Skip to main content
SpringerLink
Log in

Isolation and characterization of a new highly effective 17β-estradiol-degrading Gordonia sp. strain R9

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

In this report, Gordonia sp. strain R9 isolated from an enrichment culture of chicken leachate was confirmed to degrade 17β-estradiol (E2), which can also use other estrogens (estrone, estriol, and 17α-ethynylestradiol) and testosterone as sole carbon and energy sources. Optimization of growth conditions showed that Gordonia sp. strain R9 can tolerate a very wide range of temperature (4–40 °C) and pH (1.0–11.0), and is sensitive to antibiotics including kanamycin, ampicillin, chloramphenicol, and carbenicillin. Optimal culture conditions for E2 degradation were 30 °C and pH 7.0 with almost 100% degradation of E2 concentrations ranging from 50 µg/L to 5 mg/L within 24 h. The E2 intermediates so generated included estrone (E1), estratriol (E3), (3Z)-3-(3-hydroxy-3a-methyl-7-oxododecahydro-6H-cyclopenta[a]naphthalen-6-ylidene) propanoic acid and 3-hydroxy-3a-methyl-7-oxododecahydro-1H-cyclopenta[a]naphthalene-6-carboxylic acid. These results indicate that the highly effective E2-degradative ability of Gordonia sp. strain R9 merits further investigation as a candidate for large-scale estrogen biodegradation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Arenskötter M, Bröker D, Steinbüchel A (2004) Biology of the metabolically diverse genus Gordonia. Appl Environ Microbiol 70:3195–3204

    PubMed  PubMed Central  Google Scholar 

  • Bartelt-Hunt S, Snow DD, Damon-Powell T, Miesbach D (2011) Occurrence of steroid hormones and antibiotics in shallow groundwater impacted by livestock waste control facilities. J Contam Hydrol 123:94–103

    CAS  PubMed  Google Scholar 

  • Bergstrand LH, Cardenas E, Holert J, Hamme JDV, Mohn WW (2016) Delineation of steroid-degrading microorganisms through comparative genomic analysis. mBio 7:00166-16

    Google Scholar 

  • Blunt SM, Benotti MJ, Rosen MR, Hedlund BP, Moser DP (2017) Reversible reduction of estrone to 17 beta-estradiol by Rhizobium, Sphingopyxis, and Pseudomonas isolates from the Las Vegas Wash. J Environ Qual 46:281–287

    CAS  PubMed  Google Scholar 

  • Caldwell DJ, Mastrocco F, Anderson PD, Lange R, Sumpter JP (2012) Predicted-no-effect concentrations for the steroid estrogens estrone, 17β-estradiol, estriol, and 17α-ethinylestradiol. Environ Toxicol Chem 31:1396–1406

    CAS  PubMed  Google Scholar 

  • Chen TS, Chen TC, Yeh KJC, Chao HR, Liaw ET, Hsieh CY, Chen KC, Hsieh LT, Yeh YL (2010) High estrogen concentrations in receiving river discharge from a concentrated livestock feedlot. Sci Total Environ 408:3223–3230

    CAS  PubMed  Google Scholar 

  • Chen YL, Fu HY, Lee TH, Shih CJ, Huang L, Wang YS, Ismail W, Chiang YR (2018) Estrogen degraders and estrogen degradation pathway identified in an activated sludge. Appl Environ Microbiol 84:e00001–e00018

    CAS  PubMed  PubMed Central  Google Scholar 

  • Combalbert S, Hernandez-Raquet G (2010) Occurrence, fate, and biodegradation of estrogens in sewage and manure. Appl Microbiol Biotechnol 86:1671–1692

    CAS  PubMed  Google Scholar 

  • Czajka CP, Londry KL (2006) Anaerobic biotransformation of estrogens. Sci Total Environ 367:932–941

    CAS  PubMed  Google Scholar 

  • Drzyzga O, Navarro LJM, Fernández HL, García FE, Perera J (2009) Gordonia cholesterolivorans sp. nov., a cholesterol-degrading actinomycete isolated from sewage sludge. Int J Syst Evol Microbiol 59:1011–1015

