Microbial degradation of steroidal estrogens

Chemosphere

Volumn 91, Issue 9, 2013, Pages 1225-1235

  Yu, Chang Ping ^a   Deeb, Rula A ^b   Chu, Kung Hui ^c  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b ARCADIS US Inc   (United States)

^c Texas AandM University   (United States)

Author keywords

Biodegradation; Estrogen; Kinetics; Pathways; Review

Indexed keywords

ENZYME KINETICS; MICROORGANISMS; REVIEWS;

BIODEGRADATION KINETICS; DIFFERENT OPERATING CONDITIONS; ENVIRONMENTAL OCCURRENCE; ESTROGEN; MICROBIAL BIODEGRADATION; MICROBIAL COMMUNITIES; MICROBIAL DEGRADATION; PATHWAYS;

BIODEGRADATION;

ESTROGEN;

ACTIVATED SLUDGE; ANOXIC CONDITIONS; BIODEGRADATION; BIOREACTOR; ESTROGENIC COMPOUND; FUTURE PROSPECT; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; MOLECULAR ANALYSIS; PHYLOGENETICS; REACTION KINETICS; RESEARCH WORK; STEROID; TRACKING;

AEROBIC BACTERIUM; BACTERIAL GROWTH; CHEMICAL REACTION; COMPOST; KINETICS; MICROBIAL COMMUNITY; MICROBIAL DEGRADATION; NONHUMAN; PHYLOGENY; REVIEW; SEA; SLUDGE; SOIL; TOOTH PLAQUE;

EID: 84876453141     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2013.01.112     Document Type: Review

References (93)

