Assessing the impact of synthetic estrogen on the microbiome of aerated submerged fixed-film reactors simulating tertiary sewage treatment and isolation of estrogen-degrading consortium: Science of the Total Environment

C.L.S. Vilela, R.S. Peixoto, C.T.C.D.C. Rachid, J.P. Bassin

Research output: Contribution to journalArticlepeer-review

5 Scopus citations


17α-ethinylestradiol (EE2) is a synthetic estrogen that can cause harmful effects on animals, such as male feminization and infertility. However, the impact of the EE2 contamination on microbial communities and the potential role of bacterial strains as bioremediation agents are underexplored. The aim of this work was to evaluate the impact of EE2 on the microbial community dynamics of aerated submerged fixed-film reactors (ASFFR) simulating a polishing step downstream of a secondary sewage treatment. For this purpose, the reactors were fed with a synthetic medium with low COD content (around 50 mg l−1), supplemented (reactor H) or not (reactor C) with 1 μg l−1 of EE2. Sludge samples were periodically collected during the bioreactors operation to assess the bacterial profile over time by 16S rRNA gene amplicon sequencing or by bacterial isolation using culture-dependent approach. The results revealed that the most abundant phyla in both reactors were Proteobacteria and Bacteroidetes. At genus level, Chitinophagaceae, Nitrosomonas and Bdellovibrio predominated. Significant effects caused by EE2 treatment and bioreactors operating time were observed by non-metric multidimensional scaling. Therefore, even at low concentrations as 1 μg l−1, EE2 is capable of influencing the bioreactor microbiome. Culture-dependent methods showed that six bacterial isolates, closely related to Pseudomonas and Acinetobacter genera, could grow on EE2 as the sole carbon source under aerobic conditions. These organisms may potentially be used for the assembly of an EE2-degrading bacterial consortium and further exploited for bioremediation applications, including tertiary sewage treatment to remove hormone-related compounds not metabolized in secondary depuration stages. © 2020 Elsevier B.V.
Original languageEnglish
JournalSci. Total Environ.
StatePublished - 2020

Bibliographical note

Cited By :1

Export Date: 5 May 2021


Correspondence Address: Bassin, J.P.; Chemical Engineering Program/COPPE, P.O. Box 68502, Brazil; email:

Molecular Sequence Numbers: GENBANK: MF627709, MF627710, MF627711, MF627712, MF627713, MF627714;

Chemicals/CAS: ethinylestradiol, 57-63-6; Estradiol Congeners; Estrogens; Ethinyl Estradiol; RNA, Ribosomal, 16S; Sewage

Funding details: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, CAPES

Funding details: Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq

Funding details: Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro, FAPERJ

Funding text 1: The authors would like to express their gratitude to Coordination for the Improvement of Higher Education Personnel (CAPES), Brazilian National Council for Scientific and Technological Development (CNPq) and Carlos Chagas Filho Foundation for Research Support of the State of Rio de Janeiro (FAPERJ) for the financial support.

