Skip to main content
SpringerLink
Log in

Enrichment and characterization of a highly efficient tetrahydrofuran-degrading bacterial culture

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

Abstract

Tetrahydrofuran (THF) is a ubiquitous toxic and carcinogenic pollutant. Screening for pure or mixed-culture microorganisms that can efficiently degrade THF is difficult due to its chemical stability. In this study, an enrichment culture, H-1, with a stable THF-degrading ability and microbial community structure was enriched from activated sludge and could efficiently degrade 95% of 40 mM THF within 6 days. The optimal THF degradation conditions for H-1 were an initial pH of 7.0–8.0 and a temperature of 30 °C. The substrate tolerance concentration of H-1 reached 200 mM. Heavy metals tolerance concentrations of Cu2+, Cd2+ and Pb2+ of H-1 was 0.5 mM, 0.4 mM and 0.03 mM, and 4 mM Mn2+ did not significantly influence the THF degradation ratio or biomass of H-1. H-1 might be a good material for actual wastewater treatment because of its efficient THF degradation performance and ability to resist various stressful conditions. In addition, the THF-degrading efficiency of H-1 was enhanced by the addition of moderate carbon sources. High-throughput sequencing of the 16S rRNA gene showed that Rhodococcus sp. (a potential THF-degrading strain) and Hydrogenophaga sp. (a potential non-THF-degrading strain) were the dominant microorganisms in the H-1 culture. These results indicate the potential coexistence of cooperation and competition between THF-degrading bacteria and nondegrading bacteria in this enrichment culture.

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adam M (2016) Biodegradation of marine crude oil pollution using a salt-tolerant bacterial consortium isolated from Bohai Bay, China. Mar Pollut Bull 105:43–50

    PubMed  Google Scholar 

  • Arjoon A, Olaniran AO, Pillay B (2015) Kinetics of heavy metal inhibition of 1,2-dichloroethane biodegradation in co-contaminated water. J Basic Microbiol 55:277–284. https://doi.org/10.1002/jobm.201200776

    Article  CAS  PubMed  Google Scholar 

  • Babel S, Dacera DDM (2006) Heavy metal removal from contaminated sludge for land application: a review. Waste Manage 26:988–1004

    CAS  Google Scholar 

  • Benomar S et al (2015) Nutritional stress induces exchange of cell material and energetic coupling between bacterial species. Nat Commun 6:6283

    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

    CAS  PubMed  Google Scholar 

  • Boon E, Meehan CJ, Whidden C, Wong DH-J, Langille MG, Beiko RG (2014) Interactions in the microbiome: communities of organisms and communities of genes. FEMS Microbiol Rev 38:90–118

    CAS  PubMed  Google Scholar 

  • Chaturvedi AD, Pal D, Penta S, Kumar A (2015) Ecotoxic heavy metals transformation by bacteria and fungi in aquatic ecosystem. World J Microbiol Biotechnol 31:1595–1603. https://doi.org/10.1007/s11274-015-1911-5

    Article  CAS  PubMed  Google Scholar 

  • Chen K-C, Wu J-Y, Liou D-J, Hwang S-CJ (2003) Decolorization of the textile dyes by newly isolated bacterial strains. J Biotechnol 101:57–68

    CAS  PubMed  Google Scholar 

  • Chen J-M, Zhou Y-Y, Chen D-Z, Jin X-J (2010) A newly isolated strain capable of effectively degrading tetrahydrofuran and its performance in a continuous flow system. Bioresour Technol 101:6461–6467

    CAS  PubMed  Google Scholar 

  • Daye K, Groff J, Kirpekar A, Mazumder R (2003) High efficiency degradation of tetrahydrofuran (THF) using a membrane bioreactor: identification of THF-degrading cultures of Pseudonocardia sp. strain M1 and Rhodococcus ruber isolate M2. J Ind Microbiol Biotechnol 30:705–714

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604

    Article  CAS  PubMed  Google Scholar 

  • Foster KR, Bell T (2012) Competition, not cooperation, dominates interactions among culturable microbial species. Curr Biol 22:1845–1850. https://doi.org/10.1016/j.cub.2012.08.005

    Article  CAS  PubMed  Google Scholar 

  • Gamer A, Jaeckh R, Leibold E, Kaufmann W, Gembardt C, Bahnemann R, Van Ravenzwaay B (2002) Investigations on cell proliferation and enzyme induction in male rat kidney and female mouse liver caused by tetrahydrofuran. Toxicol Sci 70:140–149

    CAS  PubMed  Google Scholar 

  • He Z, Xiao H, Tang L, Min H, Lu Z (2013) Biodegradation of di-n-butyl phthalate by a stable bacterial consortium, HD-1, enriched from activated sludge. Bioresour Technol 128:526–532