    CAS  PubMed  Google Scholar 

  • Drzyzga O, Fernández H, Morales M, Navarro LL, Perera J (2011) Cholesterol degradation by Gordonia cholesterolivorans. Appl Environ Microbiol 77:4802–4810

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duong CN, Ra JS, Cho J, Kim SD, Choi HK, Park JH, Kim KW, Inam E, Kim SD (2010) Estrogenic chemicals and estrogenicity in river waters of South Korea and seven Asian countries. Chemosphere 78:286–293

    CAS  PubMed  Google Scholar 

  • Dytczak MA, Londry KL, Oleszkiewicz JA (2008) Biotransformation of estrogens in nitrifying activated sludge under aerobic and alternating anoxic/aerobic conditions. Water Environ Res 80:47–52

    CAS  PubMed  Google Scholar 

  • Fahrbach M, Kuever J, Meinke R, Kampfer P, Hollender J (2006) Denitratisoma oestradiolicum gen. nov., sp nov., a 17 beta-oestradiol-degrading, denitrifying betaproteobacterium. Int J Syst Evol Microbiol 56:1547–1552

    CAS  PubMed  Google Scholar 

  • Fahrbach M, Kuever J, Remesch M, Huber BE, Kampfer P, Dott W, Hollender J (2008) Steroidobacter denitrificans gen. nov., sp. nov., a steroidal hormone-degrading gammaproteobacterium. J Syst Evol Microbiol 58:2215–2223

    CAS  Google Scholar 

  • Fujii K, Kikuchi S, Satomi M, Ushio-Sata N, Morita N (2002) Degradation of 17β-estradiol by a gram-negative bacterium isolated from activated sludge in a sewage treatment plant in Tokyo, Japan. Appl Environ Microbiol 68:2057–2060

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ge F, Li W, Chen G, Liu Y, Zhang G, Yong B, Wang Q, Wang N, Huang Z, Li W, Wang J, Wu C, Xie Q, Liu G (2011) Draft genome sequence of Gordonia neofelifaecis NRRL B-59395, a cholesterol-degrading actinomycete. J Bacteriol 193:5045–5046

    CAS  PubMed  PubMed Central  Google Scholar 

  • Göhler A, Xiong G, Paulsen S, Trentmann G, Maser E (2008) Testosterone-inducible regulator is a kinase that drives steroid sensing and metabolism in Comamonas testosteroni. J Biol Chem 283:17380–17390

    PubMed  Google Scholar 

  • Gong W, Xiong G, Maser E (2012) Identification and characterization of the LysR-type transcriptional regulator HsdR for steroid-inducible expression of the 3α-hydroxysteroid dehydrogenase/carbonyl reductase gene in Comamonas testosteroni. Appl Environ Microbiol 78:941–950

    CAS  PubMed  PubMed Central  Google Scholar 

  • Griffith DR, Kido Soule MC, Eglinton TI, Kujawinski EB, Gschwend PM (2016) Steroidal estrogen sources in a sewage-impactedcoastal ocean. Environ Sci Proc Impacts 18:981–991

    CAS  Google Scholar 

  • Haiyan R, Shulan J, Ahmad N, Dao W, Cheng C (2007) Degradation characteristics and metabolic pathway of 17α-ethynylestradiol by Sphingobacterium sp. JCR5. Chemosphere 66:340–346

    PubMed  Google Scholar 

  • Hiessl S, Schuldes J, Thürmer A, Halbsguth T, Bröker D, Angelov A, Liebl W, Daniel R, Steinbüchel A (2012) Involvement of two latex-clearing proteins during rubber degradation and insights into the subsequent degradation pathway revealed by the genome sequence of Gordonia polyisoprenivorans strain VH2. Appl Environ Microbiol 78:2874–2887

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holert J, Cardenas E, Bergstrand LH, Zaikova E, Hahn AS, Hallam SJ, Mohn WW (2018) Metagenomes reveal global distribution of bacterial steroid catabolism in natural, engineered, and host environments. mBio 9:eo2345-17

