Skip to main content
Log in

Degradation of 1,4-Dioxane by Xanthobacter sp. YN2

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

1,4-Dioxane is a highly toxic and carcinogenic pollutant found worldwide in groundwater and soil environments. Several microorganisms have been isolated by their ability to grow on 1,4-dioxane; however, low 1,4-dioxane tolerance and slow degradation kinetics remain obstacles for their use in 1,4-dioxane bioremediation. We report here the isolation and characterization of a new strain, Xanthobacter sp. YN2, capable of highly efficient 1,4-dioxane degradation. High degradation efficiency and high tolerance to 1,4-dioxane make this new strain an ideal candidate for the biodegradation of 1,4-dioxane in various treatment facilities. The maximum degradation rate of 1,4-dioxane was found to be 1.10 mg-1,4-dioxane/h mg-protein. Furthermore, Xanthobacter sp. YN2 was shown to grow in the presence of higher than 3000 mg/L 1,4-dioxane with little to no degradation inhibition. In addition, Xanthobacter sp. YN2 could grow on and degrade 1,4-dioxane at pH ranges 5 to 8 and temperatures between 20 and 40 °C. Xanthobacter sp. YN2 was also found to be able to grow on a variety of other substrates including several analogs of 1,4-dioxane. Genome sequence analyses revealed the presence of two soluble di-iron monooxygenase (SDIMO) gene clusters, and regulation studies determined that all of the genes in these two clusters were upregulated in the presence of 1,4-dioxane. This study provides insights into the bacterial stress response and the highly efficient biodegradation of 1,4-dioxane as well as the identification of a novel Group-2 SDIMO.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Stepien DK, Diehl P, Helm J, Thoms A, Püttmann W (2014) Fate of 1,4-dioxane in the aquatic environment: from sewage to drinking water. Water Res 48(1):406–419. https://doi.org/10.1016/j.watres.2013.09.057

    Article  CAS  PubMed  Google Scholar 

  2. Hinchee RE, Dahlen PR, Johnson PC, Burris DR (2018) 1,4-dioxane soil remediation using enhanced soil vapor extraction: I field demonstration. Ground Water Monit Remediat 38(2):40–48. https://doi.org/10.1111/gwmr.12264

    Article  CAS  Google Scholar 

  3. Chiang SY, Anderson R, Wilken M, Walecka-Hutchison C (2016) Practical perspectives of 1,4-dioxane investigation and remediation. Remediation 27(1):7–27. https://doi.org/10.1002/rem.21494

    Article  Google Scholar 

  4. Abe A (1999) Distribution of 1, 4-dioxane in relation to possible sources in the water environment. Sci Total Environ 227(1):41–47

    Article  CAS  Google Scholar 

  5. Karges U, Becker J, Puettmann W (2018) 1,4-dioxane pollution at contaminated groundwater sites in western Germany and its distribution within a TCE plume. Sci Total Environ 619:712–720. https://doi.org/10.1016/j.scitotenv.2017.11.043

    Article  CAS  PubMed  Google Scholar 

  6. da Silva MLB, Woroszylo C, Castillo NF, Adamson DT, Alvarez PJ (2018) Associating potential 1, 4-dioxane biodegradation activity with groundwater geochemical parameters at four different contaminated sites. J Environ Manag 206:60–64. https://doi.org/10.1016/j.jenvman.2017.10.031

    Article  CAS  Google Scholar 

  7. Adamson DT, Mahendra S, Walker KL, Rauch SR, Sengupta S, Newell CJ (2014) A multisite survey to identify the scale of the 1,4-dioxane problem at contaminated groundwater sites. Environ Sci Technol Lett 1(5):254–258. https://doi.org/10.1021/ez500092u

    Article  CAS  Google Scholar 

  8. Mohr T, Stickney J, Diguiseppi W (2010) Environmental investigation and remediation: 1,4-dioxane and other solvent stabilizers. CRC Press, Boca Raton

