Carbon sources that enable enrichment of 1,4-dioxane-degrading bacteria in landfill leachate

Abstract

1,4-Dioxane (DX) is a recalcitrant cyclic ether that has gained attention as an emerging pollutant in the aquatic environment. Enrichment of indigenous DX-degrading bacteria, which are considered to be minor populations even in DX-impacted environments, is the key for efficient biological DX removal. Therefore, this study aimed to explore carbon sources applicable for the enrichment of DX-degrading bacteria present in landfill leachate, which is a potential source of DX pollution. Microorganisms collected from landfill leachate were cultivated on six different carbon sources (DX, tetrahydrofuran (THF), 1,3,5-trioxane (TX), ethylene glycol (EG), diethylene glycol (DEG), and 1,4-butanediol (BD)) in a sequential batch mode. Consequently, enrichment cultures cultivated on THF in addition to DX improved the DX degradation ability compared to that of the original leachate sample, while those on the other test carbon sources did not. The results indicated that THF can be an alternative carbon source to enrich DX-degrading bacteria, and that TX, EG, DEG and BD are not applicable to concentrate DX-degrading bacteria in complex microbial consortia. In addition, sequencing analyses of 16S rRNA and soluble di-iron monooxygenase (SDIMO) genes revealed notable dominance of thm/dxm genes involved in group 5 SDIMO both in DX- and THF-enrichment cultures. The analysis also showed a predominance of Pseudonocardia in THF-enrichment culture, suggesting that Pseudonocardia harboring thm/dxm genes contributes to enhanced DX degradation in THF-enrichment culture.

This is a preview of subscription content, access via your institution.

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

References

  1. Adamson DT, Anderson RH, Mahendra S, Newell CJ (2015) Evidence of 1,4-dioxane attenuation at groundwater sites contaminated with chlorinated solvents and 1,4-dioxane. Environ Sci Technol 49:6510–6518

    CAS  PubMed  Google Scholar 

  2. Amann RI, Ludwig W, Schleiter KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Aoyagi T, Morishita F, Sugiyama Y, Ichikawa D, Mayumi D, Kikuchi Y, Ogata A, Muraoka K, Habe H, Hori T (2018) Identification of active and taxonomically diverse 1,4-dioxane degraders in a full-scale activated sludge system by high-sensitivity stable isotope probing. ISME J 12:2376–2388

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Bernhardt D, Diekmann H (1991) Degradation of dioxane, tetrahydrofuran and other cyclic ethers by an environmental Rhodococcus strain. Appl Microbiol Biotechnol 36:120–123

    CAS  PubMed  Google Scholar 

  5. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108:4516–4522

    CAS  PubMed  Google Scholar 

  7. Chen D-Z, Jin X-J, Chen J, Ye J-X, Jiang N-X, Chen J-M (2016) Intermediates and substrate interaction of 1,4-dioxane degradation by the effective metabolizer Xanthobacter flavus DT8. Int Biodeterior Biodegrad 106:133–140

    CAS  Google Scholar 

  8. Coleman NV, Bui NB, Holmes AJ (2006) Soluble di-iron monooxygenase gene diversity in soils, sediments and ethene enrichments. Environ Microbiol 8:1228–1239

    CAS  PubMed  Google Scholar 

  9. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    CAS  Google Scholar 

  10. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    CAS  PubMed  PubMed Central  Google Scholar 

  11. He Y, Mathieu J, Yang Y, Yu P, da Silva M, 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 4:494–499

    CAS  Google Scholar 

  12. He Y, Mathieu J, da Silva MLB, Li M, Alvarez PJJ (2018) 1,4-Dioxane-degrading consortia can be enriched from uncontaminated soils: prevalence of Mycobacterium and soluble di-iron monooxygenase genes. Microb Biotechnol 11:189–198

    CAS  PubMed  Google Scholar 

  13. Huang H, Shen D, Li N, Shan D, Shentu J, Zhou Y (2014) Biodegradation of 1,4-dioxane by a novel strain and its biodegradation pathway. Water Air Soil Pollut 225:2135

    Google Scholar 

  14. Inoue D, Tsunoda T, Sawada K, Yamamoto N, Saito Y, Sei K, Ike M (2016) 1,4-Dioxane degradation potential of members of the genera Pseudonocardia and Rhodococcus. Biodegradation 27:277–286

    CAS  PubMed  Google Scholar 

  15. Inoue D, Tsunoda T, Yamamoto N, Ike M, Sei K (2018) 1,4-Dioxane degradation characteristics of Rhodococcus aetherivorans JCM 14343. Biodegradation 29:301–310

    CAS  PubMed  Google Scholar 

  16. International Agency for Research on Cancer (IARC) (1999) 1,4-Dioxane. In: IARC monographs on the evaluation of carcinogenic risks to humans, vol. 71, Re-evaluation of some organic chemicals, hydrazine and hydrogen peroxide. IARC, Lyon, pp. 589–602

  17. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  Google Scholar 

  18. Li M, Fiorenza S, Chatham JR, Mahendra S, Alvarez PJJ (2010) 1,4-Dioxane biodegradation at low temperatures in Arctic groundwater samples. Water Res 44:2894–2900

    CAS  PubMed  Google Scholar 

  19. 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 47:9950–9958

    CAS  PubMed  Google Scholar 

  20. 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 1:122–127

    CAS  Google Scholar 

  21. Li M, Liu Y, He Y, Mathieu J, Hatton J, DiGuiseppi W, Alvarez PJJ (2017) Hindrance of 1,4-dioxane biodegradation in microcosms biostimulated with inducing or non-inducing auxiliary substrates. Water Res 112:217–225