1. Andersen H., Siegrist H., Halling-Srensen B., Ternes T.A. Fate of estrogens in a municipal sewage treatment plant. Environ. Sci. Technol. 2003, 37:4021.
2. Atkinson S., Atkinson M.J., Tarrant A.M. Estrogens from sewage in coastal marine environments. Environ. Health Persp. 2003, 111:531-535.
3. Auriol M., Filali-Meknassi Y., Adams C.D., Tyagi R.D., Noguerol T.-N., Piña B. Removal of estrogenic activity of natural and synthetic hormones from a municipal wastewater: efficiency of horseradish peroxidase and laccase from Trametes versicolo. Chemosphere 2008, 70:445-452.
4. Auriol M., Filali-Meknassia Y., Adams C.D., Tyagi R.D. Natural and synthetic hormone removal using the horseradish peroxidase enzyme: temperature and pH effects. Water Res. 2006, 40:2847-2856.
5. Auriol M., Filali-Meknassia Y., Tyagi R.D., Adams C.D. Laccase-catalyzed conversion of natural and synthetic hormones from a municipal wastewater. Water Res. 2007, 41:3281-3288.
6. Baronti C., Curini R., D'Ascenzo G., Di Corcia A., Gentili A., Samperi R. Monitoring natural and syntheticestrogens at activated sludge sewage treatment plants and in a receiving river water. Environ. Sci. Technol. 2000, 34:5059-5066.
7. Bjerregaard L., Madsen A., Korsgaard B., Bjerregaard P. Gonad histology and vitellogenin concentrations in brown trout (Salmo trutta) from Danish streams impacted by sewage effluent. Ecotoxicology 2006, 15:315-327.
8. Blánquez P., Guieyssea B. Continuous biodegradation of 17β-estradiol and 17α-ethynylestradiol by Trametes versicolor. J. Hazard. Mater. 2008, 150:459-462.
9. Chu, K.H., 2010. Biodegradation and treatment potentials of estrogens invited presentation at symposium 221/division Q: microbial biodegradation of environmental endocrine disrupting compounds. The 110th General Meeting of American Society for Microbiology. San Diego, CA. May 23-27, 2010.
10. Cody R.P., Bortone S.A. Masculinization of mosquitofish as an indicator of exposure to kraft mill effluent. B. Environ. Contam. Toxicol. 1997, 58:429-436.
11. Combalbert S., Hernandez-Raquet G. Occurrence, fate, and biodegradation of estrogens in sewage and manure. Appl. Microbiol. Biotechnol. 2010, 86:1671-1692.
12. Coombe R.G., Tsong Y.Y., Hamilton P.B., Sih C.J. Mechanisms of steroid oxidation by microorganisms. J. Biol. Chem. 1966, 241:1587-1595.
13. Czajka C.P., Londry K.L. Anaerobic biotransformation of estrogens. Sci. Total Environ. 2006, 367:932-941.
14. Della Greca M., Pinto G., Pistillo P., Pollio A., Previtera L., Temussi F. Biotransformation of ethinylestradiol by microalgae. Chemosphere 2008, 70:2047-2053.
15. Drewes J., Hemming J., Ladenburger S.J., Schauer J., Sonzogni W. An assessment of endocrine disrupting activity changes during wastewater treatment through the use of bioassays and chemical measurements. Water Environ. Res. 2005, 77:12-23.
16. Dubroca J., Collignon N., Brault A., Hernandez-Raquet G., Patureau D., Mougin C. Fate of 17β-estradiol in terrestrial model ecosystems amended with contaminated composted biosolids. Environ. Chem. Lett. 2009, 7:369-373.
17. Esplugas S., Bila D.M., Krause L.G.T., Dezotti M. Ozonation and advanced oxidation technologies to remove endocrine disrupting chemicals (EDCs) and pharmaceuticals and personal care products (PPCPs) in water effluents. J. Hazard. Mater. 2007, 149:631-642.
18. Fahrbach M., Kuever J., Meinke R., Kampfer P., Hollender J. Denitratisoma oestradiolicum gen. nov., sp. nov., a 17β-oestradiol-degrading, denitrifying betaproteobacterium. Int. J. Syst. Evol. Microbiol. 2006, 56:1547-1552.
19. 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. Int. J. Syst. Evol. Micorbiol. 2008, 58:2215-2223.
