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Anaerobic Dechlorination of Tetrachlorobisphenol A in River Sediment and Associated Changes in Bacterial Communities

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Abstract

Tetrachlorobisphenol A (TCBPA) is a widely used flame retardant and a potential endocrine disruptor. We estimated the role of the microbial community in degradation of TCBPA in river sediment from the vicinity of an E-waste processing facility. The effects of different anaerobic conditions on degradation efficiency of TCBPA were investigated, and differences in bacterial communities among these conditions were analyzed by 16S ribosomal RNA (rRNA) gene sequencing. The most effective dechlorination of TCBPA occurred under methanogenic conditions followed by electron donor-enhanced conditions and sulfate-reducing conditions with initial sulfate concentrations of 1, 10, and 20 mM. The extent of TCBPA removal under these conditions mentioned above was 65, 44, 43, 23, and 23%, respectively. 16S rRNA gene sequence analysis indicated that five dominant genera in the phylum Chloroflexi and another five species of Bacteroidetes, Chlorobi, and Firmicutes in these five systems were largely involved in TCBPA dechlorination. The initial sample had a total relative abundance of autochtonous potential dechlorinating bacteria of 12%. After 160 days, these values increased to 29–43% under above conditions. Addition of TCBPA decreased bacterial diversity. Efficiency of TCBPA degradation depends on the abundance and metabolism of dechlorinating bacterial guilds. The effectiveness of dechlorinating microbes in degradation of TCBPA was reduced by high sulfate concentrations.

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References

  • Aulenta, F., Beccari, M., Majone, M., Papini, M. P., & Tandoi, V. (2008). Competition for H2 between sulfate reduction and dechlorination in butyrate-fed anaerobic cultures. Process Biochemistry, 43(2), 161–168.

    Article  CAS  Google Scholar 

  • Bao, P., Hu, Z., Wang, X., Chen, J., Ba, Y., Hua, J., Zhu, C., Zhong, M., & Wu, C. (2012). Dechlorination of p, p'-DDTs coupled with sulfate reduction by novel sulfate-reducing bacterium Clostridium sp. BXM. Environmental Pollution, 162, 303–310.

    Article  CAS  Google Scholar 

  • Bastos, P. M., Eriksson, J., Green, N., & Bergman, K. (2008). A standardized method for assessment of oxidative transformations of brominated phenols in water. Chemosphere, 70(7), 1196–1202.

    Article  CAS  Google Scholar 

  • Blanco, E., Casais, M. C., Mejuto, M. C., & Cela, R. (2005). Analysis of tetrabromobisphenol A and other phenolic compounds in water samples by non-aqueous capillary electrophoresis coupled to photodiode array ultraviolet detection. Journal of Chromatography A, 1071(1–2), 205–211.

    Article  CAS  Google Scholar 

  • Bunge, M., Adrian, L., Kraus, A., Opel, M., Lorenz, W. G., Andreesen, J. R., Gorisch, H., & Lechner, U. (2003). Reductive dehalogenation of chlorinated dioxins by an anaerobic bacterium. Nature, 421(6921), 357–360.

    Article  CAS  Google Scholar 

  • Casatta, N., Mascolo, G., Roscioli, C., & Viganò, L. (2015). Tracing endocrine disrupting chemicals in a coastal lagoon (Sacca di Goro, Italy): sediment contamination and bioaccumulation in Manila clams. Science of the Total Environment, 511, 214–222.

    Article  CAS  Google Scholar 

  • Chang, B., Yuan, S., & Ren, Y. (2012). Anaerobic degradation of tetrabromobisphenol-A in river sediment. Ecological Engineering, 49, 73–76.

    Article  Google Scholar 

  • Chen, M., Cao, F., Li, F., Liu, C., Tong, H., Wu, W., & Hu, M. (2013). Anaerobic transformation of DDT related to iron(III) reduction and microbial community structure in paddy soils. Journal of Agricultural and Food Chemistry, 61(9), 2224–2233.

    Article  CAS  Google Scholar 

  • Chu, S., Haffner, G. D., & Letcher, R. J. (2005). Simultaneous determination of tetrabromobisphenol A, tetrachlorobisphenol A, bisphenol A and other halogenated analogues in sediment and sludge by high performance liquid chromatography-electrospray tandem mass spectrometry. Journal of Chromatography A, 1097(1–2), 25–32.