References: Adeel, M., Song, X., Wang, Y., Francis, D., Yang, Y., Environmental impact of estrogens on human, animal and plant life: a critical review (2017) Environ. Int., 99, pp. 107-119; Adlercreutz, H., Martin, F., Jarvenpaa, P., Fotsls, T., Steroid absorption and enteroheoptic recycling contraception (1979) J. Steroid. Biochem., 20, pp. 201-223; Andrade, L.L., Leite, D.C.A., Ferreira, E.M., Ferreira, L.Q., Paula, G.R., Maguire, M.J., Hubert, C.R.J., Rosado, A.S., Microbial diversity and anaerobic hydrocarbon degradation potential in an oil-contaminated mangrove sediment (2010) BMC Microbiol., 12, pp. 1-10; Apha, Stardand Methods for the Examination of Water and Wastewater (2005), 21st ed. American Public Health Association, American Water Works Association, Water Environmental Federation Washington; Barel-Cohen, K., Shoreb, L.S., Shemesh Wenzel, A., Mueller, J., Kronfeld-Schor, N., Monitoring of natural and synthetic hormones in a polluted river (2006) J. Environ. Manag., 78, pp. 16-23; Bassin, J.P., Rachid, C.T.C.C., Vilela, C.L.S., Cao, S.M.S., Peixoto, R.S., Dezotti, M., Revealing the bacterial profile of an anoxic-aerobic moving-bed biofilm reactor system treating a chemical industry wastewater (2017) Int. Biodeterior. Biodegradation, 120, pp. 152-160; Bilal, M., Iqbal, H.M., Persistence and impact of steroidal estrogens on the environment and their laccase-assisted removal (2019) Sci. Total Environ., 690, pp. 447-459; Bloom, M.S., Micu, R., Neamtiu, I., Female infertility and emerging organic pollutants of concern (2016) Curr. Epidem. Report, 3, pp. 39-50; Blunt, S.M., Benotti, M.J., Rosen, M.R., Hedlund, B., Moser, D., Reversible reduction of estrone to 17β-estradiol by Rhizobium, Sphingopyxis, and Pseudomonas isolates from the Las Vegas Wash (2017) J. Environ. Qual., 46, pp. 281-287; Bourne, D.G., Iida, Y., Uthicke, S., Smith-Keune, C., Changes in coral-associated microbial communities during a bleaching event (2008) ISME J, 2, pp. 350-363; Brown, E.J., Resnick, S.M., Rebstock, C., Luong, H.V., Lindstrom, J., UAF radiorespirometric protocol for assessing hydrocarbon mineralization potential in environmental samples (1991) Biodegr, 2, pp. 121-127; Burlington, H., Lindeman, V.F., Effect of DDT on testes and secondary sex characters of white leghorn cockerels (1950) P. Soc. Exp. Biol. Med., 74, pp. 48-51; Cao, S.M., Fontoura, G.A., Dezotti, M., Bassin, J.P., Combined organic matter and nitrogen removal from a chemical industry wastewater in a two-stage MBBR system (2016) Environ. Technol., 37, pp. 96-107; Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Lozupone, C.A., Turnbaugh, P.J., Fierer, N., Knight, R., Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample (2011) P. Ntl. Acad. Sci., 108, pp. 4516-4522; Carr, E.L., Kampfer, P., Patel, B.K.C., Gurtler, V., Seviour, R.J., Seven novel species of Acinetobacter isolated from activated sludge (2003) Int. J. Syst. Evol. Micr., 53, pp. 953-963; Chen, K.L., Madak-Erdogan, Z., Estrogen and microbiota crosstalk: should we pay attention (2016) Trends Endocrin. Met., 27, pp. 752-755; Chiang, Y.R., Fang, J.Y., Ismail, W., Wang, P., Initial steps in anoxic testosterone degradation by Steroidobacter denitrificans (2010) Microbiol, 156, pp. 2253-2259; Colborn, T., Vom Saal, F.S., Soto, A.M., Developmental effects of endocrine-disrupting chemicals in wildlife and humans (1993) Environ. Health. Persp., 101, pp. 378-384; Cole, J.R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R.J., Kulam-Syed-Mohideen, A.S., Tiedje, J.M., The ribosomal database project: improved alignments and new tools for rRNA analysis (2009) Nucleic Acids Res., 37, pp. 141-145; Combalbert, S., Raquet, G.H., Occurrence, fate, and biodegradation of estrogens in sewage and manure (2010) Appl. Microbiol. Biot., 86, pp. 1671-1692; Daston, G.P., Gooch, J.W., Breslin, W.J., Sherey, D.L., Nikiforov, A.I., Fico, T.A., Gorsuch, J.W., Environmental