    CAS  PubMed  Google Scholar 

  • Hermida SA et al (2006) 2′-Deoxyguanosine, 2′-deoxycytidine, and 2′-deoxyadenosine adducts resulting from the reaction of tetrahydrofuran with DNA bases. Chem Res Toxicol 19:927–936

    CAS  PubMed  Google Scholar 

  • Hug LA, Beiko RG, Rowe AR, Richardson RE, Edwards EA (2012) Comparative metagenomics of three Dehalococcoides-containing enrichment cultures: the role of the non-dechlorinating community. BMC Genomics 13:327

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ikehata K, Wang-Staley L, Qu X, Li Y (2016) Treatment of groundwater contaminated with 1, 4-dioxane, tetrahydrofuran, and chlorinated volatile organic compounds using advanced oxidation processes. Ozone Sci Eng 38:413–424

    CAS  Google Scholar 

  • Isaacson C, Mohr TK, 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

    CAS  PubMed  Google Scholar 

  • Kılıç NK, Nielsen JL, Yüce M, Dönmez G (2007) Characterization of a simple bacterial consortium for effective treatment of wastewaters with reactive dyes and Cr(VI). Chemosphere 67:826–831

    PubMed  Google Scholar 

  • Kim D-J, Choi J-W, Choi N-C, Mahendran B, Lee C-E (2005) Modeling of growth kinetics for Pseudomonas spp. during benzene degradation. Appl Microbiol Biotechnol 69:456–462

    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

    CAS  PubMed  Google Scholar 

  • King E, Painter H (1983) Assessment of biodegradability of chemicals in water by manometric respirometry. Comm Eur Communities EUR 8631:31

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lan RS, Smith CA, Hyman MR (2013) Oxidation of cyclic ethers by alkane-grown Mycobacterium vaccae JOB5. Remediat J 23:23–42

    Google Scholar 

  • Larkin MJ, Kulakov LA, Allen CC (2006) Biodegradation by members of the genus Rhodococcus: biochemistry, physiology, and genetic adaptation. Adv Appl Microbiol 59:1–29

    CAS  PubMed  Google Scholar 

  • Lee K, Park J-W, Ahn I-S (2003) Effect of additional carbon source on naphthalene biodegradation by Pseudomonas putida G7. J Hazard Mater 105:157–167

    CAS  PubMed  Google Scholar 

  • Liu Z, He Z, Huang H, Ran X, Oluwafunmilayo AO, Lu Z (2017) pH Stress-induced cooperation between Rhodococcus ruber YYL and Bacillus cereus MLY1 in biodegradation of tetrahydrofuran. Front Microbiol 8:2297

    PubMed  PubMed Central  Google Scholar 

  • Luo J, Hein C, Mücklich F, Solioz M (2017) Killing of bacteria by copper, cadmium, and silver surfaces reveals relevant physicochemical parameters. Biointerphases 12:020301. https://doi.org/10.1116/1.4980127

    Article  CAS  PubMed  Google Scholar 

  • Maidak BL, Olsen GJ, Larsen N, Overbeek R, McCaughey MJ, Woese CR (1997) The RDP (ribosomal database project). Nucleic Acids Res 25:109–110

    CAS  PubMed  PubMed Central  Google Scholar 

  • Malley LA, Christoph GR, Stadler JC, Hansen JF, Biesemeier JA, Jasti SL (2001) Acute and subchronic neurotoxicological evaluation of tetrahydrofuran by inhalation in rats. Drug Chem Toxicol 24:201–219

    CAS  PubMed  Google Scholar 

  • Martínková L, Uhnáková B, Pátek M, Nešvera J, Křen V (2009) Biodegradation potential of the genus Rhodococcus. Environ Int 35:162–177

    PubMed  Google Scholar 

  • 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 22:312–316

    CAS  PubMed  Google Scholar 

  • McCutcheon JP, von Dohlen CD (2011) An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr Biol 21:1366–1372

    CAS  PubMed  PubMed Central  Google Scholar 

  • Metsger L, Bittner S (2000) Autocatalytic oxidation of ethers with sodium bromate. Tetrahedron 56:1905–1910

    CAS  Google Scholar 

  • Moody DE (1991) The effect of tetrahydrofuran on biological systems: does a hepatotoxic potential exist? Drug Chem Toxicol 14:319–342

    CAS  PubMed  Google Scholar 

  • Oh ST, Kim JR, Premier GC, Lee TH, Kim C, Sloan WT (2010) Sustainable wastewater treatment: how might microbial fuel cells contribute. Biotechnol Adv 28:871–881

    CAS  PubMed  Google Scholar 

  • Parales R, Adamus J, White N, May H (1994) Degradation of 1, 4-dioxane by an actinomycete in pure culture. Appl Environ Microbiol 60:4527–4530

    CAS  PubMed  PubMed Central  Google Scholar 

  • Phelan VV, Liu W-T, Pogliano K, Dorrestein PC (2012) Microbial metabolic exchange—the chemotype-to-phenotype link. Nat Chem Biol 8:26