    Article  CAS  Google Scholar 

  • DeWeerd, K. A., Concannon, F., & Suflita, J. M. (1991). Relationship between hydrogen consumption, dehalogenation, and the reduction of sulfur oxyanions by Desulfomonile tiedjei. Applied and Environmental Microbiology, 57(7), 1929–1934.

    CAS  Google Scholar 

  • Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., & Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27(16), 2194–2200.

    Article  CAS  Google Scholar 

  • Eriksson, J., Rahm, S., Green, N., Bergman, K., & Jakobsson, E. (2004). Photochemical transformations of tetrabromobisphenol A and related phenols in water. Chemosphere, 54(1), 117–126.

    Article  CAS  Google Scholar 

  • Fan, Z., Hu, J., An, W., & Yang, M. (2013). Detection and occurrence of chlorinated byproducts of bisphenol A, nonylphenol, and estrogens in drinking water of China: comparison to the parent compounds. Environmental Science & Technology, 47(19), 10841–10850.

    Article  CAS  Google Scholar 

  • Fang, H., Cai, L., Yang, Y., Ju, F., Li, X., Yu, Y., & Zhang, T. (2014). Metagenomic analysis reveals potential biodegradation pathways of persistent pesticides in freshwater and marine sediments. Science of the Total Environment, 470–471, 983–992.

    Article  Google Scholar 

  • Fennell, D. E., Nijenhuis, I., Wilson, S. F., Zinder, S. H., & Häggblom, M. M. (2004). Dehalococcoides ethenogenes strain 195 reductively dechlorinates diverse chlorinated aromatic pollutants. Environmental Science & Technology, 38(7), 2075–2081.

    Article  CAS  Google Scholar 

  • Fukazawa, H., Hoshino, K., Shiozawa, T., Matsushita, H., & Terao, Y. (2001). Identification and quantification of chlorinated bisphenol A in wastewater from wastepaper recycling plants. Chemosphere, 44(5), 973–979.

    Article  CAS  Google Scholar 

  • Gallart-Ayala, H., Moyano, E., & Galceran, M. T. (2010). On-line solid phase extraction fast liquid chromatography-tandem mass spectrometry for the analysis of bisphenol A and its chlorinated derivatives in water samples. Journal of Chromatography A, 1217(21), 3511–3518.

    Article  CAS  Google Scholar 

  • Gomes, B. C., Adorno, M. A. T., Okada, D. Y., Delforno, T. P., Lima Gomes, P. C. F., Sakamoto, I. K., & Varesche, M. B. A. (2014). Analysis of a microbial community associated with polychlorinated biphenyl degradation in anaerobic batch reactors. Biodegradation, 25(6), 797–810.

    Article  CAS  Google Scholar 

  • Horikoshi, S., Miura, T., Kajitani, M., Horikoshi, N., & Serpone, N. (2008). Photodegradation of tetrahalobisphenol-A (X = Cl, Br) flame retardants and delineation of factors affecting the process. Applied Catalysis, B: Environmental, 84(3–4), 797–802.

    Article  CAS  Google Scholar 

  • Herlemann, D. P., Labrenz, M., Jurgens, K., Bertilsson, S., Waniek, J. J., & Andersson, A. F. (2011). Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME Journal, 5(10), 1571–1579.

    Article  CAS  Google Scholar 

  • Ismail, Z. Z., & Pavlostathis, S. G. (2010). Influence of sulfate reduction on the microbial dechlorination of pentachloroaniline in a mixed anaerobic culture. Biodegradation, 21(1), 43–57.

    Article  CAS  Google Scholar 

  • Jayachandran, G., Görisch, H., & Adrian, L. (2003). Dehalorespiration with hexachlorobenzene and pentachlorobenzene by Dehalococcoides sp. strain CBDB1. Archives of Microbiology, 180(6), 411–416.

    Article  CAS  Google Scholar 

  • Jayamani, I., & Cupples, A. M. (2015). Stable isotope probing reveals the importance of Comamonas and Pseudomonadaceae in RDX degradation in samples from a Navy detonation site. Environmental Science and Pollution Research, 22(13), 10340–10350.

