Skip to main content
Log in

Potential for cometabolic biodegradation of 1,4-dioxane in aquifers with methane or ethane as primary substrates

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

Abstract

The objective of this research was to evaluate the potential for two gases, methane and ethane, to stimulate the biological degradation of 1,4-dioxane (1,4-D) in groundwater aquifers via aerobic cometabolism. Experiments with aquifer microcosms, enrichment cultures from aquifers, mesophilic pure cultures, and purified enzyme (soluble methane monooxygenase; sMMO) were conducted. During an aquifer microcosm study, ethane was observed to stimulate the aerobic biodegradation of 1,4-D. An ethane-oxidizing enrichment culture from these samples, and a pure culture capable of growing on ethane (Mycobacterium sphagni ENV482) that was isolated from a different aquifer also biodegraded 1,4-D. Unlike ethane, methane was not observed to appreciably stimulate the biodegradation of 1,4-D in aquifer microcosms or in methane-oxidizing mixed cultures enriched from two different aquifers. Three different pure cultures of mesophilic methanotrophs also did not degrade 1,4-D, although each rapidly oxidized 1,1,2-trichloroethene (TCE). Subsequent studies showed that 1,4-D is not a substrate for purified sMMO enzyme from Methylosinus trichosporium OB3b, at least not at the concentrations evaluated, which significantly exceeded those typically observed at contaminated sites. Thus, our data indicate that ethane, which is a common daughter product of the biotic or abiotic reductive dechlorination of chlorinated ethanes and ethenes, may serve as a substrate to enhance 1,4-D degradation in aquifers, particularly in zones where these products mix with aerobic groundwater. It may also be possible to stimulate 1,4-D biodegradation in an aerobic aquifer through addition of ethane gas. Conversely, our results suggest that methane may have limited importance in natural attenuation or for enhancing biodegradation of 1,4-D in groundwater environments.

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
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

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

    Article  CAS  PubMed  Google Scholar 

  • Anderson RH, Anderson JK, Bower PA (2012) Co-occurrence of 1,4-dioxane with trichloroethylene in chlorinated solvent plumes at US Air Force installations: fact or fiction. Integr Environ Assess Manag 8:731–737

    Article  CAS  PubMed  Google Scholar 

  • ATCC (2016) ATCC medium: 2157 Methylocella medium. https://atcc.org/~/media/01D07065549946AC863C486728B33349.ashx

  • Banerjee R (2013) Kinetic and spectroscopic characterization of intermediates in the soluble methane monooxygenase catalytic cycle: the old and the new, in biochemistry, molecular biology, and biophysics. University of Minnesota, Minneapolis

    Google Scholar 

  • Banerjee R, Meier KK, Münck E, Lipscomb JD (2013) Intermediate P* from soluble methane monooxygenase contains a diferrous cluster. Biochemistry 52:4331–4342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banerjee R, Proshlyakov Y, Lipscomb JD, Proshlyakov DA (2015) Structure of the key species in the enzymatic oxidation of methane to methanol. Nature 518:431–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beauvais LG, Lippard SJ (2005) Reactions of the peroxo intermediate of soluble methane monooxygenase hydroxylase with ethers. J Am Chem Soc 127:7370–7378

    Article  CAS  PubMed  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 

  • Brockman FJ, Payne W, Workman DJ, Soong A, Manley S, Hazen TC (1995) Effect of gaseous nitrogen and phosphorus injection on in istu bioremediation of a trichloroethylene-contaminated site. J Hazard Mat 41:287–298

    Article  CAS  Google Scholar 

  • Chiang S-Y, Mora DR, 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 

  • Chu KH, Alvarez-Cohen L (1999) Evaluation of toxic effects of aeration and trichloroethylene oxidation on methanotrophic bacteria grown with different nitrogen sources. Appl Environ Microbiol 65:766–772

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crombie AT, Murrell JC (2014) Trace-gas metabolic versatility of the facultative methanotroph Methylocella silvestris. Nature 510:148–151

    Article  CAS  PubMed  Google Scholar 

  • De Bruin WP, Koterman MJ, Posthumus MA, Schraa G, Zehnder AJ (1992) Complete biological reductive transformation of tetrachloroethene to ethane. Appl Environ Microbiol 58:1996–2000

    PubMed  PubMed Central  Google Scholar 

  • Dedysh SN, Panikov NS, Tiedje JM (1998a) Acidophilic methanotrophic communities from Sphagnum peat bogs. Appl Environ Microbiol 64:922–929

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dedysh SN, Panikov NS, Liesack W, Großkopf R, Zhou J, Tiedje JM (1998b) Isolation of acidophilic methane-oxidizing bacteria from northern peat wetlands. Science 282:281–284

