Applied Microbiology and Biotechnology

, Volume 104, Issue 3, pp 1291–1305 | Cite as

Characterization of an 17β-estradiol-degrading bacterium Stenotrophomonas maltophilia SJTL3 tolerant to adverse environmental factors

  • Weiliang Xiong
  • Chong Yin
  • Wanli Peng
  • Zixin Deng
  • Shuangjun Lin
  • Rubing LiangEmail author
Environmental biotechnology


Bioremediation of environmental estrogens requires microorganisms with stable degradation efficiency and great stress tolerance in complex environments. In this work, Stenotrophomonas maltophilia SJTL3 isolated from wastewater was found to be able to degrade over 90% of 10 μg/mL 17β-estradiol (E2) in a week and the degradation dynamic was fitted by the first-order kinetic equations. Estrone was the first and major intermediate of E2 biodegradation. Strain SJTL3 exhibited strong tolerance to several adverse conditions like extreme pH (3.0–11.0), high osmolality (2%), co-existing heavy metals (6.25 μg/mL of Cu2+) and surfactants (5 CMC of Tween 80), and retained normal cell vitality and stable E2-degradaing efficiency. In solid soil, strain SJTL3 could remove nearly 100% of 1 μg/mL of E2 after the bacteria inoculation and 8-day culture. As to the contamination of 10 μg/mL E2 in soil, the biodegradation efficiency was about 90%. The further obtainment of the whole genome of strain SJTL3 and genome analysis revealed that this strain contained not only the potential genes responsible for estrogen degradation, but also the genes encoding proteins involved in stress tolerance. This work could promote the estrogen-biodegrading mechanism study and provide insights into the bioremediation application.


Stenotrophomonas maltophilia SJTL3 Biodegradation 17β-estradiol Estrone Stress tolerance 



We acknowledge Shanghai Personal Biotech Co., Ltd. for genome sequencing.

Author contributions

R L designed the experiments; X L and R L wrote the manuscript. X L, C Y, and W P performed the experiments. D Z and L S gave support on the experiments. All the authors discussed the results and commented on the manuscript.

Funding information

This work was supported by the National Science Foundation of China (31570099) and the Natural Science Foundation of Shanghai (19ZR1475500).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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

Supplementary material

253_2019_10281_MOESM1_ESM.pdf (1000 kb)
ESM 1 (PDF 1000 kb)