    Article  CAS  Google Scholar 

  • Kalasekar, S. M., Zacharia, E., Kessler, N., Ducharme, N. A., Gustafsson, J. K., Kakadiaris, I. A., & Bondesson, M. (2015). Identification of environmental chemicals that induce yolk malabsorption in zebrafish using automated image segmentation. Reproductive Toxicology, 55, 20–29.

    Article  CAS  Google Scholar 

  • Leung, A. O. W., Luksemburg, W. J., Wong, A. S., & Wong, M. H. (2007). Spatial distribution of polybrominated diphenyl ethers and polychlorinated dibenzo-p-dioxins and dibenzofurans in soil and combusted residue at guiyu, an electronic waste recycling site in southeast China. Environmental Science & Technology, 41(8), 2730–2737.

    Article  CAS  Google Scholar 

  • Li, L. (2014). Transformation of tetrabromobisphenol A and tetrachlorobisphenol A in river sediments. Guang Zhou: South China University of Technology (in Chinese).

    Google Scholar 

  • Lin, N., Shan, Z., Zhu, C., & Ren, Y. (2015). Heavy metal and PCB contamination in river sediments of an E-waste recycling site in Qingyuan. Environmental Chemistry, 34(9), 1685–1693. in Chinese.

    CAS  Google Scholar 

  • Liu, D., Lei, L., Yang, B., Yu, Q., & Li, Z. (2013). Direct electron transfer from electrode to electrochemically active bacteria in a bioelectrochemical dechlorination system. Bioresource Technology, 148, 9–14.

    Article  CAS  Google Scholar 

  • Liu, S., Li, L., & Ren, Y. (2014). Anaerobic biodegradation of TCBPA in river sediment and the role of sulfate reducing bacteria (SRB) in TCBPA’s degradation. Environmental Chemistry, 33(06), 915–922. in Chinese.

    CAS  Google Scholar 

  • Loffler, F. E., Yan, J., Ritalahti, K. M., Adrian, L., Edwards, E. A., Konstantinidis, K. T., Muller, J. A., Fullerton, H., Zinder, S. H., & Spormann, A. M. (2013). Dehalococcoides mccartyi gen. nov., sp. nov., obligately organohalide-respiring anaerobic bacteria relevant to halogen cycling and bioremediation, belong to a novel bacterial class, Dehalococcoidia classis nov., order Dehalococcoidales ord. nov. and family Dehalococcoidaceae fam. nov., within the phylum Chloroflexi. International Journal of Systematic and Evolutionary Microbiology, 63(Pt 2), 625–635.

    Article  CAS  Google Scholar 

  • Magoc, T., & Salzberg, S. L. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27(21), 2957–2963.

    Article  CAS  Google Scholar 

  • Men, Y., Feil, H., Verberkmoes, N. C., Shah, M. B., Johnson, D. R., Lee, P. K., West, K. A., Zinder, S. H., Andersen, G. L., & Alvarez-Cohen, L. (2012). Sustainable syntrophic growth of Dehalococcoides ethenogenes strain 195 with Desulfovibrio vulgaris Hildenborough and Methanobacterium congolense: global transcriptomic and proteomic analyses. ISME Journal, 6(2), 410–421.

    Article  CAS  Google Scholar 

  • Miura, T., Yamazoe, A., Ito, M., Ohji, S., Hosoyama, A., Takahata, Y., & Fujita, N. (2015). The impact of injections of different nutrients on the bacterial community and its dechlorination activity in chloroethene-contaminated groundwater. Microbes and Environments, 30(2), 164–171.

    Article  Google Scholar 

  • Nies, L., & Vogel, T. M. (1990). Effects of organic substrates on dechlorination of Aroclor 1242 in anaerobic sediments. Applied and Environmental Microbiology, 56(9), 2612–2617.

    CAS  Google Scholar 

  • Panagiotakis, I., Mamais, D., Pantazidou, M., Rossetti, S., Aulenta, F., & Tandoi, V. (2014). Predominance of Dehalococcoides in the presence of different sulfate concentrations. Water, Air, & Soil Pollution, 225, 1.

    Article  CAS  Google Scholar 

  • Pérez-de-Mora, A., Zila, A., McMaster, M. L., & Edwards, E. A. (2014). Bioremediation of chlorinated ethenes in fractured bedrock and associated changes in dechlorinating and nondechlorinating microbial populations. Environmental Science & Technology, 48(10), 5770–5779.