    Article  CAS  PubMed  Google Scholar 

  • Dedysh SN, Liesack W, Khmelenina VN, Suzina NE, Trotsenko YA, Semrau JD, Bares AM, Panikov NS, Tiedje JM (2000) Methylocella palustris gen nov., a new methane-oxidizing acidophilic bacterium from peat bogs, representing a novel subtype of serine pathway methanotrophs. Int J Syst Evol Microbiol 50:955–969

    Article  CAS  PubMed  Google Scholar 

  • DiStefano TD, Gossett JM, Zinder SH (1991) Reductive dechlorination of high concentrations of tetrachloroethene to ethene by an anaerobic enrichment culture in the absence of methanogenesis. Appl Environ Microbiol 57:2287–2292

    CAS  PubMed  PubMed Central  Google Scholar 

  • EPA; US Environmental Protection Agency (2009) Drinking Water Contaminant Candidate List 3: Final. Federal Register Notice. https://www.federalregister.gov/documents/2009/10/08/E9-24287/drinking-water-contaminant-candidate-list-3-final

  • EPA; US Environmental Protection Agency (2014) Technical Fact Sheet: 1,4-Dioxane. United States Environmental Protection Agency,Office of Solid Waste and Emergency Response. EPA 505-F-14-011. https://www.epa.gov/sites/production/files/2014-03/documents/ffrro_factsheet_contaminant_14-dioxane_january2014_final.pdf

  • Foster JW, Davis RH (1966) A methane-dependent coccus, with notes on classification and nomenclature or obligate, methane-utilizing bacteria. J Bacteriol 91:1924–1931

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fox BG, Borneman JG, Wackett LP, Lipscomb JD (1990a) Haloalkene oxidation by the soluble methane monooxygenase from Methylosinus trichosporium OB3b: mechanistic and environmental implications. Biochemistry 29:6419–6427

    Article  CAS  PubMed  Google Scholar 

  • Fox BG, Froland WA, Jollie DR, Lipscomb JD (1990b) Methane monooxygenase from Methylosinus trichosporium OB3b. Methods Enzymol 188:191–202

    Article  CAS  PubMed  Google Scholar 

  • Freedman DL, Gossett JM (1989) Biological reductive dechlorination of tetrachloroethylene and trichloroethylene to ethylene under methanogenic conditions. Appl Environ Microbiol 55:2144–2151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Freedman DL, Herz SD (1996) Use of ethylene and ethane as primary substrates for aerobic cometabolism of vinyl chloride. Water Environ Res 68:320–328

    Article  Google Scholar 

  • Gedalanga PB, Pornwongthong P, Mora R, Chiang S-YD, Baldwin B, Ogles D, Mahendra S (2014) Identification of biomarker genes to predict biodegradation of 1,4-dioxane. Appl Environ Microbiol 80:3209–3218

    Article  PubMed  PubMed Central  Google Scholar 

  • Gedalanga P, Madison A, Miao Y, Richards T, Hatton J, DiGuiseppi WH, Wilson J, Mahendra S (2016) A multiple lines of evidence framework to evaluate intrinsic biodegradation of 1,4-dioxane. Remediat J 27(1):93–114

    Article  Google Scholar 

  • Green J, Dalton H (1989) Substrate specificity of soluble methane monooxygenase. J Biol Chem 264:17698–17703

    CAS  PubMed  Google Scholar 

  • Grostern A, Alvarez-Cohen L (2013) RubisCO-based CO2 fixation and C1 metabolism in the actinobacterium Pseudonocardia dioxanivorans CB1190. Environ Microbiol 15:3040–3053

    CAS  PubMed  Google Scholar 

  • Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hareland WA, Crawford RL, Chapman PJ, Dagley S (1975) Metabolic function and properties of 4-hydroxyphenylacetic acid 1-hydroxylase from Pseudomonas acidovorans. J Bacteriol 121:272–285

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hatzinger PB, Streger SH, Begley JF (2015) Enhancing aerobic biodegradation of 1,2-dibromoethane in groundwater using ethane or propane and inorganic nutrients. J Contam Hydrol 172:61–70

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Koh S-C, Bowman JP, Sayler GS (1993) Soluble methane monooxygenase production and trichloroethylene degradation by a type I methanotroph, Methylomonas methanica 68-1. Appl Environ Microbiol 59:960–967

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee S-W, Keeney DR, Lim D-H, DiSpirito AA, Semrau JD (2006) Mixed pollutant degradation by Methylosinus trichosporium OB3b expressing either soluble or particulate methane monooxygenase: can the tortoise beat the hare? Appl Environ Microbiol 72:7503–7509

    Article  CAS  PubMed  PubMed Central  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, Liu Y, Mathieu J, Alvarez PJJ (2017) Comparison of 1,4-dioxane cometabolism with the amendment of different alkane gases. Presentation at the fourth International Symposium on Bioremediation and Sustainable Environmental Technologies. Miami, FL, May 22–25