estrogens and reproductive health: a discussion of the human and environmental data (1997) Reprod. Toxicol., 11, pp. 465-481; Escher, B.I., Pronk, W., Suter, M.J.F., Maurer, M., Monitoring the removal efficiency of pharmaceuticals and hormones in different treatment processes of source-separated urine with bioassays (2006) Environ. Sci. Technol., 40, pp. 5091-5101; Fahrbach, M., Kuever, J., Remesch, M., Huber, B.E., Kampfer, P., Dott, W., Hollender, J., Steroidobacter denitrificans gen. nov., sp. nov., a steroidal hormone-degrading gammaproteobacterium (2008) Int. J. Syst. Evol. Micr., 58, pp. 2215-2223; Fernandez, L., Louvado, A., Esteves, V.I., Gome, N.C., Almeida, A., Cunha, A., Biodegradation of 17β-estradiol by bacteria isolated from deep sea sediments in aerobic and anaerobic media (2017) J. Hazard. Mater., 323, pp. 359-366; Giambiagi-Marval, M., Mafrae, L.A., Penido, G.C., Bastos, M.C.F., Distinct groups of plasmids correlated with bacteriocin production in Staphylococcus aureus (1990) J. Gen. Microbiol., 136, pp. 1591-1599; Godoy, F., Vancanneyt, M., Martínez, M., Steinbüchel, A., Swings, J., Rehm, B.H., Sphingopyxis chilensi ssp. nov., a chlorophenol-degrading bacterium that accumulates polyhydroxyalkanoate, and transfer of Sphingomonas alaskensis to Sphingopyxis alaskensis comb. nov (2003) Int. J. Syst. Evol. Microbiol., 53, pp. 473-477; Guo, J., Ni, B., Han, X., Chen, X., Bond, P., Peng, Y., Yuan, Z., Unraveling microbial structure and diversity of activated sludge in a full-scale simultaneous nitrogen and phosphorus removal plant using metagenomic sequencing (2017) Enzyme Microb. Tech., 102, pp. 1-24; Hall, J.E., Guyton, C.A., Tratado de Fisiologia Médica (2006), pp. 905-908. , 11 ed. Elsevier Brasil; Harb, M., Wei, C.H., Wang, N., Amy, G., Hong, P.Y., Organic micropollutants in aerobic and anaerobic membrane bioreactors: changes in microbial communities and gene expression (2016) Bioresour. Technol., 218, pp. 882-891; Hutchins, S.R., White, M.V., Hudson, F.M., Fine, D.D., Analysis of lagoon samples from different concentrated animal feeding operations for estrogens and estrogen conjugates (2007) Environ. Sci. Technol., 41, pp. 738-744; Hyman, M.R., Wood, P.M., Methane oxidation by Nitrosomonas europaea (1983) Biochem. J., 212, pp. 31-37; Hyman, M.R., Murton, I.B., Arp, D.J., Interaction of ammonia monooxygenase from Nitrosomonas europeae with alkanes, alkenes and alkynes (1988) Appl. Environ. Microbiol., 54, pp. 3187-3190; Hyman, M.R., Page, C.L., Arp, D.J., Oxidation of methyluoride and dimethylether by ammonia monooxygenase in Nitrosomonas europaea (1994) Appl. Environ. Microbiol., 60, pp. 3033-3035; Isabelle, M., Villemur, R., Juteau, P., Lépine, F., Isolation of estrogen-degrading bacteria from an activated sludge bioreactor treating swine waste, including a strain that converts estrone to β-estradiol (2011) Can. J. Microbiol., 57, pp. 559-568; Jin, T., Zhang, T., Ye, L., Lee, O., Wong, Y.H., Qian, P.Y., Diversity and quantity of ammonia-oxidizing Archaea and Bacteria in sediment of the Pearl River Estuary, China (2011) Appl. Microbiol. Biot., 90, pp. 1137-1145; Johnson, A.C., Belfroid, A., Di Corcia, A., Estimating steroid estrogen inputs into activated sludge treatment works and observations on their removal from the effluent (2000) Sci. Total Environ., 256, pp. 163-173; Kabir, E.R., Rahman, M.S., Rahman, I., A review on endocrine disruptors and their possible impacts on human health (2015) Environ. Toxicol. Pharm., 40, pp. 241-258; Ke, J., Zhuang, W., Gin, K.Y.-H., Reinhard, M., Hoon, L.T., Tay, J.