20. Fan Z., Casey F.X.M., Hakk H., Larsen G.L. Persistence and fate of 17β-estradiol and testosterone in agricultural soils. Chemosphere 2007, 67:886-895.
21. Fine D.D., Breidenbach G.P., Price T.L., Hutchins S.R. Quantitation of estrogens in ground water and swine lagoon samples using solid-phase extraction, pentafluorobenzyl/trimethylsilyl derivatizations and gas chromatography-negative ion chemical ionization tandem mass spectrometry. J. Chromatogr. A 2003, 1017:167-185.
22. Folmar L.C., Denslow N.D., Rao V., Chow M., Crain D.A., Enblom J., Marcino J., Guillette L.J. Vitellogenin induction and reduced serum testosterone concentrations in feral male carp (Cyprinus carpio) captured near a major metropolitan sewage treatment plant. Environ. Health Persp. 1996, 104:1096-1101.
23. Fujii K., Kikuchi S., Satomi M., Ushio-Sata N., Morita N. Degradation of 17β-estradiol by a Gram-negative bacterium isolated from activated sludge in a sewage treatment plant in Tokyo. Japan. Appl. Environ. Microbiol. 2002, 68:2057-2060.
24. Gaulke L.S., Strand S.E., Kalhorn T.F., Stensel H.D. 17α-ethinylestradiol transformation via abiotic nitration in the presence of ammonia oxidizing bacteria. Environ. Sci. Technol. 2008, 42:7622-7627.
25. Hashimoto S., Bessho H., Hara A., Nakamura M., Iguchi T., Fujita K. Elevated serum vitellogenin levels and gonadal abnormalities in wild male flounder (Pleuronectes yokohamae) from Tokyo Bay. Japan. Mar. Environ. Res. 2000, 49:37-53.
26. Hashimoto, T., Onda, K., Morita, T., Luxmy, B.S., Tada, K., Miya, A., Murakami, T., 2010. Contribution of the estrogen-degrading bacterium Novosphingobium sp. strain JEM-1 to estrogen removal in wastewater treatment. J. Environ. Eng. - ASCE 136, 890-896.
27. Hu A., He J., Chu K.H., Yu C.-P. Genome sequence of a 17β-estradiol-utilizing bacterium Sphingomonas strain KC8. J. Bacteriol. 2011, 193:4266-4267.
28. 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. Environ. Sci. Technol. 2007, 41:738-744.
29. Ivanov V., Lim J.J.-W., Stabnikova O., Gin K.Y.-H. Biodegradation of estrogens by facultative anaerobic iron-reducing bacteria. Process Biochem. 2010, 45:284-287.
30. Jarvenpaa P., Kosunen T., Fotsis T., Adlercreutz H. Invitro metabolism of estrogens by isolated intestinal microorganisms and by human fecal microflora. J. Steroid Biochem. 1980, 13:345-349.
31. Jiang L., Yang J., Chen J. Isolation and characteristics of 17β-estradiol-degrading Bacillus spp. strains from activated sludge. Biodegradation 2010, 21:729-736.
32. Jobling S., Nolan M., Tyler C.R., Brighty G., Sumpter J.P. Widespread sexual disruption in wild fish. Environ. Sci. Technol. 1998, 32:2498-2506.
33. Johnson A.C., Sumpter J.P. Removal of endocrine-disrupting chemicals in activated sludge treatment works. Environ. Sci. Technol. 2001, 35:4697-4703.
34. Jürgens M.D., Holthaus K.I.E., Johnson A.C., Smith J.J.L., Hetheridge M., Williams R.J. The potential for estradiol and ethinylestradiol degradation in English rivers. Environ. Toxicol. Chem. 2002, 21:480-488.
35. Ke J.X., Zhuang W.Q., 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. Appl. Microbiol. Biotechnol. 2007, 75:1163-1171.
36. Khanal S.K., Xie B., Thompson M.L., Sung S., Ong S.K., Van Leeuwent J. Fate, transport, and biodegradation of natural estrogens in the environment and engineered systems. Environ. Sci. Technol. 2006, 40:6537-6546.
37. Kirk L.A., Tyler C.R., Lye C.M., Sumpter J.P. Changes in estrogenic and androgenic activities at different stages of treatment in wastewater treatment works. Environ. Toxicol. Chem. 2002, 21:972-979.
38. Koh Y.K., Chiu T.Y., Boobis A., Cartmell E., Scrimshaw M.D., Lester J.N. Treatment and removal strategies for estrogens from wastewater. Environ. Technol. 2008, 29:245-267.
