karolski
  • Marcela dos Passos Galluzzi Baltazar
  • Maria Anita Mendes
  • Claudio Augusto Oller do Nascimento
  • Elen Aquino Perpetuo
Article
  • 70 Downloads

Abstract

The human exposure to bisphenol A (BPA) occurs frequently. Once, this compound was one of the highest volume chemicals produced worldwide and used as a plasticizer in many products. However, even at low concentration, it can cause severe damage to the endocrine system because of its endocrine disruptor activity. Thus, mitigation studies to remove or reduce this contaminant from the environment are essential. An alternative method of removing it from the environment is the use of bioremediation processes to the selected bacteria isolated from a BPA-impacted area. In this work, four halotolerant strains were isolated from the Santos Estuary System, one of the most important Brazilian examples of environmental degradation. In the present work, one strain presented strong BPA tolerance and high BPA-degrading activity and could grow in a minimum medium containing BPA as the main carbon source. Strain MH137742 was identified as Shewanella haliotis, based on 16S rRNA gene sequencing and mass spectrometry identification by MALDI-TOF Biotyper. Shewanella haliotis was able to tolerate up to 150 mg L−1 of BPA and biotransform 75 mg L−1 in 10 h in a liquid culture medium. Based on the analysis of the produced metabolites by LC-MS, it was possible to predict the metabolic pathway used by this microorganism to degrade the BPA.

Keywords

Bisphenol A Bioremediation Biodegradation Shewanella haliotis Estuarine environment 

Notes

Author Contribution

This statement is to certify that all Authors have seen and approved the manuscript being submitted. We attest to the fact that all Authors listed on the title page have contributed significantly to the work, have read the manuscript, attest to the validity and legitimacy of the data and its interpretation, and agree to its submission to the Applied Biochemistry and Biotechnology. On behalf of all Co-Authors, the corresponding Author shall bear full responsibility for the submission.

Funding Information

This research was supported by Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP 2013/50218-2) and by CAPES.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that there is no conflict of interest.

Supplementary material

12010_2019_2989_MOESM1_ESM.jpg (55 kb)
Supplement 1 Bisphenol A calibration curve (JPG 54 kb)
12010_2019_2989_MOESM2_ESM.jpg (89 kb)
Supplement 2 Determination of μmax to Shewanella haliotis on culture medium in absence of bisphenol A (JPG 88 kb)
12010_2019_2989_MOESM3_ESM.jpg (93 kb)
Supplement 3 Determination of μmax to Shewanella haliotis on culture medium containing 75 mg.L−1 of BPA. (JPG 93 kb)
12010_2019_2989_MOESM4_ESM.jpg (24 kb)
Supplement 4 Inoculum in solid culture medium. 1. Pseudomonas aeruginosa; 2. Pseudomonas otidis; 3. Klebsiella pneumoniae; 4. Enterobacter cloacae; 5. Bacillus cereus; 6. Bacillus therungiensis; 7. Bacillus altitutinis; 8. Acinetobacter tandoii; 9. Acinetobacter pittii; 10. Aeromonas hydrophila; 11. Rhodococcus ruber. (JPG 24 kb)
12010_2019_2989_MOESM5_ESM.jpg (73 kb)
Supplement 5 MALDI-TOF Biotyper bacteria identification (JPG 72 kb)
12010_2019_2989_MOESM6_ESM.jpg (87 kb)
Supplement 6 HPLC chromatograms regarding BPA degradation. (JPG 86 kb)

