Skip to main content
SpringerLink
Log in

1,4-Dioxane degradation potential of members of the genera Pseudonocardia and Rhodococcus

  • Original Paper
  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

In recent years, several strains capable of degrading 1,4-dioxane have been isolated from the genera Pseudonocardia and Rhodococcus. This study was conducted to evaluate the 1,4-dioxane degradation potential of phylogenetically diverse strains in these genera. The abilities to degrade 1,4-dioxane as a sole carbon and energy source and co-metabolically with tetrahydrofuran (THF) were evaluated for 13 Pseudonocardia and 12 Rhodococcus species. Pseudonocardia dioxanivorans JCM 13855T, which is a 1,4-dioxane degrading bacterium also known as P. dioxanivorans CB1190, and Rhodococcus aetherivorans JCM 14343T could degrade 1,4-dioxane as the sole carbon and energy source. In addition to these two strains, ten Pseudonocardia strains could degrade THF, but no Rhodococcus strains could degrade THF. Of the ten Pseudonocardia strains, Pseudonocardia acacia JCM 16707T and Pseudonocardia asaccharolytica JCM 10410T degraded 1,4-dioxane co-metabolically with THF. These results indicated that 1,4-dioxane degradation potential, including degradation for growth and by co-metabolism with THF, is possessed by selected strains of Pseudonocardia and Rhodococcus, although THF degradation potential appeared to be widely distributed in Pseudonocardia. Analysis of soluble di-iron monooxygenase (SDIMO) α-subunit genes in THF and/or 1,4-dioxane degrading strains revealed that not only THF and 1,4-dioxane monooxygenases but also propane monooxygenase-like SDIMOs can be involved in 1,4-dioxane degradation.

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

Similar content being viewed by others

References

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

    Article  CAS  PubMed  Google Scholar 

  • Adams CD, Scanlan PA, Secrist ND (1994) Oxidation and biodegradability enhancement of 1,4-dioxane using hydrogen peroxide and ozone. Environ Sci Technol 28:1812–1818

    Article  CAS  PubMed  Google Scholar 

  • Agency for Toxic Substances and Disease Registry (ATSDR) (2012) Toxicological profile for 1,4-dioxane. United States Department of Health and Human Services, Public Health Service, Atlanta, GA. http://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=955&tid=199. Accessed 28 February 2016

  • Alvarez PJJ, Vogel TM (1991) Substrate interactions of benzene, toluene, and para-xylene during microbial degradation by pure cultures and mixed culture aquifer slurries. Appl Environ Microbiol 57:2981–2985

    CAS  PubMed  PubMed Central  Google Scholar 

  • Auffret M, Labbé D, Thouand G, Greer CW, Fayolle-Guichard F (2009) Degradation of a mixture of hydrocarbons, gasoline, and diesel oil additives by Rhodococcus aetherivorans and Rhodococcus wratislaviensis. Appl Environ Microbiol 75:7774–7782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cao B, Nagarajan K, Loh KC (2009) Biodegradation of aromatic compounds: current status and opportunities for biomolecular approaches. Appl Microbiol Biotechnol 85:207–228

    Article  CAS  PubMed  Google Scholar 

  • Chiang SYD, Mora R, Diguiseppi WH, Davis G, Sublette K, Gedalanga P, Mahendra S (2012) Characterizing the intrinsic bioremediation potential of 1,4-dioxane and trichloroethene using innovative environmental diagnostic tools. J Environ Monit 14:2317–2326

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Damborský J (1999) Tetrachloroethene-dehalogenating bacteria. Folia Microbiol 44:247–262

    Article  Google Scholar 

  • Deeb RA, Alvarez-Cohen L (1999) Temperature effects and substrate interactions during the aerobic biotransformation of BTEX mixtures by toluene-enriched consortia and Rhodococcus rhodochrous. Biotechnol Bioeng 62:526–536

    Article  CAS  PubMed  Google Scholar 

  • Eddy SR (1995) Multiple alignment using hidden Markov models. In: Rawlings C, Clark D, Altman R, Hunter L, Lengauer T, Wodak S (eds.) Proceedings of the third international conference on intelligent systems for molecular biology. AAAI Press, Menlo Park, pp 114–120

  • Fujiwara T, Tamada T, Kurata Y, Ono Y, Kose T, Ono Y, Nishimura F, Ohtoshi K (2008) Investigation of 1,4-dioxane originating from incineration residues produced by incineration of municipal solid waste. Chemosphere 71:894–901

    Article  CAS  PubMed  Google Scholar 

  • Goodfellow M, Jones AL, Maldonado LA, Salanitro J (2004) Rhodococcus aetherivorans sp. nov., a new species that contains methyl t-butyl ether-degrading actinomycetes. Syst Appl Microbiol 27:61–65

    Article  CAS  PubMed  Google Scholar 

  • Hori K, Kobayashi A, Ikeda H, Unno H (2009) Rhodococcus aetherivorans IAR1, a new bacterial strain synthesizing poly(3-hydroxybutyrate-co-3-hydroxyvalerate) from toluene. J Biosci Bioeng 107:145–150

    Article  CAS  PubMed  Google Scholar 

  • 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

  • Isaacson C, Mohr TKG, Field JA (2006) Quantitative determination of 1,4-dioxane and tetrahydrofuran in groundwater by solid phase extraction GC/MS/MS. Environ Sci Technol 40:7305–7311

    Article  CAS  PubMed  Google Scholar 

  • Kämpfer P, Kroppenstedt RM (2004) Pseudonocardia benzenivorans sp. nov. Int J Syst Evol Microbiol 54:749–751