39. Kornman K.S., Loesche W.J. Effects of estradiol and progesterone on Bacteroides melaninogenicus and Bacteroides gingivalis. Infect. Immun. 1982, 35:256-263.
40. Kurisu F., Ogura M., Saitoh S., Yamazoe A., Yagi O. Degradation of natural estrogen and identification of the metabolites produced by soil isolates of Rhodococcus sp. and Sphingomonas sp. J. Biosci. Bioeng. 2010, 109:576-582.
41. Layton A.C., Gregory B.W., Seward J.R., Schultz T.W., Sayler G.S. Mineralization of steroidal hormones by biosolids in wastewater treatment systems in Tennessee USA. Environ. Sci. Technol. 2000, 34:3925-3931.
42. Lee H.B., Liu D. Degradation of 17β-estradiol and its metabolites by sewage bacteria. Water Air Soil Pollut. 2002, 134:353-368.
43. Li C.-R., Lee S.-H., Kim S.-S., Kim A., Lee K., Lu M., Kim H.-E., Kwak I.-J., Lee Y.-J., Kim D.-K., Lee J.-S., Kang S.-W., Huh M.-D., Chung K.-H., Park J.-S. Environmental estrogenic effects and gonadal development in wild goldfish (Carassius auratus). Environ. Monit. Assess. 2009, 150:397-404.
44. Li Z., Nandakumar R., Madayiputhiya N., Li X. Proteomic analysis of 17β-estradiol degradation by Stenotrophomonas maltophilia. Environ. Sci. Technol. 2012, 46:5947-5955.
45. Liang R., Liu H., Tao F., Liu Y., Ma C., Liu X., Liu J. Genome sequence of Pseudomonas putida strain SJTE-1, a bacterium capable of degrading estrogens and persistent organic pollutants. J. Bacteriol. 2012, 194:4781-4782.
46. Liu Z.-H., Ito M., Kanjo Y., Yamamoto A. Profile and removal of endocrine disrupting chemicals by using an ER/AR competitive ligand binding assay and chemical analyses. J. Environ. Sci. 2009, 21:900-906.
47. Liu Z.-H., Kanjo Y., Mizutani S. Removal mechanisms for endocrine disrupting compounds (EDCs) in wastewater treatment - physical means, biodegradation, and chemical advanced oxidation: a review. Sci. Total Environ. 2009, 407:731-748.
48. Liu Z.-H., Kanjo Y., Mizutani S. Urinary excretion rates of natural estrogens and androgens from humans, and their occurrence and fate in the environment: a review. Sci. Total Environ. 2009, 407:4975-4985.
49. Matsui S., Takigami H., Matsuda T., Taniguchi N., Adachi J., Kawami H., Shimizu Y. Estrogen and estrogen mimics contamination in water and the role of sewage treatment. Water Sci. Technol. 2000, 42(12):173-179.
50. Matsuoka S., Kikuchi M., Kimura S., Kurokawa Y., Kawai S. Determination of estrogenic substances in the water of Muko River using in vitro assays, and the degradation of natural estrogens by aquatic bacteria. J. Health Sci. 2005, 51:178-184.
51. Muller M., Patureau D., Godon J.J., Delgenes J.P., Hernandez-Raquet G. Molecular and kinetic characterization of mixed cultures degrading natural and synthetic estrogens. Appl. Microbiol. Biotechnol. 2010, 85:691-701.
52. Nakai S., Yamamura A., Tanaka S., Shi J., Nishikawa M., Nakashimada Y., Hosomi M. Pathway of 17β-estradiol degradation by Nitrosomonas europaea and reduction in 17β-estradiol-derived estrogenic activity. Environ. Chem. Lett. 2011, 9:1-6.
53. O'Grady D., Evangelista S., Yargeau V. Removal of aqueous 17α-ethinylestradiol by Rhodococcus species. Environ. Eng. Sci. 2009, 26:1393-1400.
54. Ojanotkoharri A., Laine M., Tenovuo J. Metabolism of 17β-estradiol by oral Streptococcus mutans, Streptococcus sanguis, Bacillus cereus and Candida albicans. Oral Microbiol. Immun. 1991, 6:126-128.
55. Pauwels B., Wille K., Noppe H., De Brabander H., Van de Wiele T., Verstraete W., Boon N. 17α-ethinylestradiol cometabolism by bacteria degrading estrone, 17β-estradiol and estriol. Biodegradation 2008, 19:683-693.