    Article  Google Scholar 

  • Philips, J., Haest, P. J., Springael, D., & Smolders, E. (2013). Inhibition of geobacter dechlorinators at elevated trichloroethene concentrations is explained by a reduced activity rather than by an enhanced cell decay. Environmental Science & Technology, 47(3), 1510–1517.

    CAS  Google Scholar 

  • Podosokorskaya, O. A., Kadnikov, V. V., Gavrilov, S. N., Mardanov, A. V., Merkel, A. Y., Karnachuk, O. V., Ravin, N. V., Bonch-Osmolovskaya, E. A., & Kublanov, I. V. (2013). Characterization of Melioribacter roseus gen. nov., sp. nov., A novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria, and a proposal of a novel bacterial phylum Ignavibacteriae. Environmental Microbiology, 15(6), 1759–1771.

    Article  CAS  Google Scholar 

  • Praveckova, M., Brennerova, M. V., Cvancarova, M., De Alencastro, L. F., Holliger, C., & Rossi, P. (2015). Divergent PCB organohalide-respiring consortia enriched from the efflux channel of a former Delor manufacturer in Eastern Europe. Ecotoxicology and Environmental Safety, 120, 223–234.

    Article  CAS  Google Scholar 

  • Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Gloeckner, F. O. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research, 41(D1), D590–D596.

    Article  CAS  Google Scholar 

  • Rasool, K., Mahmoud, K. A., & Lee, D. S. (2015). Influence of co-substrate on textile wastewater treatment and microbial community changes in the anaerobic biological sulfate reduction process. Journal of Hazardous Materials, 299, 453–461.

    Article  CAS  Google Scholar 

  • Richardson, R. E. (2013). Genomic insights into organohalide respiration. Current Opinion in Biotechnology, 24(3), 498–505.

    Article  CAS  Google Scholar 

  • Ruan, T., Liang, D., Song, S., Song, M., Wang, H., & Jiang, G. (2015). Evaluation of the in vitro estrogenicity of emerging bisphenol analogs and their respective estrogenic contributions in municipal sewage sludge in China. Chemosphere, 124, 150–155.

    Article  CAS  Google Scholar 

  • Sánchez-Brunete, C., Miguel, E., & Tadeo, J. L. (2009). Determination of tetrabromobisphenol-A, tetrachlorobisphenol-A and bisphenol-A in soil by ultrasonic assisted extraction and gas chromatography-mass spectrometry. Journal of Chromatography A, 1216(29), 5497–5503.

    Article  Google Scholar 

  • Schmieder, R., & Edwards, R. (2011). Quality control and preprocessing of metagenomic datasets. Bioinformatics, 27(6), 863–864.

    Article  CAS  Google Scholar 

  • Song, S., Song, M., Zeng, L., Wang, T., Liu, R., Ruan, T., & Jiang, G. (2014). Occurrence and profiles of bisphenol analogues in municipal sewage sludge in China. Environmental Pollution, 186, 14–19.

    Article  CAS  Google Scholar 

  • Suzuki, D., Baba, D., Satheeja Santhi, V., Jebakumar Solomon, R. D., & Katayama, A. (2013). Use of a glass bead-containing liquid medium for efficient production of a soil-free culture with polychlorinated biphenyl-dechlorination activity. World Journal of Microbiology and Biotechnology, 29(8), 1461–1471.

    Article  CAS  Google Scholar 

  • Terasaki, M., Kosaka, K., Kunikane, S., Makino, M., & Shiraishi, F. (2011). Assessment of thyroid hormone activity of halogenated bisphenol A using a yeast two-hybrid assay. Chemosphere, 84(10), 1527–1530.

    Article  CAS  Google Scholar 

  • Tsydenova, O., & Bengtsson, M. (2011). Chemical hazards associated with treatment of waste electrical and electronic equipment. Waste Management, 31(1), 45–58.

    Article  CAS  Google Scholar 

  • Voordeckers, J. W., Fennell, D. E., Jones, K., & Haggblom, M. M. (2002). Anaerobic biotransformation of tetrabromobisphenol A, tetrachlorobisphenol A, and bisphenol A in estuarine sediments. Environmental Science & Technology, 36(4), 696–701.