-H., Characterization of estrogen-degrading bacteria isolated from an artificial sandy aquifer with ultrafiltered secondary effluent as the medium (2007) Appl. Microbiol. Biot., 75, pp. 1163-1171; Kertesz, M.A., Kawasaki, A., Hydrocarbon degrading Sphingomonads: Sphingomonas, Sphingobium, Novosphingobium and Sphingopyxis (2010) Handbook of Hydrocarbon and Lipid Microbiology, , K.N. Timmis Springer Berlin, Heidelberg; Kornmant, K.S., Loesche, W.J., Effects of estradiol and progesterone on Bacteroides melaninogenicus and Bacteroides gingivalis (1982) Infect. Immun., 35, pp. 256-263; Kumar, S., Stecher, G., Li, M., Knyaz, C., Tamura, K., MEGA X: molecular evolutionary genetics analysis across computing platforms (2018) Mol. Biol. Evol., 35, pp. 1547-1549; Lane, D.J., (1991) 16S/23S rRNA Sequencing. In: Nucleic Acid Techniques in Bacterial Systematics, pp. 115-175. , E. Stackebrandt M. Goodfellow Jonh, W., Sons New York; Larcher, S., Yargeau, V., Biodegradation of 17α-ethinylestradiol by heterotrophic bacteria (2013) Environ. Pollut., 173, pp. 17-22; Leu, Y., Wang, P., Shiao, M.S., Ismail, W., Chiang, Y.R., A novel testosterone catabolic pathway in bacteria (2011) J. Bacteriol., 193, pp. 4447-4455; Lim, Y.L., Morad, N., bin Lalung, J., Chan, S.Y., Bakar, S.A.A.A., Isolation and identification of 17α-ethinylestradiol-degrading bacterial strains from POME and cow dung (2016) Int. J. Environ. Sci. Dev., 7, pp. 881-884; Lyte, M., Ernst, S., Catecholamine induced growth of gram-negative bacteria (1992) Life Sci., 50, pp. 203-212; Ma, C., Qin, D., Sun, Q., Zhang, F., Liu, H., Yu, C., Removal of environmental estrogens by bacterial cell immobilization technique (2016) Chemosphere, 144, pp. 607-614; McLachlan, J.A., Simpson, E., Martin, M., Endocrine disrupters and female reproductive health (2006) Best Practice Research: Clin. Endocrinol. Met., 20, pp. 63-75; Michiels, E.D., Vergauwen, L., Lai, F.Y., Town, R.M., Covaci, A., van Nuijs, A.L., Van Cruchten, S.J., Knapen, D., Advancing the Zebrafish embryo test for endocrine disruptor screening using micro-injection: Ethinyl estradiol as a case study (2019) Environ. Toxicol. Chem., 38, pp. 533-547; Muller, M., Combalbert, S., Delgenès, N., Bergheaud, V., Rocher, V., Benoit, P., Delgenès, J.P., Raquet, G.H., Occurrence of estrogens in sewage sludge and their fate during plant-scale anaerobic digestion (2010) Chemosphere, 81, pp. 65-71; Nash, J.P., Kime, D.E., Van Der Ven, L.T.M., Wester, P.W., Brion, F., Maack, G., Stahlschmidt-Allner, P., Tyler, C.R., Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish (2004) Environ. Health. Persp., 112, pp. 1725-1733; Nelson, D.L., Cox, M.M., Lehninger: Princípios de Bioquímica (2005), 4ª ed. W.H. Ediciones Omega, Freeman; Neuman, H., Debelius, J.W., Knight, R., Koren, O., Microbial endocrinology: the interplay between the microbiota and the endocrine system (2015) FEMS Microbiol. Rev., 39, pp. 509-521; Nogueira, A.A., Bassin, J.P., Cerqueira, A.C., Dezotti, M., Integration of biofiltration and advanced oxidation processes for tertiary treatment of an oil refinery wastewater aiming at water reuse (2016) Environ. Sci. Pollut. Res. Int., 23, pp. 9730-9741; Pamplona-Silva, M.T., Mazzeo, D.E.C., Bianchi, J., Marin-Morales, M.A., Estrogenic compounds: chemical characteristics, detection methods, biological and environmental effects (2018) Water Air Soil Poll, 229, p. 144; Panter, G.H., Thompson, R.S., Sumpter, J.P., Adverse reproductive effects in male fathead minnows (Pimephales promelas) exposed to environmentally relevant concentrations of the natural oestrogens, oestradiol and oestrone (1998) Aquat. Toxicol., 42, pp. 243-253; Peixoto, R.S., Chaer, G.M., Franco, N., Junior, F.B.R., Mendes, I.C., Rosado, A.S., A decade of land use contributes to changes in the chemistry, biochemistry and bacterial community structures of soils in the Cerrado (2010) Anton. Leeuw., 98, pp. 403-413; Peixoto, R.S., Chaer, G.M., Carmo, F.L., Araújo, F.V., Paes, J.E., Volpon, A., Santiago, G.A., Rosado, A.S., Bacterial communities reflect the spatial variation in pollutant levels in Brazilian mangrove sediment (2011) Anton. Leeuw., 99, pp. 341-354; Rachid, C.T.C.C., Santos, A.L., Piccolo, M.C., Balieiro, F.C., Coutinho, H.L.C., Peixoto, R.S., Tiedje, J.M., Rosado, A.S., Effect