    Article  PubMed  Google Scholar 

  • Kelly SL, Aitchison EW, Deshpande M, Schnoor JL, Alvarez PJJ (2001) Biodegradation of 1,4-dioxane in planted and unplanted soil: effect of bioaugmentation with Amycolata sp. CB1190. Water Res 35:3791–3800

    Article  Google Scholar 

  • Kim CG, Seo HJ, Lee BR (2006) Decomposition of 1,4-dioxane by advanced oxidation and biochemical process. J Environ Sci Health A 41:599–611

    Article  CAS  Google Scholar 

  • Kishimoto N, Nakagawa T, Asano M, Abe M, Yamada M, Ono Y (2008) Ozonation combined with electrolysis of 1,4-dioxane using a two-compartment electrolytic flow cell with solid electrolyte. Water Res 42:379–385

    Article  CAS  PubMed  Google Scholar 

  • Kohlweyer U, Tiemer B, Schräder T, Andreesen JR (2000) Tetrahydrofuran degradation by a newly isolated culture of Pseudonocardia sp. strain K1. FEMS Microbiol Lett 186:301–306

    Article  CAS  PubMed  Google Scholar 

  • Lesage S, Jackson RE, Priddle MW, Riemann PG (1990) Occurrence and fate of organic solvent residues in anoxic groundwater at the Gloucester Landfill, Canada. Environ Sci Technol 24:559–566

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Li M, Van Orden ET, DeVries DJ, Xiong Z, Hinchee R, Alvarez PJ (2015) Bench-scale biodegradation tests to assess natural attenuation potential of 1,4-dioxane at three sites in California. Biodegradation 26:39–50

    Article  CAS  PubMed  Google Scholar 

  • Mahendra S, Alvarez-Cohen L (2006) Kinetics of 1,4-dioxane biodegradation by monooxygenase-expressing bacteria. Environ Sci Technol 40:5435–5442

    Article  CAS  PubMed  Google Scholar 

  • Matsui R, Takagi K, Sakakibara F, Abe T, Shiiba K (2016) Identification and characterization of 1,4-dioxane-degrading microbe separated from surface seawater by the seawater-charcoal perfusion apparatus. Biodegradation. doi:10.1007/s10532-016-9763-8

    PubMed  Google Scholar 

  • Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

  • 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 

  • Prabahar V, Dube S, Reddy GSN, Shivaji S (2004) Pseudonocardia antarctica sp. nov. an Actinomycetes from McMurdo Dry Valleys, Antarctica. Syst Appl Microbiol 27:66–71

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Shukla AK, Upadhyay SN, Dubey SK (2014) Current trends in trichloroethylene biodegradation: a review. Crit Rev Biotechnol 34:101–114

    Article  CAS  PubMed  Google Scholar 

  • 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 48:406–419

    Article  CAS  PubMed  Google Scholar 

  • Sun W, Cupples AM (2012) Diversity of five anaerobic toluene-degrading microbial communities investigated using stable isotope probing. Appl Environ Microbiol 78:972–980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tajima T, Hayashida N, Matsumura R, Omura A, Nakashimada Y, Kato J (2012) Isolation and characterization of tetrahydrofuran-degrading Rhodococcus aetherivorans strain M8. Process Biochem 47:1665–1669

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weelink SAB, van Eekert MHA, Stams AJM (2010) Degradation of BTEX by anaerobic bacteria: physiology and application. Rev Environ Sci Biotechnol 9:359–385

    Article  CAS  Google Scholar 

  • Wolfe NL, Jeffers PM (2000) Hydrolysis. In: Boethling RS, Mackay D (eds) Handbook of property estimation methods for chemicals: environmental and health sciences. Lewis Publishers, Chelsea, pp 311–334

    Google Scholar 

Download references

Acknowledgments

This study was supported by Environment Research and Technology Development Fund (5B-1201) of the Ministry of the Environment, Japan, by the Adaptable and Seamless Technology Transfer Program through Target-driven R&D (A-STEP) of the Japan Science and Technology (JST), Japan, and by the Kurita Water and Environment Foundation (15A066).

Author information

Authors and Affiliations

  1. Department of Health Science, Kitasato University, 1-15-1 Kitasato, Sagamihara-Minami, Kanagawa, 252-0373, Japan

    Daisuke Inoue, Kazuko Sawada & Kazunari Sei

  2. Environment and Medical Sciences Course, Graduate School of Medical Sciences, Kitasato University, 1-15-1 Kitasato, Sagamihara-Minami, Kanagawa, 252-0373, Japan

    Daisuke Inoue, Tsubasa Tsunoda & Kazunari Sei

  3. Technology Center, Taisei Corporation, 344-1 Nase-cho, Totsuka-ku, Yokohama, Kanagawa, 245-0051, Japan

    Norifumi Yamamoto & Yuji Saito

  4. Division of Sustainable Energy and Environmental Engineering, Osaka University, 2-1 Yamadaoka, Suita, Osaka, 565-0871, Japan

    Norifumi Yamamoto & Michihiko Ike

Authors
  1. Daisuke Inoue
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tsubasa Tsunoda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kazuko Sawada
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Norifumi Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuji Saito
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kazunari Sei
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michihiko Ike
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daisuke Inoue.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 145 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Inoue, D., Tsunoda, T., Sawada, K. et al. 1,4-Dioxane degradation potential of members of the genera Pseudonocardia and Rhodococcus . Biodegradation 27, 277–286 (2016). https://doi.org/10.1007/s10532-016-9772-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10532-016-9772-7

Keywords

Search

Navigation