Abstract
Biodegradation of 1,4-Dioxane at environmentally relevant concentrations usually requires the addition of a primary electron-donor substrate to sustain biomass growth. Ethane is a promising substrate, since it is available as a degradation product of 1,4-Dioxane’s common co-contaminants. This study reports kinetic parameters for ethane biodegradation and co-oxidations of ethane and 1,4-Dioxane. Based on experiments combined with mathematical modeling, we found that ethane promoted 1,4-Dioxane biodegradation when the initial mass ratio of ethane:1,4-Dioxane was < 9:1 mg COD/mg COD, while it inhibited 1,4-Dioxane degradation when the ratio was > 9:1. A model-independent estimator was used for kinetic-parameter estimation, and all parameter values for 1,4-Dioxane were consistent with literature-reported ranges. Estimated parameters support competitive inhibition between ethane as the primary substrate and 1,4-Dioxane as the secondary substrate. The results also support that bacteria that co-oxidize ethane and 1,4-Dioxane had a competitive advantage over bacteria that can use only one of the two substrates. The minimum concentration of ethane to sustain ethane-oxidizing bacteria and ethane and 1,4-Dioxane-co-oxidizing bacteria was 0.09 mg COD/L, which is approximately 20-fold lower than the minimum concentration reported for propane, another common substrate used to promote 1,4-Dioxane biodegradation. The minimum 1,4-Dioxane concentration required to sustain steady-state biomass with 1,4-Dioxane as the sole primary substrate was 1.3 mg COD/L. As 1,4-Dioxane concentrations at most groundwater sites are less than 0.18 mg COD/L, providing ethane as a primary substrate is vital to support biomass growth and consequently enable 1,4-Dioxane bioremediation.
Graphical abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adamson DT, Newell CJ, Mahendra S, Bryant D, Wong M (2017a) In situ treatment and management strategies for 1,4-Dioxane-contaminated groundwater. SERDP Project ER-2307, Alexandria
Adamson DT, Piña EA, Cartwright AE, Rauch SR, Anderson RH, Mohr T, Connor JA (2017b) 1,4-Dioxane drinking water occurrence data from the third unregulated contaminant monitoring rule. Sci Total Environ 596–597:236–245. https://doi.org/10.1016/j.scitotenv.2017.04.085
Barajas-Rodriguez FJ, Freedman DL (2018) Aerobic biodegradation kinetics for 1,4-dioxane under metabolic and cometabolic conditions. J Hazard Mater 350:180–188. https://doi.org/10.1016/j.jhazmat.2018.02.030
Barndõk H, Cortijo L, Hermosilla D, Negro C, Blanco Á (2014) Removal of 1,4-dioxane from industrial wastewaters: routes of decomposition under different operational conditions to determine the ozone oxidation capacity. J Hazard Mater 280:340–347. https://doi.org/10.1016/j.jhazmat.2014.07.077
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 Biodegradation 106:133–140. https://doi.org/10.1016/j.ibiod.2015.09.018
Chiang S-YD, Anderson RH, Wilken M, Walecka-hutchison C (2016) Practical perspectives of 1,4-dioxane investigation and remediation. Remediation 27:7–27. https://doi.org/10.1002/rem.21494
Deng D, Li F, Li M (2018) A novel propane monooxygenase initiating degradation of 1,4-dioxane by Mycobacterium dioxanotrophicus PH-06. Environ Sci Technol Lett 5:86–91. https://doi.org/10.1021/acs.estlett.7b00504
Deng D, Pham DN, Li F, Li M (2020) Discovery of an inducible toluene monooxygenase that cooxidizes 1,4-dioxane and 1,1-dichloroethylene in propanotrophic Azoarcus sp. strain DD4. Appl Environ Microbiol 86:1–14. https://doi.org/10.1128/AEM.01163-20
DiGuiseppi W, Walecka-Hutchison C, Hatton J (2016) 1,4-Dioxane treatment technologies. Remediation 27:71–92. https://doi.org/10.1002/rem.21498
Doherty J (2019) PEST model-independent parameter estimation. User manual part I: PEST, SENSAN and global optimisers, 7th edn. Watermark Numerical Computing, Brisbane
EPA (2013) Toxicological Review of 1,4-Dioxane. Support of summary information on the Integrated Risk Information System (IRIS). U.S. Environmental Protection Agency, Washington DC
