Biodegradation of 17 β-estradiol by Serratia marcescens and Stenotrophomonas tumulicola co-culture isolated from a sewage treatment plant in Upper Egypt
-
Ibrahim Mahmoud Ali
,
Hamada Mohamed Mohamed Halby
,
Bahaa-Eldin Anwar Abd-Elrady
,
Mohamed Taha Salim
,
Heba Ahmed Mohamed
Abstract
Background and Objectives: 17 β- estradiol (E2) is an important pollutant of the aquatic system. It is responsible for sexual disruptions in the majority of aquatic organisms. This study aimed to search for bacteria with high potential degradation of E2 as an important method for bioremediation.
Materials and Methods: Sewage water samples were collected and treated to isolate bacterial strains which were identified by conventional methods and 16S ribosomal RNA gene sequence analysis. The biodegradation of E2 by the isolated strains was evaluated under different environmental conditions.
Results: Two bacterial strains were recovered from sewage water samples and identified as Stenotrophomonas tumulicola and Serratia marcescens, (named ASc2 and ASc5 respectively). Co-culture of the two strains showed biodegradation of approximately 93.6% of E2 (50 mg. L-1) within 48 hours. However, the biodegradation capacity of the same E2 concentration was 69.4% and 71.2% for ASc2 and ASc5 each alone, respectively. The optimum cultivation conditions for efficient E2 biodegradation by co-culture were 5% (v/v) inoculation volume with 50 mg. L-1 of E2 as the initial concentration at pH 7 and 30°C within 48 hours inoculation period.
Conclusion: This study detected new bacterial strains that are capable of rapid degradation of estrogen as an environmental pollutant.
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18. Byers HK, Stackebrandt E, Hayward C, Blackall LL. Molecular investigation of a microbial mat associated with the great artesian basin. FEMS Microbiol Ecol 1998; 25: 391-403.
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21. 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.
22. Jiang L, Yang J, Chen J. Isolation and characteristics of 17β-estradiol-degrading Bacillus spp. strains from activated sludge. Biodegradation 2010; 21: 729-736.
23. Khattab R, Elnwishy N, Hannora A, Mattiasson B, Omran H, Alharbi O, et al. Biodegradation of 17-β-estradiol in water. Int J Environ Sci Technol 2019; 16: 4935-4944.
24. Urszula G, Izabela G, Danuta W, Sylwia Ł. Isolation and characterization of a novel strain of Stenotrophomonas maltophilia possessing various dioxygenases for monocyclic hydrocarbon degradation. Braz J Microbiol 2009; 40: 285-291.
25. Li Z, Nandakumar R, Madayiputhiya N, Li X. Proteomic analysis of 17β-estradiol degradation by Stenotrophomonas maltophilia. Environ Sci Technol 2012; 46: 5947-5955.
26. Xiong W, Yin C, Wang Y, Lin S, Deng Z, Liang R. Characterization of an efficient estrogen-degrading bacterium Stenotrophomonas maltophilia SJTH1 in saline-, alkaline-, heavy metal-contained environments or solid soil and identification of four 17β-estradiol-oxidizing dehydrogenases. J Hazard Mater 2020; 385: 121616.
27. Xiong W, Yin C, Peng W, Deng Z, Lin S, Liang R. Characterization of a 17 β-estradiol-degrading bacterium Stenotrophomonas maltophilia SJTL3 tolerant to adverse environmental factors. Appl Microbiol Biotechnol 2020; 104: 1291-1305.
28. Gupta A, Thakur IS. Biodegradation of wastewater organic contaminants using Serratia sp. ISTVKR1 isolated from sewage sludge. Biochem Eng J 2015; 102: 115-124.
29. Zhao X, Wang Y, Xu X, Tian K, Zhou D, Meng F, et al. Genomics analysis of the steroid estrogen-degrading bacterium Serratia nematodiphila DH-S01. Biotechnol Biotechnol Equip 2020; 34: 430-440.
30. Li M, Zhao X, Zhang X, Wu D, Leng S. Biodegradation of 17β-estradiol by bacterial co-culture isolated from manure. Sci Rep 2018; 8: 3787.
31. Tian K, Meng F, Meng Q, Gao Y, Zhang L, Wang L, et al. The analysis of estrogen-degrading and functional metabolism genes in Rhodococcus equi DSSKP-R-001. Int J Genomics 2020; 2020: 9369182.
32. AlAhadeb JI. Effective biodeterioration of a common endocrine disruptor 17β-estradiol using mixed microbial cultures isolated from waste water. Environ Res 2022; 206: 112559.
33. Liu J, Liu J, Xu D, Ling W, Li S, Chen M. Isolation, immobilization, and degradation performance of the 17β-estradiol-degrading bacterium Rhodococcus sp. JX-2. Water Air Soil Pollut 2016; 227: 422.