of sugarcane burning or green harvest methods on the Brazilian Cerrado soil bacterial community structure (2013) PLoS One, 8; Raman, D.R., Williams, E.L., Layton, A.C., Burns, R.T., Easter, J.P., Daugherty, A.S., Mullen, M.D., Sayler, G.S., Estrogen content of dairy and swine wastes (2004) Environ. Sci. Technol., 38, pp. 3567-3573; Richardson, S.D., Kimura, S.Y., Emerging environmental contaminants: challenges facing our next generation and potential engineering solutions (2017) Environ. Technol. Innov., 8, pp. 40-56; Rosenfeld, C.S., Cooke, P.S., Endocrine disruption through membrane estrogen receptors and novel pathways leading to rapid toxicological and epigenetic effects (2019) J. Steroid Biochem. Mol. Biol., 187, pp. 106-117; Roshchina, V., Evolutionary considerations of neurotransmitters in microbial, plant, and animal cells (2010) Microbial Endocrinology: Interkingdom Signaling in Infectious Disease and Health, pp. 17-52. , M. Lyte P. Fitzgerald Springer New York; Routledge, E.J., Sheahan, D., Desbrow, C., Brighty, G.C., Waldock, M., Sumpter, J.P., Identification of estrogenic chemicals in STW effluent. In vivo responses in trout and roach (1998) Environ. Sci. Technol., 32, pp. 1559-1565; Saaristo, M., Johnstone, C.P., Xu, K., Allinson, M., Wong, B.B., The endocrine disruptor, 17α-ethinyl estradiol, alters male mate choice in a freshwater fish (2019) Aquatic Toxicol, 208, pp. 118-125; Sanapareddy, N., Hamp, T.J., Gonzalez, L.C., Hilger, H.A., Fodor, A.A., Clinton, S.M., Molecular diversity of a North Carolina wastewater treatment plant as revealed by pyrosequencing (2009) Appl. Environ. Microbiol., 75, pp. 1688-1696; Santos, H.F., Cury, J.C., Carmo, F.L., Rosado, A.S., Peixoto, R.S., 18S rDNA sequences from microeukaryotes reveal oil indicators in mangrove sediment (2010) PLoS One, 5; Santos, H.F., Cury, J.C., Carmo, F.L., Santos, A.L., Tiedje, J., van Elsas, J.D., Rosado, A.S., Peixoto, R.S., Mangrove bacterial diversity and the impact of oil contamination revealed by pyrosequencing: bacterial proxies for oil pollution (2011) PLoS One, 6; Santos, H.F., Carmo, F.L., Duarte, G., Dini-Andreote, F., Castro, C.B., Rosado, A.S., Van Elsas, J.D., Peixoto, R.S., Climate change affects key nitrogen-fixing bacterial populations on coral reefs (2014) ISME J, 8, pp. 2272-2279; Santos, H.F., Duarte, G.A.S., Rachid, C.T.C.C., Chaloub, R.M., Calderon, E.N., Marangoni, L.F., Bianchini, A., Peixoto, R.S., Impact of oil spills on coral reefs can be reduced by bioremediation using probiotic microbiota (2015) Sci. Rep., 5; Sarma, H., Nava, A.R., Manriquez, A.M.E., Dominguez, D.C., Lee, W.-Y., Biodegradation of bisphenol A by bacterial consortia isolated directly from river sediments (2014) Environ. Technol. Innov., 14; Saunders, A.M., Albertsen, M., Vollertse, N.J., Nielsen, P.H., The activated sludge ecosystem contains a core community of abundant organisms (2016) ISME J, 10, pp. 11-20; Schleif, R.F., Wensink, P.C., Practical Methods in Molecular Biology (1981), Spring-verlag New York; Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Weber, C.F., Introducing mothur: open source, platform-independent, community-supported software for describing and comparing microbial communities (2009) App. Environ. Microbiol., 75, pp. 7537-7541; Schulster, M., Bernie, A.M., Ramasamy, R., The role of estradiol in male reproductive function (2016) Asian J. Androl., 18, pp. 435-440; Shi, J., Fujisawa, S., Nakai, S., Hosomi, M., Biodegradation of natural and synthetic estrogens by nitrifying activated sludge and ammonia-oxidizing bacterium Nitrosomonas europaea (2004) Water Res., 38, pp. 2323-2330; Sinigalliano, C.D., Kuhn, D.N., Jones, R.D., Amplification of the amoA gene from diverse species of ammonium-oxidizing bacteria and from an indigenous bacterial population from seawater (1995) Appl. Environ. Microbiol., 61, pp. 