    CAS  PubMed  Google Scholar 

  22. Li M, Yang Y, He Y, Mathieu J, Yu C, Li Q, Alvarez PJJ (2018) Detection and cell sorting of Pseudonocardia species by fluorescence in situ hybridization and flow cytometry using 16S rRNA-targeted oligonucleotide probes. Appl Microbiol Biotechnol 102:3375–3386

    CAS  PubMed  Google Scholar 

  23. Macedo AJ, Timmis KN, Abraham W-R (2007) Widespread capacity to metabolize polychlorinated biphenyls by diverse microbial communites in soils with no significant exposure to PCB contamination. Environ Microbiol 9:1890–1897

    CAS  PubMed  Google Scholar 

  24. 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 41:7330–7336

    CAS  PubMed  Google Scholar 

  25. Masuda H, McClay K, Steffan R, Zylstra GJ (2012) Biodegradation of tetrahydrofuran and 1,4-dioxane by soluble diiron monooxygenase in Pseudonocardia sp. strain ENV478. J Mol Microbiol Biotechnol 22:312–316

    CAS  PubMed  Google Scholar 

  26. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618

    CAS  PubMed  Google Scholar 

  27. Nadkarni MA, Martin FE, Jacques NA, Hunter N (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148:257–266

    CAS  PubMed  Google Scholar 

  28. Nam JH, Ventura JS, Yeom IT, Lee Y, Jahng D (2016) Structural and kinetic characteristics of 1,4-dioxane-degrading bacterial consortia containing the phylum TM7. J Microbiol Biotechnol 26:1951–1964

    CAS  PubMed  Google Scholar 

  29. Parales RE, Adamus JE, White N, May HD (1994) Degradation of 1,4-dioxane by an actinomycete in pure culture. Appl Environ Microbiol 60:4527–4530

    CAS  PubMed  PubMed Central  Google Scholar 

  30. 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 79:7702–7708

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Sei K, Kakinoki T, Inoue D, Soda S, Fujita M, Ike M (2010) Evaluation of the biodegradation potential of 1,4-dioxane in river, soil and activated sludge samples. Biodegradation 21:585–591

    CAS  PubMed  Google Scholar 

  32. Sei K, Miyagaki K, Kakinoki T, Fukugasako K, Inoue D, Ike M (2013a) Isolation and characterization of bacterial strains that have high ability to degrade 1,4-dioxane as a sole carbon and energy source. Biodegradation 24:665–674

    CAS  PubMed  Google Scholar 

  33. Sei K, Oyama M, Kakinoki T, Inoue D, Ike M (2013b) Isolation and characterization of tetrahydrofuran-degrading bacteria for 1,4-dioxane-containing wastewater treatment by co-metabolic degradation. J Water Environ Technol 11:11–19

    Google Scholar 

  34. Stepien DK, Diehl P, Helm J, Thomas A, Püttmann W (2014) Fate of 1,4-dioxane in the aquatic environment: From sewage to drinking water. Water Res 48:406–419

    CAS  PubMed  Google Scholar 

  35. Vainberg S, McClay K, Masuda H, Root D, Condee C, Zylstra GJ, Steffan RJ (2006) Biodegradation of ether pollutants by Pseudonocardia sp. strain ENV478. Appl Environ Microbiol 72:5218–5224

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Wang B, Teng Y, Xu Y, Chen W, Ren W, Li Y, Christie P, Luo Y (2018) Effect of mixed soil microbiomes on pyrene removal and the response of the soil microorganisms. Sci Total Environ 640–641:9–17

    PubMed  Google Scholar 

  37. White GF, Russell NJ, Tidswell EC (1996) Bacterial scission of ether bonds. Microbiol Rev 60:216–232

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Yabuki Y, Yoshida G, Daifuku T, Ono J, Banno A (2018) Biological treatment of 1,4-dioxane in wastewater from landfill by indigenous microbes attached to flowing carriers. J Water Environ Technol 16:245–255

    Google Scholar 

  39. Yamamoto N, Inoue D, Sei K, Saito Y, Ike M (2018a) Field test of on-site treatment of 1,4-dioxane-contaminated groundwater using Pseudonocardia sp. D17. J Water Environ Technol 16:256–268

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  41. Zenker MJ, Borden RC, Barlaz MA (2000) Mineralization of 1,4-dioxane in the presence of a structural analog. Biodegradation 11:239–246

    CAS  PubMed  Google Scholar 

  42. Zhang S, Gedalanga PB, Mahendra S (2017) Advances in bioremediation of 1,4-dioxane-contaminated waters. J Environ Manage 204:765–774

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was partially supported by JSPS KAKENHI Grant Numbers JP16K12624 and JP19H04301.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Daisuke Inoue.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 69 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Inoue, D., Hisada, K., Okumura, T. et al. Carbon sources that enable enrichment of 1,4-dioxane-degrading bacteria in landfill leachate. Biodegradation 31, 23–34 (2020). https://doi.org/10.1007/s10532-019-09891-w

Download citation

Keywords

  • Carbon source
  • 1,4-Dioxane-degrading bacteria
  • Enrichment
  • Landfill leachate
  • Soluble di-iron monooxygenase
  • thm/dxm genes