    Google Scholar 

  • Horinouchi M, Hayashi T, Kudo T (2012) Steroid degradation in Comamonas testosteroni. J Steroid Biochem Mol Biol 129:4–14

    CAS  PubMed  Google Scholar 

  • Ke J, Zhuang W, Gin YH, Reinhard M, Hoon LT, Tay JH (2007) Characterization of estrogen degrading bacteria isolated from an artificial sandy aquifer with ultrafiltered secondary effluent as the medium. Appl Microbiol Biotechnol 75:1163–1171

    CAS  PubMed  Google Scholar 

  • Khanal SK, Xie B, Thompson ML, Sung S, Ong SK, Leeuwe J (2006) Fate, transport, and biodegradation of natural estrogens in the environment and engineered systems. Environ Sci Technol 40:6537-46

    PubMed  Google Scholar 

  • Kurisu F, Ogura M, Saitoh S, Yamazoe A, Yagi O (2010) Degradation of natural estrogen and identification of the metabolites produced by soil isolates of Rhodococcus sp. and Sphingomonas sp. J Biosci Bioeng 109:576–582

    CAS  PubMed  Google Scholar 

  • Lai KM, Scrimshaw MD, Lester JN (2002) Biotransformation and bioconcentration of steroid estrogens by Chlorella vulgaris. Appl Environ Microbiol 68(2002):859–864

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Z, Nandakumar R, Madayiputhiya N, Li X (2012) Proteomic analysis of 17β-estradiol degradation by Stenotrophomonas maltophilia. Environ Sci Technol 46:5947–5955

    CAS  PubMed  Google Scholar 

  • Liu N, Shi YE, Li M, Zhang TD, Gao S (2015) Simultaneous determination of four trace estrogens in feces, leachate, tap and groundwater using solid-liquid extraction/auto solid-phase extraction and high-performance liquid chromatography with fluorescence detection. J Sep Sci 38:3494–3501

    CAS  PubMed  Google Scholar 

  • Nakai S, Yamamura A, Tanaka S, Shi J, Nishikawa M, Nakashimada Y, Hosomi M (2011) Pathway of 17β-estradiol degradation by Nitrosomonas europaea and reduction in 17β-estradiol-derived estrogenic activity. Environ Chem Lett 9:1–6

    CAS  Google Scholar 

  • Roh H, Chu KH (2010) A 17β-Estradiol-utilizing bacterium, Sphingomonas strain KC8: part I-characterization and abundance in wastewater treatment plants. Environ Sci Technol 44:4943–4950

    CAS  PubMed  Google Scholar 

  • Schneider K, Graf E, Irran E, Nicholson G, Stainsby FM, Goodfellow M, Borden SA, Keller S, Süssmuth RD, Fiedler HP (2008) Bendigoles A ~ C, new steroids from Gordonia australis Acta 2299. J Antibiot 61:356–364

    CAS  PubMed  Google Scholar 

  • Shtratnikova VY, Schelkunov MI, Fokina VV, Pekov YA, Ivashina T, Donova MV (2016) Genome-wide bioinformatics analysis of steroid metabolism-associated genes in Nocardioides simplex VKM Ac-2033D. Curr Genet 62:643–656

    CAS  PubMed  Google Scholar 

  • Wang P, Zheng D, Wang Y, Liang R (2018) One 3-oxoacyl-(acyl-Carrier-protein) reductase functions as 17β-hydroxysteroid dehydrogenase in the estrogen-degrading Pseudomonas putida SJTE-1. Biochem Biophys Res Commun 505:910–916

    CAS  PubMed  Google Scholar 

  • Wang P, Zheng D, Liang R (2019a) Isolation and characterization of an estrogen-degrading Pseudomonas putida strain SJTE-1. 3 Biotech 9:61

    PubMed  PubMed Central  Google Scholar 

  • Wang YQ, Li YW, Chen QL, Liu ZH (2019b) Long-term exposure of xenoestrogens with environmental relevant concentrations disrupted spermatogenesis of zebra fish through altering sex hormone balance, stimulating germ cell proliferation, meiosis and enhancing apoptosis. Environ Poll 244:486–494