    Google Scholar 

  9. McElroy AC, Hyman MR, Knappe DR (2019) 1,4-dioxane in drinking water: emerging for forty years and still unregulated. Curr Opin Environ Sci Health. https://doi.org/10.1016/j.coesh.2019.01.003

    Article  Google Scholar 

  10. Steffan RJ, McClay KR, Masuda H, Zylstra GJ (2007) ER-1422: Biodegradation of 1, 4-dioxane. Shaw Environmental Inc, Lawrenceville NJ

    Google Scholar 

  11. Isaka K, Udagawa M, Kimura Y, Sei K, Ike M (2015) Biological wastewater treatment of 1,4-dioxane using polyethylene glycol gel carriers entrapping afipia sp. D1. J Biosci Bioeng 121(2):203–208. https://doi.org/10.1016/j.jbiosc.2015.06.006

    Article  CAS  PubMed  Google Scholar 

  12. Sei K, Miyagaki K, Kakinoki T, Fukugasako K, Inoue D, Ike M (2013) Isolation and characterization of bacterial strains that have high ability to degrade 1,4-dioxane as a sole carbon and energy source. Biodegradation 24(5):665–674. https://doi.org/10.1007/s10532-012-9614-1

    Article  CAS  PubMed  Google Scholar 

  13. Huang H (2015) Study on the characteristics and quorum sensing of 1,4-dioxane degradation by A. Baumannii DD1. Zhejiang Gongshang University,

  14. Jin XJ, Chen DZ, Zhu RY, Chen J, Chen JM (2012) Characteristics of 1,4-dioxane degradation by xanthobacter flavus DT8. Environ Sci 33(5):1657–1662

    CAS  Google Scholar 

  15. Pugazhendi A, Banu JR, Dhavamani J, Yeom IT (2015) Biodegradation of 1,4-dioxane by rhodanobacter AYS5 and the role of additional substrates. Ann Microbiol 65(4):2201–2208. https://doi.org/10.1007/s13213-015-1060-y

    Article  CAS  Google Scholar 

  16. Sun B, Ko K, Ramsay JA (2011) Biodegradation of 1,4-dioxane by a flavobacterium. Biodegradation 22(3):651–659. https://doi.org/10.1007/s10532-010-9438-9

    Article  CAS  PubMed  Google Scholar 

  17. Zenker MJ, Borden RC, Barlaz MA (2000) Mineralization of 1,4-dioxane in the presence of a structural analog. Biodegradation 11(4):239–246. https://doi.org/10.1023/A:1011156924700

    Article  CAS  PubMed  Google Scholar 

  18. Parales R, Adamus J, White N, May H (1994) Degradation of 1, 4-dioxane by an actinomycete in pure culture. Appl Environ Microbiol 60(12):4527–4530. https://doi.org/10.1016/0922-338X(95)92742-U

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Rolston HM, Hyman MR, Semprini L (2019) Aerobic cometabolism of 1,4-dioxane by isobutane-utilizing microorganisms including rhodococcus rhodochrous strain 21198 in aquifer microcosms: experimental and modeling study. Sci Total Environ 694:133688. https://doi.org/10.1016/j.scitotenv.2019.133688

    Article  CAS  PubMed  Google Scholar 

  20. Skinner K, Cuiffetti L, Hyman M (2009) Metabolism and cometabolism of cyclic ethers by a filamentous fungus, a graphium sp. Appl Environ Microbiol 75(17):5514–5522. https://doi.org/10.1128/aem.00078-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Masuda H, Mcclay K, Steffan RJ, Zylstra GJ (2012) Biodegradation of tetrahydrofuran and 1,4-dioxane by soluble diiron monooxygenase in pseudonocardia sp. strain ENV478. J Mol Microbiol Biotechnol 22(5):312–316. https://doi.org/10.1159/000343817