34. Wu S, Hao P, Gou C, Zhang X, Wang L, Basang W, et al. Lysinibacillus sp. GG242 from cattle slurries degrades 17β-estradiol and possible 2 transformation routes. Microorganisms 2022; 10: 1745.
35. Ge H, Yang L, Li B, Feng Y, Wang S, Zheng Y, et al. A comparative study on the biodegradation of 17β-estradiol by Candida utilis CU-2 and Lactobacillus casei LC-1. Front Energy Res 2021; 9: 10.3389/fenrg.2021.661850.
36. Li S, Liu J, Sun K, Yang Z, Ling W. Degradation of 17β-estradiol by Novosphingobium sp. ES2-1 in an aqueous solution contaminated with tetracyclines. Environ Pollut 2020; 260: 114063.
37. Yu Q, Wang P, Liu D, Gao R, Shao H, Zhao H, et al. Degradation characteristics and metabolic pathway of 17β-estradiol (E2) by Rhodococcus sp. DS201. Biotechnol Bioprocess Eng 2016; 21: 804-813.
2. Jobling S, Williams R, Johnson A, Taylor A, Gross-Sorokin M, Nolan M, et al. Predicted exposures to steroid estrogens in UK rivers correlate with widespread sexual disruption in wild fish populations. Environ Health Perspect 2006; 114(Suppl 1): 32-39.
3. Li Y, Sun Y, Zhang H, Wang L, Zhang W, Niu L, et al. The responses of bacterial community and N2O emission to nitrogen input in lake sediment: estrogen as a co-pollutant. Environ Res 2019; 179: 108769.
4. Sacdal R, Madriaga J, Espino MP. Overview of the analysis, occurrence, and ecological effects of hormones in lake waters in Asia. Environ Res 2020; 182: 109091.
5. Peiris C, Nawalage S, Wewalwela JJ, Gunatilake SR, Vithanage M. Biochar based sorptive remediation of steroidal estrogen contaminated aqueous systems: A critical review. Environ Res 2020; 191: 110183.
6. Nakada N, Nyunoya H, Nakamura M, Hara A, Iguchi T, Takada H. Identification of estrogenic compounds in wastewater effluent. Environ Toxicol Chem 2004; 23: 2807-2815.
7. Fan Z, Casey FX, Hakk H, Larsen GL. Persistence and the fate of 17β-estradiol and testosterone in agricultural soils. Chemosphere 2007; 67: 886-895.
8. 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.
9. González A, Kroll KJ, Silva-Sanchez C, Carriquiriborde P, Fernandino JI, Denslow ND, et al. Steroid hormones and estrogenic activity in the wastewater outfall and receiving waters of the Chascomús chained shallow lakes system (Argentina). Sci Total Environ 2020; 743: 140401.
10. Kirk LA, Tyler CR, Lye CM, Sumpter JP. Changes in estrogenic and androgenic activities at different stages of treatment in wastewater treatment works. Environ Toxi Chem 2002; 21: 972-979.
11. Hamid H, Eskicioglu C. Fate of estrogenic hormones in wastewater and sludge treatment: A review of properties and analytical detection techniques in sludge matrix. Water Res 2012; 46: 5813-5833.
12. Ting YF, Praveena SM. Sources, mechanisms, and fate of steroid estrogens in wastewater treatment plants: a mini-review. Environ Monit Assess 2017; 189: 178.
13. D'ascenzo G, Di Corcia A, Gentili A, Mancini R, Mastropasqua R, Nazzari M, et al. The Fate of natural estrogen conjugates in municipal sewage transport and treatment facilities. Sci Total Environ 2003; 302: 199-209.
14. Snyder SA, Adham S, Redding AM, Cannon FS, DeCarolis J, Oppenheimer J, et al. Role of membranes and activated carbon in the removal of endocrine disruptors and pharmaceuticals. Desalination 2007; 202: 156-181.
15. Whidbey CM, Daumit KE, Nguyen T-H, Ashworth DD, Davis JC, Latch DE. Photochemical-induced changes of in vitro estrogenic activity of steroid hormones. Water Res 2012; 46: 5287-5296.
16. Yu C-P, Deeb RA, Chu K-H. Microbial degradation of steroidal estrogens. Chemosphere 2013; 91: 1225-1235.
17. Li S, Liu J, Sun M, Ling W, Zhu X. Isolation, characterization, and degradation performance of the 17β-estradiol-degrading bacterium Novosphingobium sp. E2S. Int J Environ Res Public Health 2017; 14: 115.
18. Byers HK, Stackebrandt E, Hayward C, Blackall LL. Molecular investigation of a microbial mat associated with the great artesian basin. FEMS Microbiol Ecol 1998; 25: 391-403.
19. Xu R-F, Sun M-X, Liu J, Wang H, Li X, Zhu X-Z, et al. Isolation, identification and characterization of a diethylstilbestrol-degrading bacterial strain Serratia sp. Huan Jing Ke Xue 2014; 35: 3169-3174.