2702-2706; Song, H.L., Yangc, X.L., Xiac, M.Q., Chen, M., Co-metabolic degradation of steroid estrogens by heterotrophic bacteria and nitrifying bacteria in MBRs (2017) J. Environ. Sci. Health A, 52, pp. 778-784; Soondong, K., Kim, T., Yu, G.H., Jung, J., Park, H., Bacterial community composition and diversity of a full-scale integrated fixed-film activated sludge system as investigated by pyrosequencing (2010) J. Microbiol. Biotechnol., 20, pp. 1717-1723; Tabb, M.M., Blumberg, B., New modes of action for endocrine-disrupting chemicals (2006) Mol. Endocrinol., 20, pp. 475-482; Tamura, K., Nei, M., Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees (1993) Mol. Biol. Evol., 10, pp. 512-526; Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S., MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods (2011) Mol. Biol. Evol., 28, pp. 2731-2739; Tashiro, Y., Takemura, A., Fukii, H., Takahira, K., Nakanishi, Y., Livestock wastes as a source of estrogens and their effects on wildlife of Manko tidal flat, Okinawa (2003) Mar. Pollut. Bull., 47, pp. 143-147; Vader, J.S., van Ginkel, C.G., Sperling, F.M.G.M., Jong, J., de Boer, W., Graaf, S., van der Most, M., Stokman, P.G.W., Degradation of ethinyl estradiol by nitrifying activated sludge (2000) Chemosphere, 41, pp. 1239-1243; Vilela, C.L.S., Bassin, J.P., Peixoto, R.S., Water contamination by endocrine disruptors: impacts, microbiological aspects and trends for environmental protection (2018) Environ. Poll., 235, pp. 546-559; Villemur, R., Santos, S.C.C., Ouellette, J., Juteau, P., Lépine, F., Déziel, E., Biodegradation of endocrine disruptors in solid-liquid two-phase partitioning systems by enrichment cultures (2013) Appl. Environ. Microbiol., 79, pp. 4701-4711; Vishniac, W., Santer, M., The thiobacilli (1957) Bacteriol. Rev., 21, pp. 195-213; Wang, L.Y., Tam, N.F., Zhang, X.H., Assimilation of 17α-ethinylestradiol by sludge and its stress on microbial communities under aerobic and anaerobic conditions (2011) J. Environ. Sci. Health A, 463, pp. 242-247; Waring, R.H., Harris, R.M., Endocrine disrupters: a human risk? (2005) Mol. Cell. Endocrinol., 244, pp. 2-9; Weiland-Bräuer, N., Fischer, M.A., Schramm, K., Schmitz, R.A., Polychlorinated biphenyl (PCB)-degrading potential of microbes present in a cryoconite of Jamtalferner Glacier (2017) Front. Microbiol., 15, p. 1005; Welshons, W.V., Thayer, K.A., Judy, B.M., Taylor, J.A., Curran, E.M., vom Saal, F.S., Large effects from small exposures. I. Mechanisms for endocrine-disrupting chemicals with estrogenic activity (2003) Environ. Health Perspect., 111 (8), pp. 994-1006; Whitman, W.B., Bacteria and the fate of estrogen in the environment (2017) Cell. Chem. Biol., 22, pp. 652-653; Wood, P.M., Nitrification as a bacterial energy source (1986) Nitrification. Special Publ. Soc. Gen. Microbiol, 20, pp. 39-62. , J.I. Prosser IRL Press Oxford; Yoshimoto, T., Nagai, F., Fijimoto, J., Watanabe, K., Mizukoshi, H., Makino, T., Kimura, K., Omura, H., Degradation of estrogens by Rhodococcus zopfii and Rhodococcus equi isolates from activated sludge in wastewater treatment plants (2004) Appl. Environ. Microbiol., 70, pp. 5283-5289; Yu, C.P., Roh, H., Chu, K.H., 17b-estradiol-degrading bacteria isolated from activated sludge (2007) Environ. Sci. Technol., 41, pp. 486-492; Zhang, X., Essmann, M., Burt, E.T., Larsen, B., Estrogen effects on Candida albicans: a potential virulence-regulating mechanism (2000) J. Infect. Dis., 181, pp. 1441-1446; Zhang, T., Shao, M.-F., Ye, L., 454 Pyrosequencing reveals bacterial diversity of activated sludge from 14 sewage treatment plants (2012) ISME J, 6, pp. 1137-1147; Zhang, P., Jia, R., Zhang, Y., Shi, P., Chai, T., Quinoline-degrading strain Pseudomonas aeruginosa KDQ4 isolated from coking activated sludge is capable of the simultaneous removal of phenol in a dual substrate system (2016) J. Environ. Sci. Health A, (13), pp. 1139-1148