    Article  CAS  PubMed  Google Scholar 

  22. Li M, Mathieu J, Liu Y, Van Orden ET, Yang Y, Fiorenza S, Alvarez PJJ (2014) The abundance of Tetrahydrofuran/Dioxane monooxygenase Genes (thmA/dxmA) and 1,4-dioxane degradation activity are significantly correlated at various impacted aquifers. Environ Sci Technol Lett 1(1):122–127. https://doi.org/10.1021/ez400176h

    Article  CAS  Google Scholar 

  23. Li M, Mathieu J, Yang Y, Fiorenza S, Deng Y, He Z, Zhou J, Alvarez PJJ (2013) Widespread distribution of soluble Di-Iron monooxygenase (SDIMO) genes in arctic groundwater impacted by 1,4-dioxane. Environ Sci Technol 47(17):9950–9958. https://doi.org/10.1021/es402228x

    Article  CAS  PubMed  Google Scholar 

  24. Sales CM, Grostern A, Parales JV, Parales RE, Alvarez-Cohen L (2013) Oxidation of the cyclic ethers 1,4-dioxane and tetrahydrofuran by a monooxygenase in two pseudonocardia species. Appl Environ Microbiol 79(24):7702–7708. https://doi.org/10.1128/AEM.02418-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. He Y, Mathieu J, Yang Y, Yu P, Silva MLBD, Alvarez PJJ (2017) 1,4-dioxane biodegradation by mycobacterium dioxanotrophicus PH-06 is associated with a group-6 soluble Di-iron monooxygenase. Environ Sci Technol Lett 4(11):494–499. https://doi.org/10.1021/acs.estlett.7b00456

    Article  CAS  Google Scholar 

  26. He Y, Wei K, Si K, Mathieu J, Li M, Pjj A (2017) Whole-Genome sequence of the 1,4-dioxane-degrading bacterium mycobacterium dioxanotrophicus PH-06. Genome Announc 5(35):e00625-e1617. https://doi.org/10.1128/genomeA.00625-17

    Article  PubMed  PubMed Central  Google Scholar 

  27. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, Phillippy AM (2017) Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res 27(5):722. https://doi.org/10.1101/gr.215087.116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. 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(1):75. https://doi.org/10.1186/1471-2164-9-75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Xu GT, Piao C, Chang JP, Guo LM, Yang XQ, Li Y (2019) Sinorhodobacter populi sp. nov, isolated from the symptomatic bark tissue of populus× euramericana canker. Int J Syst Evol Microbiol 69(4):1220–1224. https://doi.org/10.1099/ijs.0.066068-0

    Article  CAS  PubMed  Google Scholar 

  30. Mornico D, Miché L, Béna G, Nouwen N, Verméglio A, Vallenet D, Smith AA, Giraud E, Médigue C, Moulin L (2012) Comparative genomics of aeschynomene symbionts: insights into the ecological lifestyle of nod-independent photosynthetic bradyrhizobia. Genes 3(1):35–61. https://doi.org/10.3390/genes3010035

    Article  CAS  Google Scholar 

  31. Huang MM, Guo LL, Wu YH, Lai QL, Shao ZZ, Wang CS, Wu M, Xu XW (2017) Pseudooceanicola lipolyticus sp. nov., a marine alphaproteobacterium, reclassification of oceanicola flagellatus as pseudooceanicola flagellatus comb. nov. and emended description of the genus pseudooceanicola. Int J Syst Evol Microbiol 68(1):409–415. https://doi.org/10.1099/ijsem.0.002521

    Article  CAS  PubMed  Google Scholar 

  32. Notomista E, Lahm A, Di Donato A, Tramontano A (2003) Evolution of bacterial and archaeal multicomponent monooxygenases. J Mol Evol 56(4):435–445. https://doi.org/10.1007/s00239-002-2414-1

    Article  CAS  PubMed  Google Scholar 

  33. Coleman NV, Bui NB, Holmes AJ (2006) Soluble di-iron monooxygenase gene diversity in soils, sediments and ethene enrichments. Environ Microbiol 8(7):1228–1239. https://doi.org/10.1111/j.1462-2920.2006.01015.x