20. Wojnarowski K, Podobiński P, Cholewińska P, Smoliński J, Dorobisz K. Impact of estrogens present in environment on health and welfare of animals. Animals (Basel) 2021; 11: 2152.
21. 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.
22. Jiang L, Yang J, Chen J. Isolation and characteristics of 17β-estradiol-degrading Bacillus spp. strains from activated sludge. Biodegradation 2010; 21: 729-736.
23. Khattab R, Elnwishy N, Hannora A, Mattiasson B, Omran H, Alharbi O, et al. Biodegradation of 17-β-estradiol in water. Int J Environ Sci Technol 2019; 16: 4935-4944.
24. Urszula G, Izabela G, Danuta W, Sylwia Ł. Isolation and characterization of a novel strain of Stenotrophomonas maltophilia possessing various dioxygenases for monocyclic hydrocarbon degradation. Braz J Microbiol 2009; 40: 285-291.
25. Li Z, Nandakumar R, Madayiputhiya N, Li X. Proteomic analysis of 17β-estradiol degradation by Stenotrophomonas maltophilia. Environ Sci Technol 2012; 46: 5947-5955.
26. Xiong W, Yin C, Wang Y, Lin S, Deng Z, Liang R. Characterization of an efficient estrogen-degrading bacterium Stenotrophomonas maltophilia SJTH1 in saline-, alkaline-, heavy metal-contained environments or solid soil and identification of four 17β-estradiol-oxidizing dehydrogenases. J Hazard Mater 2020; 385: 121616.
27. Xiong W, Yin C, Peng W, Deng Z, Lin S, Liang R. Characterization of a 17 β-estradiol-degrading bacterium Stenotrophomonas maltophilia SJTL3 tolerant to adverse environmental factors. Appl Microbiol Biotechnol 2020; 104: 1291-1305.
28. Gupta A, Thakur IS. Biodegradation of wastewater organic contaminants using Serratia sp. ISTVKR1 isolated from sewage sludge. Biochem Eng J 2015; 102: 115-124.
29. Zhao X, Wang Y, Xu X, Tian K, Zhou D, Meng F, et al. Genomics analysis of the steroid estrogen-degrading bacterium Serratia nematodiphila DH-S01. Biotechnol Biotechnol Equip 2020; 34: 430-440.
30. Li M, Zhao X, Zhang X, Wu D, Leng S. Biodegradation of 17β-estradiol by bacterial co-culture isolated from manure. Sci Rep 2018; 8: 3787.
31. Tian K, Meng F, Meng Q, Gao Y, Zhang L, Wang L, et al. The analysis of estrogen-degrading and functional metabolism genes in Rhodococcus equi DSSKP-R-001. Int J Genomics 2020; 2020: 9369182.
32. AlAhadeb JI. Effective biodeterioration of a common endocrine disruptor 17β-estradiol using mixed microbial cultures isolated from waste water. Environ Res 2022; 206: 112559.
33. Liu J, Liu J, Xu D, Ling W, Li S, Chen M. Isolation, immobilization, and degradation performance of the 17β-estradiol-degrading bacterium Rhodococcus sp. JX-2. Water Air Soil Pollut 2016; 227: 422.
34. Wu S, Hao P, Gou C, Zhang X, Wang L, Basang W, et al. Lysinibacillus sp. GG242 from cattle slurries degrades 17β-estradiol and possible 2 transformation routes. Microorganisms 2022; 10: 1745.
35. Ge H, Yang L, Li B, Feng Y, Wang S, Zheng Y, et al. A comparative study on the biodegradation of 17β-estradiol by Candida utilis CU-2 and Lactobacillus casei LC-1. Front Energy Res 2021; 9: 10.3389/fenrg.2021.661850.
36. Li S, Liu J, Sun K, Yang Z, Ling W. Degradation of 17β-estradiol by Novosphingobium sp. ES2-1 in an aqueous solution contaminated with tetracyclines. Environ Pollut 2020; 260: 114063.
37. Yu Q, Wang P, Liu D, Gao R, Shao H, Zhao H, et al. Degradation characteristics and metabolic pathway of 17β-estradiol (E2) by Rhodococcus sp. DS201. Biotechnol Bioprocess Eng 2016; 21: 804-813.
| Files | ||
| Issue | Vol 15 No 3 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i3.12906 | |
| Keywords | ||
| 17 β-estradiol (E2); Biodegradation; Serratia marcescens; Sewage; Stenotrophomonas tumulicola | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Mahmoud Ali I, Mohamed Mohamed Halby H, Anwar Abd-Elrady B-E, Salim MT, Mohamed H. Biodegradation of 17 β-estradiol by Serratia marcescens and Stenotrophomonas tumulicola co-culture isolated from a sewage treatment plant in Upper Egypt. Iran J Microbiol. 2023;15(3):448-455.