56. Payne D.W., Talalay P. Isolation of novel microbial 3α-, 3β-, and 17β-hydroxysteroid dehydrogenases. Purification, characterization, and analytical applications of a 17β-hydroxysteroid dehydrogenase from an Alcaligenes sp. J. Biol. Chem. 1985, 260:13648-13655.
57. Racz L., Goel R.K. Fate and removal of estrogens in municipal wastewater. J. Environ. Monit. 2010, 12:58-70.
58. Ren H., Ji S., Ahmad N.u.d., Wang D., Cui C. Degradation characteristics and metabolic pathway of 17α-ethynylestradiol by Sphingobacterium sp. JCR5. Chemosphere 2007, 66:340-346.
59. Roh H., Chu K.H. A 17β-estradiol-utilizing bacterium, Sphingomonas strain KC8: Part I - characterization and abundance in wastewater treatment plants. Environ. Sci. Technol. 2010, 44:4943-4950.
60. Roh H., Chu K.H. Effects of solids retention time on the performance of bioreactors bioaugmented with a 17β-estradiol-utilizing bacterium, Sphingomonas strain KC8. Chemosphere 2011, 84:227-233.
61. 15N-stable isotope probing. Environ. Sci. Technol. 2009, 43:2505-2511.
62. Sabirova J.S., Cloetens L.F.F., Vanhaecke L., Forrez I., Verstraete W., Boon N. Manganese-oxidizing bacteria mediate the degradation of 17α-ethinylestradiol. Microbiol. Biotechnol. 2008, 1:507-512.
63. Sang Y., Xiong G., Maser E. Identification of a new steroid degrading bacterial strain H5 from the Baltic Sea and isolation of two estradiol inducible genes. J. Steroid Biochem. 2012, 129:22-30.
64. Shappell N.W., Billey L.O., Forbes D., Matheny T.A., Poach M.E., Reddy G.B., Hunt P.G. Estrogenic activity and steroid hormones in swine wastewater through a lagoon constructed-wetland system. Environ. Sci. Technol. 2006, 41:444-450.
65. Shi J.H., Suzuki Y., Lee B.D., Nakai S., Hosomi M. Isolation and characterization of the ethynylestradiol-biodegrading microorganism Fusarium proliferatum strain HNS-1. Water Sci. Technol. 2002, 45(12):175-179.
66. Skotnicka-Pitak J., Khunjar W.O., Love N.G., Aga D.S. Characterization of metabolites formed during the biotransformation of 17α-ethinylestradiol by Nitrosomonas europaea in batch and continuous flow bioreactors. Environ. Sci. Technol. 2009, 43:3549-3555.
67. Song H.-L., Nakano K., Taniguchi T., Nomura M., Nishimura O. Estrogen removal from treated municipal effluent in small-scale constructed wetland with different depth. Bioresource Technol. 2009, 100:2945-2951.
68. Sumpter J.P., Jobling S. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ. Health Persp. 1995, 103:173-178.
69. Sumpter J.P., Johnson A.C. 10th Anniversary perspective: reflections on endocrine disruption in the aquatic environment: from known knowns to unknown unknowns (and many things in between). J. Environ. Monit. 2008, 10:1476-1485.
70. Suzuki K., Hirai H., Murata H., Nishida T. Removal of estrogenic activities of 17β-estradiol and ethinylestradiol by ligninolytic enzymes from white rot fungi. Water Res. 2003, 37:1972-1975.
71. Tanaka T., Tonosaki T., Nose M., Tomidokoro N., Kadomura N., Fujii T., Taniguchi M. Treatment of model soils contaminated with phenolic endocrine-disrupting chemicals with laccase from Trametes sp in a rotating reactor. J. Biosci. Bioeng. 2001, 92:312-316.
72. Ternes T.A., Kreckel P., Mueller J. Behaviour and occurrence of estrogens in municipal sewage treatment plants - II. Aerobic batch experiments with activated sludge. Sci. Total Environ. 1999, 225:91-99.
73. Tyler C.R., Jobling S., Sumpter J.P. Endocrine disruption in wildlife: a critical review of the evidence. Crit. Rev. Toxicol. 1998, 28:319-361.
74. Vader J.S., van Ginkel C.G., Sperling F.M.G.M., de Jong J., de Boer W., de Graaf J.S., van der Most M., Stokman P.G.W. Degradation of ethinyl estradiol by nitrifying activated sludge. Chemosphere 2000, 41:1239-1243.