EPA (2017) Technical Fact sheet – 1,4-Dioxane. U.S. Environmental Protection Agency, Washington DC
Grady CPL, Daigger GT, Love NG, Filipe CDM (2011) Biological wastewater treatment. CRC Press Taylor and Francis Group, Boca Raton
Han JS, So MH, Kim CG (2009) Optimization of biological wastewater treatment conditions for 1,4-dioxane decomposition in polyester manufacturing processes. Water Sci Technol 59:995–1002. https://doi.org/10.2166/wst.2009.079
Hatzinger PB, Banerjee R, Rezes R, Streger SH, McClay K, Schaefer CE (2017) Potential for cometabolic biodegradation of 1,4-dioxane in aquifers with methane or ethane as primary substrates. Biodegradation 28:453–468. https://doi.org/10.1007/s10532-017-9808-7
He Y, Mathieu J, Yang Y, Yu P, Silva MLB, Alvarez PJJ (2017a) 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. https://doi.org/10.1021/acs.estlett.7b00456
He Y, Wei K, Si K, Mathieu J, Li M, Alvarez PJJ (2017b) Whole-genome sequence of the 1,4-dioxane-degrading bacterium Mycobacterium dioxanotrophicus PH-06. Genome Announc 5:1–3. https://doi.org/10.1128/genomeA.00625-17
Huang H, Shen D, Li N, Shan D, Shentu J, Zhou YY (2014) Biodegradation of 1,4-dioxane by a novel strain and its biodegradation pathway. Water Air Soil Pollut 225:2135. https://doi.org/10.1007/s11270-014-2135-2
IARC (1999) IARC monographs on the evaluation of carcinogenic risks to humans: re-evaluation of some organic chemicals, hydrazine and hydrogen peroxide. World Health Organization, International Agency for Research on Cancer, Lyon
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
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. https://doi.org/10.1007/s10532-018-9832-2
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
Lee KH, Wie YM, Lee Y-S (2020) Characterization of 1,4-dioxane biodegradation by a microbial community. Water 12:3372. https://doi.org/10.3390/w12123372
Lee KH, Khan IA, Inam MA, Khan R, Wie YM, Yeom IT (2022) Efficacy of continuous Flow reactors for Biological Treatment of 1,4-Dioxane contaminated Textile Wastewater using a mixed culture. Fermentation 8:1–14. https://doi.org/10.3390/fermentation8040143
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. https://doi.org/10.1016/j.watres.2017.01.047
Li F, Deng D, Li M (2020) Distinct catalytic behaviors between two 1,4-dioxane-degrading monooxygenases: kinetics, inhibition, and substrate range. Environ Sci Technol 54:1898–1908. https://doi.org/10.1021/acs.est.9b05671
Luo Y-H, Long X, Wang B, Zhou C, Tang Y, Krajmalnik-brown R, Rittmann BE (2021) A synergistic platform for continuous co-removal of 1,1,1-trichloroethane, trichloroethene, and 1,4-dioxane via catalytic dechlorination followed by biodegradation. Environ Sci Technol 55:6363–6372. https://doi.org/10.1021/acs.est.1c00542
Ma F, Wang Y, Yang J, Guo H, Su D, Yu L (2021) Degradation of 1,4-dioxane by Xanthobacter sp. YN2. Curr Microbiol 78:992–1005. https://doi.org/10.1007/s00284-021-02347-6
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. https://doi.org/10.1099/ijs.0.63085-0
Mahendra S, Alvarez-cohen L (2006) Kinetics of 1,4-dioxane biodegradation by monooxygenase-expressing bacteria. Environ Sci Technol 40:5435–5442. https://doi.org/10.1021/es060714v
Mohr TKG, Stickney JA, DiGuiseppi WH (2010) Environmental investigation and remediation: 1,4-Dioxane and other solvent stabilizers. CRC Press Taylor and Francis Group, Boca Raton
Nam J-H, Ventura J-RS, 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. https://doi.org/10.4014/jmb.1601.01095
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. https://doi.org/10.1128/aem.60.12.4527-4530.1994
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 65:2201–2208. https://doi.org/10.1007/s13213-015-1060-y
Ramalingam V, Cupples AM (2020) Enrichment of novel Actinomycetales and the detection of monooxygenases during aerobic 1,4-dioxane biodegradation with uncontaminated and contaminated inocula. Appl Microbiol Biotechnol 104:2255–2269. https://doi.org/10.1007/s00253-020-10376-7