    Article  CAS  Google Scholar 

  • Wagner, D. D., Hug, L. A., Hatt, J. K., Spitzmiller, M. R., Padilla-Crespo, E., Ritalahti, K. M., Edwards, E. A., Konstantinidis, K. T., & Loffler, F. E. (2012). Genomic determinants of organohalide-respiration in Geobacter lovleyi, an unusual member of the Geobacteraceae. BMC Genomics, 13, 200.

    Article  CAS  Google Scholar 

  • Xie, Z., Wang, Z., Wang, Q., Zhu, C., & Wu, Z. (2014). An anaerobic dynamic membrane bioreactor (AnDMBR) for landfill leachate treatment: performance and microbial community identification. Bioresource Technology, 161, 29–39.

    Article  CAS  Google Scholar 

  • Yamada, T., & Sekiguchi, Y. (2009). Cultivation of uncultured Chloroflexi subphyla: significance and ecophysiology of formerly uncultured chloroflexi ‘Subphylum I’ with natural and biotechnological relevance. Microbes and Environments, 24(3), 205–216.

    Article  Google Scholar 

  • Yan, J., Ritalahti, K. M., Wagner, D. D., & Loffler, F. E. (2012). Unexpected specificity of interspecies cobamide transfer from Geobacter spp. to organohalide-respiring Dehalococcoides mccartyi strains. Applied and Environmental Microbiology, 78(18), 6630–6636.

    Article  CAS  Google Scholar 

  • Yang, Y., Lu, L., Zhang, J., Yang, Y., Wu, Y., & Shao, B. (2014). Simultaneous determination of seven bisphenols in environmental water and solid samples by liquid chromatography-electrospray tandem mass spectrometry. Journal of Chromatography A, 1328, 26–34.

    Article  CAS  Google Scholar 

  • Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I., Dominguez-Bello, M. G., Contreras, M., Magris, M., Hidalgo, G., Baldassano, R. N., Anokhin, A. P., Heath, A. C., Warner, B., Reeder, J., Kuczynski, J., Caporaso, J. G., Lozupone, C. A., Lauber, C., Clemente, J. C., Knights, D., Knight, R., & Gordon, J. I. (2012). Human gut microbiome viewed across age and geography. Nature.

  • Yuan, S. Y., Chen, S. J., & Chang, B. V. (2011). Anaerobic degradation of tetrachlorobisphenol-A in river sediment. International Biodeterioration & Biodegradation, 65(1), 185–190.

    Article  CAS  Google Scholar 

  • Yuan, S. Y., Li, H. T., Huang, W., & Chang, B. V. (2010). Biodegradation of tetrachlorobisphenol-A in river sediment and the microbial community changes. Journal of Environmental Science and Health Part B-Pesticides Food Contaminants and Agricultural Wastes, 45(PII 9225884225), 360–365.

    Article  CAS  Google Scholar 

  • Zhang, Y., Wang, X., Hu, M., & Li, P. (2015). Effect of hydraulic retention time (HRT) on the biodegradation of trichloroethylene wastewater and anaerobic bacterial community in the UASB reactor. Applied Microbiology and Biotechnology, 99(4), 1977–1987.

    Article  CAS  Google Scholar 

  • Zhou, J., Zhou, X., Li, Y., & Xing, J. (2015). Bacterial communities in haloalkaliphilic sulfate-reducing bioreactors under different electron donors revealed by 16S rRNA MiSeq sequencing. Journal of Hazardous Materials, 295, 176–184.

    Article  CAS  Google Scholar 

  • Ziv-El, M., Delgado, A. G., Yao, Y., Kang, D., Nelson, K. G., Halden, R. U., & Krajmalnik-Brown, R. (2011). Development and characterization of DehaloR^2, a novel anaerobic microbial consortium performing rapid dechlorination of TCE to ethene. Applied Microbiology and Biotechnology, 92(5), 1063–1071.

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant No. 51178190), Special Funds for the Construction of Key Disciplines Funded Projects in Guangdong Province (Grant No. 2013CXZDA004), and the Research Fund of SIT of Guangzhou (Grant No. 2013J4100107). LetPub (www.letpub.com) provided linguistic assistance during manuscript preparation.

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Zhang, J., Liu, S., Li, L. et al. Anaerobic Dechlorination of Tetrachlorobisphenol A in River Sediment and Associated Changes in Bacterial Communities. Water Air Soil Pollut 228, 78 (2017). https://doi.org/10.1007/s11270-017-3254-3

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