75. Vajda A.M., Barber L.B., Gray J.L., Lopez E.M., Woodling J.D., Norris D.O. Reproductive disruption in fish downstream from an estrogenic wastewater effluent. Environ. Sci. Technol. 2008, 42:3407-3414.
76. Vos J.G., Dybing E., Greim H.A., Ladefoged O., Lambré C., Tarazona J.V., Brandt I., Vethaak A.D. Health effects of endocrine-disrupting chemicals on wildlife, with special reference to the European situation. Crit. Rev. Toxicol. 2000, 30:71-133.
77. Vulliet E., Cren-Olivé C., Grenier-Loustalot M.-F. Occurrence of pharmaceuticals and hormones in drinking water treated from surface waters. Environ. Chem. Lett. 2011, 9:103-114.
78. Weber S., Leuschner P., Kämpfer P., Dott W., Hollender J. Degradation of estradiol and ethinyl estradiol by activated sludge and by a defined mixed culture. Appl. Microbiol. Biotechnol. 2005, 67:106-112.
79. Writer J.H., Ryan J.N., Keefe S.H., Barber L.B. Fate of 4-nonylphenol and 17β-estradiol in the Redwood River of Minnesota. Environ. Sci. Technol. 2012, 46:860-868.
80. Xuan R., Blassengale A.A., Wang Q. Degradation of estrogenic hormones in a silt loam soil. J. Agr. Food Chem. 2008, 56:9152-9158.
81. Yi T., Harper W.F. The link between nitrification and biotransformation of 17α-ethinylestradiol. Environ. Sci. Technol. 2007, 41:4311.
82. Ying G.G., Kookana R.S. Degradation of five selected endocrine-disrupting chemicals in seawater and marine sediment. Environ. Sci. Technol. 2003, 37:1256-1260.
83. Ying G.G., Kookana R.S., Dillon P. Sorption and degradation of selected five endocrine disrupting chemicals in aquifer material. Water Res. 2003, 37:3785-3791.
84. Yoshimoto T., Nagai F., Fujimoto J., Watanabe K., Mizukoshi H., Makino T., Kimura K., Saino H., Sawada H., Omura H. Degradation of estrogens by Rhodococcus zopfii and Rhodococcus equi isolates from activated sludge in wastewater treatment plants. Appl. Environ. Microbiol. 2004, 70:5283-5289.
85. Yu C.-P., Ahuja R., Sayler G., Chu K.H. Quantitative molecular assay for fingerprinting microbial communities of wastewater and estrogen-degrading consortia. Appl. Environ. Microbiol. 2005, 71:1433-1444.
86. Yu C.-P., Chu K.H. A quantitative assay for linking microbial community function and structure of a naphthalene-degrading microbial consortium. Environ. Sci. Technol. 2005, 39:9611-9619.
87. Yu C.-P., Chu K.H. Occurrence of pharmaceuticals and personal care products along the West Prong Little Pigeon River in east Tennessee, USA. Chemosphere 2009, 75:1281-1286.
88. Yu C.-P., Roh H., Chu K.H. 17β-Estradiol-degrading bacteria isolated from activated sludge. Environ. Sci. Technol. 2007, 41:486-492.
89. Zang K., Kurisu F., Kasuga I., Furumai H., Yagi O. Analysis of the phylogenetic diversity of estrone-degrading bacteria in activated sewage sludge using microautoradiography-fluorescence in situ hybridization. Syst. Appl. Microbiol. 2008, 31:206-214.
90. Zeng Q., Li Y., Gu G. Nitrate-dependent degradation of 17α-ethinylestradiol by acclimated activated sludge under anaerobic conditions. J. Chem. Technol. Biotechnol. 2009, 84:1841-1847.
91. Zeng Q., Li Y.M., Gu G.W., Zhao J.M., Zhang C.J., Luan J.F. Sorption and biodegradation of 17β-estradiol by acclimated aerobic activated sludge and isolation of the bacterial strain. Environ. Eng. Sci. 2009, 26:783-790.
92. Zhang T., Xiong G., Maser E. Characterization of the steroid degrading bacterium S19-1 from the Baltic Sea at Kiel. Germany. Chem. - Biol. Interact. 2011, 191:83-88.
93. Zheng W., Yates S.R., Bradford S.A. Analysis of steroid hormones in a typical dairy waste disposal system. Environ. Sci. Technol. 2007, 42:530-535.