References

  1. 1.
    Morishita, Y., Nomura, Y., Fukui, C., Kawakami, T., Ikeda, T., Mukai, T., Yuba, T., Inamura, K.-I., Yamaoka, H., Miyazaki, K.-I., Okazaki, H., & Haishima, Y. (2017). Pilot study on novel blood containers with alternative plasticizers for red cell concentrate storage. PLoS One, 12(9), 1–12.  https://doi.org/10.1371/journal.pone.0185737.Google Scholar
  2. 2.
    Olea, N., Pulgas, R., Pérez, P., Olea-Serrano, F., Rivas, A., Novillo-Fertrell, A., Pedraza, V., Soto, A. M., & Sonnenschein, C. (1996). Estrogenicity of resin-based composites and sealants used in dentistry. Environmental Health Perspectives, 104(3), 298–305.CrossRefGoogle Scholar
  3. 3.
    Ben-Jonathan, N., & Steinmetz, R. (1998). Xenoestrogens: the emerging story of bisphenol A. Trends in Endocrinology and Metabolism, 9(3), 124–128.CrossRefGoogle Scholar
  4. 4.
    Staples, C. A., Dorn, P. B., Klecka, G. M., O'Block, S. T., & Harris, L. R. (1998). A review of the environmental fate, effects, and exposures of bisphenol A. Chemosphere, 36(10), 2149–2173.CrossRefGoogle Scholar
  5. 5.
    Wetherill, Y. B., Akingbemi, B. T., Kanno, J., McLachlan, J. A., Nadal, A., Sonnenschein, C., Watson, C. S., Zoeller, R. T., & Belcher, S. C. (2007). In vitro molecular mechanisms of bisphenol A action. Reproductive Toxicology, 24(2), 178–198.CrossRefGoogle Scholar
  6. 6.
    Lee, H., & Peart, T. E. (2000). Determination of bisphenol A in sewage effluent and sludge by solid-phase and supercritical fluid extraction and gas chromatography/mass spectrometry. Envrironmental Analysys, 83, 290–298.Google Scholar
  7. 7.
    Vandenberd, L. N., Chahoud, I., Heindel, J. J., Padmanabhan, V., Paumgartten, F. J. R., & Schoenfelder, G. (2010). Urinary, circulating and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environmental Health Prespectives, 118(8), 1055–1070.CrossRefGoogle Scholar
  8. 8.
    Eladak, S., Gristin, T., Moison, D., Guerquin, M. J., N'Tumba-Byn, T., Pozzi-Gaudin, S., Benachi, A., Livera, G., Rouiller-Fabre, V., & Habert, R. (2015). A new chapter in the bisphenol A story : bisphenol S and bisphenol F are not safe alternatives to this compound. Fertility and Sterility, 103(1), 11–21.CrossRefGoogle Scholar
  9. 9.
    Gould, J. C., Leonard, L. S., Maness, S. C., Wagner, B. L., Conner, K., Zacharewski, T., Safe, S., McDonnell, D. P., & Gaid, K. W. (1998). Bisphenol A interacts with the estrogen receptor alpha in a distinct manner from estradiol. Molecular and Cellular Endocrinology, 142(1-2), 203–214.CrossRefGoogle Scholar
  10. 10.
    Goloubkova, T., & Spritzer, P. M. (2000). Arquivos Brasileiros de Endocrinologia & Metabologia. Xenoestrogênios: o exemplo do bisfenol-A. Arquivos Brasileiros de Endocrinologia & Metabologia., 44(4), 323–330.CrossRefGoogle Scholar
  11. 11.
    Keri, R. A., Ho, S. M., Knudsen, K. E., Soto, A. M., & Prins, G. S. (2007). An evaluation of evidence for the carcinogenic activity of bisphenol A. Reproductive Toxicology, 24(2), 240–252.CrossRefGoogle Scholar
  12. 12.
    Mouhapatra, D. P., Brar, S. K., Tyagi, R. D., & Surampalli, R. Y. (2010). Concomitant degradation of bisphenol A during ultrasonication and Fenton oxidation and production of biofertilizer from wastewater sludge. Chemosphere, 78(5), 923–941.  https://doi.org/10.1016/j.ultsonch.2011.03.013.CrossRefGoogle Scholar
  13. 13.
    Teuten, E. L., Saquing, J. M., Knappe, D. R., Barlaz, M. A., Jonsson, S., Bjorn, A., Rowland, S. J., Thompson, R. C., Galloway, T. S., Tamashita, R., Ochi, D., Watanuki, Y., Moore, C., Viet, P. H., Tana, T. S., Prudent, M., Boonyatumanond, R., Zakaria, M. P., Akkhavong, K., Ogata, Y., Hirai, H., Iwasa, S., Mizukawa, K., Hagino, Y., Imamura, A., Sasha, M., & Takada, H. (2009). Transport and release of chemicals from plastics to the environment and to wildlife. Philosophical Transactions of the Royal Society, 364(1526), 2027–2045.  https://doi.org/10.1098/rstb.2008.0284.CrossRefGoogle Scholar
  14. 14.
    Yamanaka, H., Kuniiko, M., Takashi, O., Tatsuhiko, O., & Kiyofumi, S. (2008). Efficient microbial degradation of bisphenol A in the presence of activated carbon. Journal of Bioscience and Bioengeneering, 105(2), 157–160.CrossRefGoogle Scholar
  15. 15.
    Anderson, A. C., Sanunu, M., & Schneider, C. (2014). Rapid species-level identification of vaginal and oral lactobacilli using MALDI-TOF MS analysis and 16S rDNA sequencing. BMC Microbiology, 14, 1–9.CrossRefGoogle Scholar
  16. 16.