  1. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75PubMedPubMedCentralGoogle Scholar
  2. Beck KR, Kaserer T, Schuster D, Odermatt A (2017) Virtual screening applications in short-chain dehydrogenase/reductase research. J Steroid Biochem Mol Biol 171:157–177PubMedPubMedCentralGoogle Scholar
  3. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2003) GenBank. Nucleic Acids Res 31:23–27PubMedPubMedCentralGoogle Scholar
  4. Bilal M, Iqbal HMN (2019) Persistence and impact of steroidal estrogens on the environment and their laccase-assisted removal. Sci Total Environ 690:447–459PubMedGoogle Scholar
  5. Boutet E, Lieberherr D, Tognolli M, Schneider M, Bansal P, Bridge AJ, Poux S, Bougueleret L, Xenarios I (2016) UniProtKB/Swiss-Prot, the manually annotated section of the UniProt KnowledgeBase: how to use the entry view. Methods Mol Biol 1374:23–54PubMedGoogle Scholar
  6. Breed RS, Murray EG, Hitchens AP (1944) The outline classification used in the Bergey manual of determinative bacteriology. Bacteriol Rev 8:255–260PubMedPubMedCentralGoogle Scholar
  7. Bulzomi P, Bolli A, Galluzzo P, Leone S, Acconcia F, Marino M (2010) Naringenin and 17beta-estradiol coadministration prevents hormone-induced human cancer cell growth. IUBMB Life 62:51–60PubMedGoogle Scholar
  8. Cajthaml T (2015) Biodegradation of endocrine-disrupting compounds by ligninolytic fungi: mechanisms involved in the degradation. Environ Microbiol 17:4822–4834PubMedGoogle Scholar
  9. Cajthaml T, Kresinová Z, Svobodová K, Möder M (2009) Biodegradation of endocrine-disrupting compounds and suppression of estrogenic activity by ligninolytic fungi. Chemosphere 75:745–750PubMedGoogle Scholar
  10. Chen K, Zhu Q, Qian Y, Song Y, Yao J, Choi MM (2013) Microcalorimetric investigation of the effect of non-ionic surfactant on biodegradation of pyrene by PAH-degrading bacteria Burkholderia cepacia. Ecotoxicol Environ Saf 98:361–367PubMedGoogle Scholar
  11. Chen YL, Yu CP, Lee TH, Goh KS, Chu KH, Wang PH, Ismail W, Shih CJ, Chiang YR (2017) Biochemical mechanisms and catabolic enzymes involved in bacterial estrogen degradation pathways. Cell Chem Biol 24:712–724 e7PubMedGoogle Scholar
  12. 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 84Google Scholar
  13. Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5:e11147PubMedPubMedCentralGoogle Scholar
  14. Delcher AL, Harmon D, Kasif S, White O, Salzberg SL (1999) Improved microbial gene identification with GLIMMER. Nucleic Acids Res 27:4636–4641PubMedPubMedCentralGoogle Scholar
  15. Denisov G, Walenz B, Halpern AL, Miller J, Axelrod N, Levy S, Sutton G (2008) Consensus generation and variant detection by Celera Assembler. Bioinformatics 24:1035–1040PubMedGoogle Scholar
  16. D'Souza S, Garcia-Cabado A, Yu F, Teter K, Lukacs G, Skorecki K, Moore HP, Orlowski J, Grinstein S (1998) The epithelial sodium-hydrogen antiporter Na+/H+ exchanger 3 accumulates and is functional in recycling endosomes. J Biol Chem 273:2035–2043PubMedGoogle Scholar
  17. Eliassen AH, Hankinson SE (2008) Endogenous hormone levels and risk of breast, endometrial and ovarian cancers: prospective studies. Adv Exp Med Biol 630:148–165PubMedGoogle Scholar
  18. English AC, Richards S, Han Y, Wang M, Vee V, Qu J, Qin X, Muzny DM, Reid JG, Worley KC, Gibbs RA (2012) Mind the gap: upgrading genomes with Pacific biosciences RS long-read sequencing technology. PLoS One 7:e47768PubMedPubMedCentralGoogle Scholar
  19. Fernández L, Louvado A, Esteves VI, Gomes NCM, Almeida A, Cunha  (2017) Biodegradation of 17β-estradiol by bacteria isolated from deep sea sediments in aerobic and anaerobic media. J Hazard Mater 323:359–366PubMedGoogle Scholar
  20. Figueras MJ, Beaz-Hidalgo R, Hossain MJ, Liles MR (2014) Taxonomic affiliation of new genomes should be verified using average nucleotide identity and multilocus phylogenetic analysis. Genome Announc 2(6)Google Scholar
  21. Fletez-Brant C, Lee D, McCallion AS, Beer MA (2013) kmer-SVM: a web server for identifying predictive regulatory sequence features in genomic data sets. Nucleic Acids Res 41(Web Server issue):W544–W556PubMedPubMedCentralGoogle Scholar
  22. Fujii K, Kikuchi S, Satomi M, Ushio-Sata N, Morita N (2002) Degradation of 17beta-estradiol by a gram-negative bacterium isolated from activated sludge in a sewage treatment plant in Tokyo, Japan. Appl Environ Microbiol 68:2057–2060PubMedPubMedCentralGoogle Scholar
  23. Glenn TC (2011) Field guide to next-generation DNA sequencers. Mol Ecol Resour 11:759–769PubMedGoogle Scholar
  24. Horinouchi M, Hayashi T, Kudo T (2012) Steroid degradation in Comamonas testosteroni. J Steroid Biochem. Mol Biol 129:4–14Google Scholar
  25. Järup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182Google Scholar
  26. Juhasz AL, Stanley GA, Britz ML (2000) Microbial degradation and detoxification of high molecular weight polycyclic aromatic hydrocarbons by Stenotrophomonas maltophilia strain VUN 10,003. Lett Appl Microbiol 30:396–401PubMedGoogle Scholar