    Article  CAS  PubMed  Google Scholar 

  34. Holmes AJ, Coleman NV (2008) Evolutionary ecology and multidisciplinary approaches to prospecting for monooxygenases as biocatalysts. Antonie Van Leeuwenhoek 94(1):75–84. https://doi.org/10.1007/s10482-008-9227-1

    Article  CAS  PubMed  Google Scholar 

  35. Kim Y-M, Jeon J-R, Murugesan K, Kim E-J, Chang Y-S (2009) Biodegradation of 1, 4-dioxane and transformation of related cyclic compounds by a newly isolated mycobacterium sp. PH-06. Biodegradation 20:511–519. https://doi.org/10.1007/s10532-008-9240-0

    Article  CAS  PubMed  Google Scholar 

  36. Chen DZ, Jin XJ, Chen J, Ye JX, Jiang NX, Chen JM (2016) Intermediates and substrate interaction of 1,4-dioxane degradation by the effective metabolizer Xanthobacter flavus DT8. Int Biodeter Biodegrad 106:133–140. https://doi.org/10.1016/j.ibiod.2015.09.018

    Article  CAS  Google Scholar 

  37. Nakamiya K, Hashimoto S, Ito H, Edmonds JS, Morita M (2005) Degradation of 1,4-dioxane and cyclic ethers by an isolated fungus. Appl Environ Microbiol 71(3):1254–1258. https://doi.org/10.1128/AEM.71.3.1254-1258.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Mahendra S, Alvarez-Cohen L (2006) Kinetics of 1, 4-dioxane biodegradation by monooxygenase-expressing bacteria. Environ Sci Technol 40(17):5435–5442. https://doi.org/10.1021/es060714v

    Article  CAS  PubMed  Google Scholar 

  39. Yamamoto N, Saito Y, Inoue D, Sei K, Ike M (2018) Characterization of newly isolated pseudonocardia sp N23 with high 1,4-dioxane-degrading ability. J Biosci Bioeng 125(5):552–558

    Article  CAS  Google Scholar 

  40. Deng D, Li F, Li M (2017) A novel propane monooxygenase initiating degradation of 1,4-dioxane by mycobacterium dioxanotrophicus PH-06. Environ Sci Technol Lett. https://doi.org/10.1021/acs.estlett.7b00504

    Article  Google Scholar 

  41. Mahendra S, Petzold CJ, Baidoo EE, Keasling JD, Alvarez-Cohen L (2007) Identification of the intermediates of in vivo oxidation of 1, 4-dioxane by monooxygenase-containing bacteria. Environ Sci Technol 41(21):7330–7336. https://doi.org/10.1021/es0705745

    Article  CAS  PubMed  Google Scholar 

  42. Singh A, Kuhad R, Ward O (2009) Advances in applied bioremediation. Springer Berl. https://doi.org/10.1007/978-3-540-89621-0

    Article  Google Scholar 

  43. Hino S, Watanabe K, Takahashi N (1998) Phenol hydroxylase cloned from ralstonia eutropha strain E2 exhibits novel kinetic properties. Microbiology 144(7):1765

    Article  CAS  Google Scholar 

  44. Zhou NY, Jenkins A, Chan KCC, Leak DJ (1999) The alkene monooxygenase from xanthobacter strain Py2 is closely related to aromatic monooxygenases and catalyzes aromatic monohydroxylation of benzene, toluene, and phenol. Appl Environ Microbiol 65(4):1589

    Article  CAS  Google Scholar 

  45. Deng D, Dung P, Li F, Li M (2020) Discovery of an inducible toluene monooxygenase that co-oxidizes 1,4-Dioxane and 1,1-Dichloroethylene in propanotrophic azoarcus sp DD4. Appl Environ Microbiol. https://doi.org/10.1128/AEM.01163-20

    Article  PubMed  PubMed Central  Google Scholar 

  46. Deng D, Li F, Wu C, Mengyan L (2018) Synchronic biotransformation of 1,4-Dioxane and 1,1-Dichloroethylene by a gram-negative propanotroph azoarcus sp DD4. Environ Sci Technol Lett 5(8):526–532