    Avanzi, I. G., Gracioso, L. H., Baltazar, M. P. G., Karolski, B., Perpetuo, E. A., & Nascimento, C. A. O. (2016). Rapid bacteria identification from environmental mining samples using MALDI-TOF MS analysis. Environmental Science and Pollution Research, 24, 3717–3726.CrossRefGoogle Scholar
  17. 17.
    Chen, W., & Kuo, T. T. (1993). A simple and rapid method for the preparation of Gram-negative bacterial genomic DNA. Nucleic Acids Research, 21(9), 2260.CrossRefGoogle Scholar
  18. 18.
    Sambrook, J., Fritschi, E. F., & Maniatis, T. (1989). Molecular cloning: a laboratory manual (3rd ed.). Cold Spring Harbor NY: Cold Spring Harbor Laboratory Press.  https://doi.org/10.1016/0167-7799(91)90068-S.Google Scholar
  19. 19.
    Assadian, O., Wehse, K., Hübner, N. O., Koburger, T., Bagel, S., Jethon, F., & Kramer, A. (2011). Minimum inhibitory (MIC) and minimum microbicidal concentration (MMC) of polihexanide and triclosan against antibiotic sensitive and resistant Staphylococcus aureus and Escherichia coli strains. Krankenhhyg Interdiszip, 6, 1–7.  https://doi.org/10.3205/dgkh000163.Google Scholar
  20. 20.
    O’Toole, D. K. (1983). A simple and rapid method for the preparation of Gram-negative bacterial genomic DNA. Applied and Environmental Microbiology, 46(2), 506–508.Google Scholar
  21. 21.
    Perpetuo, E. A., Marques, R. C. P., Mendes, M. A., Lima, W. C., Menck, C. F. M., & Nascimento, C. A. O. (2009). Characterization of the phenol monooxygenase gene from Chromobacterium violaceum: potential use for phenol biodegradation. Biotechnology and Bioprocess Engineering, 14(6), 694–670.CrossRefGoogle Scholar
  22. 22.
    Matsumura, Y., Hosokawa, C., Sasaki-Mori, M., Akahira, A., Fukunaga, K., Ikeuchi, T., Oshiman, K., & Tsuchido, T. (2009). Isolation and characterization of novel bisphenol-A--degrading bacteria from soils. Biocontrol Science, 14(4), 161–169.CrossRefGoogle Scholar
  23. 23.
    Telke, A. A., Seon-Won, K., & Sanjay, P. G. (2012). Significant reduction in toxicity, BOD, and COD of textile dyes and textile industry effluent by a novel bacterium Pseudomonas sp. LBC1. Folia Microbiologica, 57(2), 115–122.CrossRefGoogle Scholar
  24. 24.
    Janda, J. M., & Abbott, S. L. (2009). The genus Aeromonas: taxonomy, pathogenicity, and infection. Clinical Microbiology Reviews, 23, 35–73.CrossRefGoogle Scholar
  25. 25.
    Yu-Peng, H., Chen, Y. J., Chang, Y. J., & Shih, Y. H. (2015). Biodegradation of bisphenol A with diverse microorganisms from river sediment. Journal of Hazardous Materials, 286, 285–290.CrossRefGoogle Scholar
  26. 26.
    Kang, J. H., & Kondo, F. (2002). Bisphenol A degradation by bacteria isolated from river water. Archives of Environmental Contamination and Toxicology, 43(3), 265–269.CrossRefGoogle Scholar
  27. 27.
    Fischer, J., Kappelmeyer, U., Kastner, M., Schauer, F., & Heipieper, H. J. (2010). The degradation of bisphenol A by the newly isolated bacterium Cupriavidus basilensis JF1 can be enhanced by biostimulation with phenol. International Biodeterioration and Biodegradation, 64(4), 324–330.CrossRefGoogle Scholar
  28. 28.
    Sasaki, M. J., Maki, K. O. Y., & Matsumura, T. T. (2005). Biodegradation of bisphenol A by cells and cell lysate from Sphingomonas sp. strain AO1. Biodegradation, 16(5), 449–459.CrossRefGoogle Scholar
  29. 29.
    Matsumura, Y., Akahira-Moriyah, A., & Sasaki-Mori, M. (2015). Isolation and characterization of novel bisphenol-A--degrading bacteria from soils. Biocontrol Science, 20(1), 35–42.CrossRefGoogle Scholar
  30. 30.
    Ike, M., Chen, M. Y., Jin, C. S., & Fujita, M. (2002). Acute toxicity, mutagenicity, and estrogenicity of biodegradation products of bisphenol-A. Environmental Toxicology, 17(5), 457–461.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Felipe Silva de Santana
    • 1
    • 2
    Email author
  • Louise Hase Gracioso
    • 1
  • Bruno Karolski
    • 1
  • Marcela dos Passos Galluzzi Baltazar
    • 3
  • Maria Anita Mendes
    • 3
  • Claudio Augusto Oller do Nascimento
    • 1
    • 3
  • Elen Aquino Perpetuo
    • 1
    • 2
    • 4
  1. 1.Environmental Research and Education Center, CEPEMA-POLI-USPUniversity of São PauloCubatãoBrazil
  2. 2.The Interunits Graduate Program in BiotechnologyUniversity of São PauloSão PauloBrazil
  3. 3.Chemical Engineering Department, POLI-USPUniversity of São PauloSão PauloBrazil
  4. 4.Department of Marine SciencesFederal University of São Paulo, Imar-UnifespSantosBrazil

Personalised recommendations