  • Lippincott D, Streger SH, Schaefer CE, Hinkle J, Stormo J, Steffan RJ (2015) Bioaugmentation and propane biosparging for in situ biodegradation of 1,4-dioxane. Groundw Monit Remediat 35:81–92

    CAS  Google Scholar 

  • Lontoh S, Semrau JD (1998) Methane and trichloroethylene degradation by Methylosinus trichosporium OB3b expressing particulate methane monooxygenase. Appl Environ Microbiol 64:1106–1114

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mahendra S, Alvarez-Cohen L (2005) Pseudonocardia dioxanivorans sp. nov., a novel actinomycete that grows on 1,4-dioxane. Int J Syst Evol Microbiol 55:593–598

    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 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Mahendra S, Grostern A, Alvarez-Cohen L (2013) The impact of chlorinated solvent co-contaminants on the biodegradation kinetics of 1,4-dioxane. Chemosphere 91:88–92

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Maymó-Gatell X, Chien Y-T, Gossett JM, Zinder SH (1997) Isolation of a bacterium that reductively dechlorinates tetrachloroethene to ethene. Science 276:1568–1571

    Article  PubMed  Google Scholar 

  • Mohr T, Stickney J, DiGuiseppi W (2010) Environmental investigation and remediation: 1,4-dioxane and other solvent stabilizers. CRC Press, Boca Raton, p 552

    Book  Google Scholar 

  • Nakamiya K, Hashimoto S, Ito H, Edmonds JS, Morita M (2010) Degradation of 1,4-dioxane and cyclic ethers by an isolated fungus. Appl Environ Microbiol 71:1254–1258

    Article  Google Scholar 

  • Orth WS, Gilham RW (1995) Dechlorination of trichloroethene in aqueous solution using Fe0. Environ Sci Technol 30:66–71

    Article  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 

  • Puls RW, Barcelona MJ (1995) Low-flow (minimal drawdown) ground-water sampling procedures. United States Environmental Protection Agency EPA/540/S-95/504. https://www.researchgate.net/profile/Michael_Barcelona/publication/237506331_United_States_Environmental_Protection_Agency_Office_of_Research_and_Development_Office_of_Solid_Waste_and_Emergency_Response_EPA540S-95504_December_1995_EPA_Ground_Water_Issue_LOW-FLOW_MINIMAL_DRAWDO/links/0a85e52ef9573672af000000.pdf

  • Sadeghi V, Mora R, Jacob P, Chiang S-H (2016) Characterizing in situ methane-enhanced biostimulation potential for 1,4-dioxane biodegradation in groundwater. Remediat J 27(1):115–132

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Semrau J (2011) Bioremediation via methanotrophy: overview of recent findings and suggestions for future research. Front Microbiol 2:209–219

    Article  PubMed  PubMed Central  Google Scholar 

  • Stroo HF, Ward CH (2008) In Situ Bioremediatiion of Perchlorate in Groundwater. Springer Science/Business Media, LLC, New York

    Google Scholar 

  • Tinberg CE, Lippard SJ (2010) Oxidation reactions performed by soluble methane monooxygenase hydroxylase intermediates Hperoxo and Q proceed by distinct mechanisms. Biochemistry 49:7902–7912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vainberg S, McClay K, Masuda H, Root D, Condee C, Zylstra GL, 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 

  • Verce MF, Freedman DL (2000) Modeling the biodegradation kinetics of vinyl chloride cometabolism by an ethane-grown Pseudomonas sp. Biotechnol Bioeng 71:274–285

    Article  CAS  PubMed  Google Scholar 

  • Wymore RA, Lee MH, Keener WK, Miller AR, Colwell FS, Watwood ME, Sorenson KS Jr (2007) Field evidence for intrinsic aerobic chlorinated ethene cometabolism by methanotrophs expressing soluble methane monooxygenase. Biorem J 11:125–139

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Lipscomb JD (2006) Role of the C-terminal region of the B component of Methylosinus trichosporium OB3b methane monooxygenase in the regulation of oxygen activation. Biochemistry 45:1459–1469

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We wish to acknowledge the Strategic Environmental Research and Development Program (SERDP; Project ER-2306) and the Air Force Civil Engineer Center (AFCEC; BAA Project 769) for supporting some of the studies described herein. Dr Michael Hyman at North Carolina State University provided helpful comments and insights. We also wish to thank Dr. Randi Rothmel and Anthony Soto of CB&I for their analytical support. The results and interpretations presented herein are solely the opinion of the authors and not of SERDP or AFCEC unless otherwise stated in official documentation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul B. Hatzinger.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 89 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hatzinger, P.B., Banerjee, R., Rezes, R. et al. Potential for cometabolic biodegradation of 1,4-dioxane in aquifers with methane or ethane as primary substrates. Biodegradation 28, 453–468 (2017). https://doi.org/10.1007/s10532-017-9808-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10532-017-9808-7

Keywords

Navigation