    Google Scholar 

  • Whitman WB (2017) Bacteria and the fate of estrogen in the environment. Cell Chem Biol 24:652–653

    CAS  PubMed  Google Scholar 

  • Wu Q, Lam JCW, Kwok KY, Tsui MMP, Lam PKS (2017) Occurrence and fate of endogenous steroid hormones, alkylphenol ethoxylates, bisphenol A and phthalates inmunicipal sewage treatment systems. J Environ Sci 61:49–58

    Google Scholar 

  • Wu K, Lee TH, Chen YL, Wang YS, Wang PH, Yu CP, Chu KH, Chiang YR (2019) Metabolites involved in aerobic degradation of the A and B rings of estrogen. Appl Environ Microbiol 85:e02223-18

    PubMed  PubMed Central  Google Scholar 

  • Xiong G, Maser E (2001) Regulation of the steroid-inducible 3alpha-hydroxysteroid dehydrogenase/carbonyl reductase gene in Comamonas testosteroni. J Biol Chem 276:9961–9970

    CAS  PubMed  Google Scholar 

  • Xiong G, Martin HJ, Maser E (2003) Identification and characterization of a novel translational repressor of the steroid-inducible 3 alpha-hydroxysteroid dehydrogenase/carbonyl reductase gene in Comamonas testosteroni. J Biol Chem 278:47400–47407

    CAS  PubMed  Google Scholar 

  • Xiong W, Peng W, Liang R (2018) Identification and genome analysis of Deinococcus actinosclerus SJTR1, a novel 17β-estradiol degradation bacterium. 3 Biotech 8:433

    PubMed  PubMed Central  Google Scholar 

  • Xu J, Zhang L, Hou J, Wang X, Liu H, Zheng D, Liang R (2017) iTRAQ-based quantitative proteomic analysis of the global response to 17β-estradiol in estrogen-degradation strain Pseudomonas putida SJTE-1. Sci Rep 7:41682

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ye X, Wang H, Kan J, Li J, Huang T, Xiong G (2017) A novel17β-hydroxysteroid dehydrogenase in Rhodococcus sp P14 for transforming 17β-estradiol to estrone. Chem Biol Interact 276:105–112

    CAS  PubMed  Google Scholar 

  • Yoshimoto T, Nagai F, Fujimoto J, Watanabe K, Mizukoshi H, Makino T, Kimura K, Saino H, Sawada H, Omura H (2004) Degradation of estrogens by Rhodococcus zopfii and Rhodococcus equi isolates from activated sludge in wastewater treatment plants. Appl Environ Microbiol 70:5283–5289

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu CP, Roh H, Chu KH (2007) 17 beta-estradiol-degrading bacteria isolated from activated sludge. Environ Sci Technol 41:486–492

    CAS  PubMed  Google Scholar 

  • Yu CP, Deeb RA, Chu KH (2013) Microbial degradation of steroidal estrogens. Chemosphere 91:1225–1235

    CAS  PubMed  Google Scholar 

  • Zeng Q, Li YM, Gu GW, Zhao JM, Zhang CJ, Luan JF (2009) Sorption and biodegradation of 17β-estradiol by acclimated aerobic activated sludge and isolation of the bacterial strain. Environ Eng Sci 26:783–790

    CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by National Science Foundation of China (Grant no. 31702299).

Author information

Authors and Affiliations

  1. Key Laboratory of Groundwater Resources and Environment, Ministry of Education, College of New Energy and Environment, Jilin University, Changchun, 130021, China

    Na Liu, Yue-e Shi, Jialu Li, Meiling Zhu & Tingdi Zhang

Authors
  1. Na Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yue-e Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jialu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Meiling Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tingdi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

TZ designed the experiments and wrote the manuscript. NL performed the experiments. YS, JL and MZ assisted the experiments. All the authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Tingdi Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethics approval and consent to participate

This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, N., Shi, Ye., Li, J. et al. Isolation and characterization of a new highly effective 17β-estradiol-degrading Gordonia sp. strain R9 . 3 Biotech 10, 174 (2020). https://doi.org/10.1007/s13205-020-2156-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-020-2156-z

Keywords

Search

Navigation