    Article  CAS  Google Scholar 

  47. Li F, Deng D, Li M (2019) Distinct catalytic behaviors between two 1,4-dioxane degrading monooxygenases: kinetics, inhibition, and substrate range. Environ Sci Technol. https://doi.org/10.1021/acs.est.9b05671

    Article  PubMed  PubMed Central  Google Scholar 

  48. Mcclay K, Schaefer CE, Vainberg S, Steffan RJ (2007) Biodegradation of Bis(2-Chloroethyl) ether by xanthobacter sp. strain ENV481. Appl Environ Microbiol 73(21):6870–6875

    Article  CAS  Google Scholar 

  49. Grostern A, Sales CM, Zhuang WQ, Erbilgin O, Alvarez-Cohen L (2012) Glyoxylate metabolism is a key feature of the metabolic degradation of 1,4-dioxane by pseudonocardiadioxanivorans strain CB1190. Appl Environ Microbiol 78(9):3298–3308

    Article  CAS  Google Scholar 

  50. Alvarez-Cohen L, McCarty PL (1991) A cometabolic biotransformation model for halogenated aliphatic compounds exhibiting product toxicity. Environ Sci Technol 25(8):1381–1387. https://doi.org/10.1021/es00020a003

    Article  CAS  Google Scholar 

  51. Sales CM, Mahendra S, Grostern A, Parales RE, Goodwin LA, Woyke T, Nolan M, Lapidus A, Chertkov O, Ovchinnikova G (2011) Genome sequence of the 1, 4-dioxane-degrading pseudonocardia dioxanivorans Strain CB1190. J Bacteriol 193(17):4549–4550

    Article  CAS  Google Scholar 

  52. He Z, Zhang H, Gao S, Lercher M, Chen W-H, Hu S (2016) Evolview v2: an online visualization and management tool for customized and annotated phylogenetic trees. Nucleic Acids Res. https://doi.org/10.1093/nar/gkw370

    Article  PubMed  PubMed Central  Google Scholar 

  53. Ramosgarcia AA, Shankar V, Saski CA, Hsiang T, Freedman DL (2018) Draft genome sequence of the 1,4-dioxane-degrading bacterium pseudonocardia dioxanivorans BERK-1. Genome Announc. https://doi.org/10.1128/genomeA.00207-18

    Article  Google Scholar 

  54. Bernhardt D, Diekmann H (1991) Degradation of dioxane, tetrahydrofuran and other cyclic ethers by an environmental rhodococcus strain. Appl Microbiol Biotechnol 36(1):120. https://doi.org/10.1007/BF00164711

    Article  CAS  PubMed  Google Scholar 

  55. Inoue D, Tsunoda T, Yamamoto N, Ike M, Sei K (2018) 1,4-Dioxane degradation characteristics of rhodococcus aetherivorans JCM 14343. Biodegradation 29(3):1–10. https://doi.org/10.1007/s10532-018-9832-2

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the National Major Science and Technology Projects of China under 2014ZX07201-012-03. The active sludge used in the study was collected from a WWTP (Harbin, China) by permission.

Author information

Authors and Affiliations

Authors

Contributions

All the authors contribute to (1) substantial contribution to conception and design or the acquisition and analysis of data, (2) drafting or critically revising the manuscript, and (3) approval of the final submitted version. FM—also contributes to conceptualization, funding acquisition, investigation, and project administration. YW—also contributes to the original draft, investigation, data curation, and visualization.

Corresponding author

Correspondence to Fang Ma.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research Involving Human and Animal Participants

This research does not involve any human participants and/or animals.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, F., Wang, Y., Yang, J. et al. Degradation of 1,4-Dioxane by Xanthobacter sp. YN2. Curr Microbiol 78, 992–1005 (2021). https://doi.org/10.1007/s00284-021-02347-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-021-02347-6

Navigation