Ramos-García ÁA, Walecka-Hutchison C, Freedman DL (2022) Effect of biostimulation and bioaugmentation on biodegradation of high concentrations of 1,4-dioxane. Biodegradation 33:157–168. https://doi.org/10.1007/s10532-022-09971-4
Rittmann BE, McCarty PL (2020) Environmental biotechnology: principles and applications. McGraw-Hill Education
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
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. https://doi.org/10.1128/AEM.02418-13
Sander R (2015) Compilation of Henry’s law constants (version 4.0) for water as solvent. Atmos Chem Phys 15:4399–4981. https://doi.org/10.5194/acp-15-4399-2015
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 24:665–674. https://doi.org/10.1007/s10532-012-9614-1
Simmer RA, Richards PM, Ewald JM, Schwarz C, Silva MLB, Mathieu J, Alvarez PJJ, Schnoor JL (2021) Rapid metabolism of 1,4-dioxane to below health advisory levels by thiamine-amended Rhodococcus ruber strain 219. Environ Sci Technol Lett 8:975–980. https://doi.org/10.1021/acs.estlett.1c00714
Tusher TR, Shimizu T, Inoue C, Chien M-F (2020) Enrichment and analysis of stable 1,4-dioxane-degrading microbial consortia consisting of novel dioxane-degraders. Microorganisms 8:50. https://doi.org/10.3390/microorganisms8010050
Tusher TR, Shimizu T, Inoue C, Chien M-F (2021) Isolation and characterization of novel bacteria capable of degrading 1,4-dioxane in the presence of diverse co-occurring compounds. Microorganisms 9:877. https://doi.org/10.3390/microorganisms9050887
Xiong Y, Mason OU, Lowe A, Zhou C, Chen G, Tang Y (2019a) Microbial Community Analysis provides insights into the Effects of Tetrahydrofuran on 1,4-Dioxane biodegradation. Appl Environ Microbiol 85:1–11. https://doi.org/10.1128/AEM.00244-19
Xiong Y, Zhang Q, Wandell R, Bresch S, Wang H, Locke BR, Tang Y (2019b) Synergistic 1,4-dioxane removal by non-thermal plasma followed by biodegradation. Chem Eng J 361:519–527. https://doi.org/10.1016/j.cej.2018.12.094
Xiong Y, Mason OU, Lowe A, Zhang Z, Zhou C, Chen G, Villalonga MJ, Tang Y (2020) Investigating promising substrates for promoting 1,4-dioxane biodegradation: effects of ethane and tetrahydrofuran on microbial consortia. Biodegradation 31:171–182. https://doi.org/10.1007/s10532-020-09901-2
Xiong Y, Wang B, Zhou C, Chen H, Chen G, Tang Y (2022) Determination of growth kinetics of microorganisms linked with 1,4-dioxane degradation in a consortium based on two improved methods. Front Environ Sci Eng 16:62. https://doi.org/10.1007/s11783-022-1567-y
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 125:552–558. https://doi.org/10.1016/j.jbiosc.2017.12.005
Yu H, Kashima H, Regan JM, Hussain A, Elbeshbishy E, Lee H-S (2017) Kinetic study on anaerobic oxidation of methane coupled to denitrification. Enzyme Microb Technol 104:47–55. https://doi.org/10.1016/j.enzmictec.2017.05.005
Zenker MJ, Borden RC, Barlaz MA (2002) Modeling cometabolism of cyclic ethers. Environ Eng Sci 19:215–228. https://doi.org/10.1089/109287502760271535
Zenker MJ, Borden RC, Barlaz MA (2003) Occurrence and treatment of 1,4-dioxane in aqueous environments. Environ Eng Sci 20:423–432. https://doi.org/10.1089/109287503768335913
Zhang S, Gedalanga PB, Mahendra S (2017) Advances in bioremediation of 1,4-dioxane-contaminated waters. J Environ Manage 204:765–774. https://doi.org/10.1016/j.jenvman.2017.05.033
Acknowledgements
This work was supported by the U.S. Department of Defense (DOD), the Strategic Environmental Research and Development Program (SERDP), through Project ER-2721.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conceptualization and methodology. Data collection and investigation were performed by YHL. Data analysis, modeling, and preparation of the first draft of the manuscript were carried out by EGT. All authors reviewed and edited the previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Tesfamariam, E.G., Luo, YH., Zhou, C. et al. Simultaneous biodegradation kinetics of 1,4-dioxane and ethane. Biodegradation (2023). https://doi.org/10.1007/s10532-023-10058-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10532-023-10058-x