  27. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36(Database issue):D480–D484PubMedGoogle Scholar
  28. Kavanagh KL, Jörnvall H, Persson B, Oppermann U (2008) Medium- and short-chain dehydrogenase/reductase gene and protein families : the SDR superfamily: functional and structural diversity within a family of metabolic and regulatory enzymes. Cell Mol Life Sci 65:3895–3906PubMedPubMedCentralGoogle Scholar
  29. Kavlock RJ (1999) Overview of endocrine disruptor research activity in the United States. Chemosphere 39:1227–1236PubMedGoogle Scholar
  30. 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 109:576–582PubMedGoogle Scholar
  31. Lee HB, Liu D (2002) Degradation of 17β-estradiol and its metabolities by sewage bacteria. Water Air Soil Pollut 134:353–368Google Scholar
  32. Li Z, Nandakumar R, Madayiputhiya N, Li X (2012) Proteomic analysis of 17beta-estradiol degradation by Stenotrophomonas maltophilia. Environ Sci Technol 46:5947–5955PubMedGoogle Scholar
  33. Li S, Liu J, Sun M, Ling W, Zhu X (2017) Isolation, characterization, and degradation performance of the 17beta-estradiol-degrading bacterium Novosphingobium sp. E2S. Int J Environ Res Public Health 14:E115PubMedGoogle Scholar
  34. Li M, Zhao X, Zhang X, Wu D, Leng S (2018) Biodegradation of 17beta-estradiol by bacterial co-culture isolated from manure. Sci Rep 8:3787PubMedPubMedCentralGoogle Scholar
  35. Liu S, Guo C, Liang X, Wu F, Dang Z (2016) Nonionic surfactants induced changes in cell characteristics and phenanthrene degradation ability of Sphingomonas sp. GY2B. Ecotoxicol Environ Saf 129:210–218PubMedGoogle Scholar
  36. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380PubMedPubMedCentralGoogle Scholar
  37. Mohammed AS, Kapri A, Goel R (2011) Heavy metal pollution: source, impact, and remedies. In: Khan MS, Zaidi A, Goel R (eds) Biomanagement of metal-contaminated soils. J. Musarrat, Springer Netherlands, Dordrecht, pp 1–28Google Scholar
  38. Mohanty S, Mukherji S (2013) Surfactant aided biodegradation of NAPLs by Burkholderia multivorans: comparison between triton X-100 and rhamnolipid JBR-515. Colloids Surf B: Biointerfaces 102:644–652PubMedGoogle Scholar
  39. Muller M, Patureau D, Godon JJ, Delgenes JP, Hernandez-Raquet G (2010) Molecular and kinetic characterization of mixed cultures degrading natural and synthetic estrogens. Appl Microbiol Biotechnol 85:691–701PubMedGoogle Scholar
  40. Powell S, Forslund K, Szklarczyk D, Trachana K, Roth A, Huerta-Cepas J, Gabaldon T, Rattei T, Creevey C, Kuhn M, Jensen LJ, von Mering C, Bork P (2014) eggNOG v4.0: nested orthology inference across 3686 organisms. Nucleic Acids Res 42(Database issue):D231–D239PubMedGoogle Scholar
  41. Shi J, Fujisawa S, Nakai S, Hosomi M (2004) Biodegradation of natural and synthetic estrogens by nitrifying activated sludge and ammonia-oxidizing bacterium Nitrosomonas europaea. Water Res 38:2322–2329PubMedGoogle Scholar
  42. Singh A, Kumar K, Pandey AK, Sharma A, Singh SB, Kumar K, Arora A, Nain L (2015) Pyrene degradation by biosurfactant producing bacterium Stenotrophomonas maltophilia. Agric Res 4:42–47Google Scholar
  43. Susin MF, Baldini RL, Gueiros-Filho F, Gomes SL (2006) GroES/GroEL and DnaK/DnaJ have distinct roles in stress responses and during cell cycle progression in Caulobacter crescentus. J Bacteriol 188:8044–8053PubMedPubMedCentralGoogle Scholar
  44. Ting YF, Praveena SM (2017) Praveena, Sources, mechanisms, and fate of steroid estrogens in wastewater treatment plants: a mini review. Environ Monit Assess 189:178PubMedGoogle Scholar
  45. Wang P, Zheng D, Peng W, Wang Y, Wang X, Xiong W, Liang R (2019) Characterization of 17β-hydroxysteroid dehydrogenase and regulators involved in estrogen degradation in Pseudomonas putida SJTE-1. Appl Microbiol Biotechnol 103:2413–2425PubMedGoogle Scholar
  46. 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 17beta-estradiol in estrogen-degradation strain Pseudomonas putida SJTE-1. Sci Rep 7:41682PubMedPubMedCentralGoogle Scholar
  47. Ye X, Wang H, Kan J, Li J, Huang T, Xiong G, Hu Z (2017) A novel 17beta-hydroxysteroid dehydrogenase in Rhodococcus sp. P14 for transforming 17beta-estradiol to estrone. Chem Biol Interact 276:105–112PubMedGoogle Scholar
  48. Yu CP, Roh H, Chu KH (2007) 17beta-estradiol-degrading bacteria isolated from activated sludge. Environ Sci Technol 41:486–492PubMedGoogle Scholar
  49. Zhang D, Zhu L, Li F (2013) Influences and mechanisms of surfactants on pyrene biodegradation based on interactions of surfactant with a Klebsiella oxytoca strain. Bioresour Technol 142:454–461PubMedGoogle Scholar
  50. Zhao X, Grimes KL, Colosi LM, Lung WS (2019) Attenuation, transport, and management of estrogens: a review. Chemosphere 230:462–478PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and BiotechnologyShanghai Jiao Tong UniversityShanghaiChina

Personalised recommendations