  • 17α-ethinylestradiol
  • Bacterial consortium
  • Bioremediation
  • Endocrine disruptors
  • Estrogen contamination
  • Bioconversion
  • Bioreactors
  • Biotechnology
  • Microorganisms
  • RNA
  • Bacterial isolation
  • Bioremediation agent
  • Fixed film reactor
  • Microbial communities
  • Microbial community dynamics
  • Non-metric multidimensional scaling
  • Synthetic estrogens
  • Sewage treatment
  • estrogen
  • ethinylestradiol
  • RNA 16S
  • estradiol derivative
  • chemical oxygen demand
  • community dynamics
  • estrogenic compound
  • gene expression
  • microbial community
  • pollutant removal
  • sewage treatment
  • Acinetobacter
  • aeration
  • amplicon
  • Article
  • bacterium culture
  • bacterium isolation
  • Bacteroidetes
  • Bdellovibrio
  • Chitinophagaceae
  • concentration (parameter)
  • controlled study
  • gene sequence
  • microbial consortium
  • Nitrosomonas
  • nonhuman
  • nucleotide sequence
  • phylum
  • population abundance
  • priority journal
  • Proteobacteria
  • Pseudomonas
  • sludge
  • animal
  • bioreactor
  • male
  • microflora
  • sewage
  • Animalia
  • Bacteria (microorganisms)
  • Animals
  • Estradiol Congeners
  • Estrogens
  • Ethinyl Estradiol
  • Male
  • Microbiota
  • RNA, Ribosomal, 16S
  • Sewage


Dive into the research topics of 'Assessing the impact of synthetic estrogen on the microbiome of aerated submerged fixed-film reactors simulating tertiary sewage treatment and isolation of estrogen-degrading consortium: Science of the Total Environment'. Together they form a unique fingerprint.

Cite this