    CAS  Google Scholar 

  • Saratale R, Saratale G, Kalyani D, Chang J-S, Govindwar S (2009) Enhanced decolorization and biodegradation of textile azo dye Scarlet R by using developed microbial consortium-GR. Bioresour Technol 100:2493–2500

    CAS  PubMed  Google Scholar 

  • Sathishkumar M, Binupriya AR, Baik SH, Yun SE (2008) Biodegradation of crude oil by individual bacterial strains and a mixed bacterial consortium isolated from hydrocarbon contaminated areas. Clean: Soil, Air, Water 36:92–96

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Skinner K, Cuiffetti L, Hyman M (2009) Metabolism and cometabolism of cyclic ethers by a filamentous fungus, a Graphium sp. Appl Environ Microbiol 75:5514–5522

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sprocati AR, Alisi C, Segre L, Tasso F, Galletti M, Cremisini C (2006) Investigating heavy metal resistance, bioaccumulation and metabolic profile of a metallophile microbial consortium native to an abandoned mine. Sci Total Environ 366:649–658

    CAS  PubMed  Google Scholar 

  • Stolyar S, Van Dien S, Hillesland KL, Pinel N, Lie TJ, Leigh JA, Stahl DA (2007) Metabolic modeling of a mutualistic microbial community. Mol Syst Biol 3:92

    PubMed  PubMed Central  Google Scholar 

  • Sun B, Ko K, Ramsay JA (2011) Biodegradation of 1, 4-dioxane by a Flavobacterium. Biodegradation 22:651–659

    CAS  PubMed  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

    CAS  Google Scholar 

  • Thavamani P, Megharaj M, Naidu R (2015) Metal-tolerant PAH-degrading bacteria: development of suitable test medium and effect of cadmium and its availability on PAH biodegradation. Environ Sci Pollut Res 22:8957–8968

    CAS  Google Scholar 

  • Thijs S, Weyens N, Sillen W, Gkorezis P, Carleer R, Vangronsveld J (2014) Potential for plant growth promotion by a consortium of stress-tolerant 2, 4-dinitrotoluene-degrading bacteria: isolation and characterization of a military soil. Microb Biotechnol 7:294–306

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wanapaisan P et al (2018) Synergistic degradation of pyrene by five culturable bacteria in a mangrove sediment-derived bacterial consortium. J Hazard Mater 342:561–570

    CAS  PubMed  Google Scholar 

  • Wang Y et al (2017) Biodegradation of di-n-butyl phthalate by bacterial consortium LV-1 enriched from river sludge. PLoS ONE 12:e0178213

    PubMed  PubMed Central  Google Scholar 

  • Xu Y, Chen X (2002) Recovering tetrahydrofuran from waste pharmaceutical liquor using new separation methods. Chem Eng (China) 30:17–19

    Google Scholar 

  • Yao Y, Lv Z, Min H, Lv Z, Jiao H (2009) Isolation, identification and characterization of a novel Rhodococcus sp. strain in biodegradation of tetrahydrofuran and its medium optimization using sequential statistics-based experimental designs. Bioresour Technol 100:2762–2769

    CAS  PubMed  Google Scholar 

  • Yao Y et al (2010) Assessment of toxicity of tetrahydrofuran on the microbial community in activated sludge. Bioresour Technol 101:5213–5221

    CAS  PubMed  Google Scholar 

  • Yao Y, Lu Z, Min H, Gao H, Zhu F (2012) The effect of tetrahydrofuran on the enzymatic activity and microbial community in activated sludge from a sequencing batch reactor. Ecotoxicology 21:56–65

    CAS  PubMed  Google Scholar 

  • Yu L, Cheng JM (2015) Effect of heavy metals Cu, Cd, Pb and Zn on enzyme activity and microbial biomass carbon in brown soil. Adv Mater Res 1073–1076:726–730

    Google Scholar 

  • Zagrodnik R, Łaniecki M (2017) The effect of pH on cooperation between dark-and photo-fermentative bacteria in a co-culture process for hydrogen production from starch. Int J Hydrog Energy 42:2878–2888

    CAS  Google Scholar 

  • Zelezniak A, Andrejev S, Ponomarova O, Mende DR, Bork P, Patil KR (2015) Metabolic dependencies drive species co-occurrence in diverse microbial communities. Proc Natl Acad Sci U S A 112:6449–6454

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Hu J, Zhu R, Zhou Q, Chen J (2013) Degradation of paracetamol by pure bacterial cultures and their microbial consortium. Appl Microbiol Biotechnol 97:3687–3698

    CAS  PubMed  Google Scholar 

  • Zhao H, Liu Q, Wang Y, Han Z, Chen Z, Mu Y (2018a) Biochar enhanced biological nitrobenzene reduction with a mixed culture in anaerobic systems: short-term and long-term assessments. Chem Eng J 351:912–921

    CAS  Google Scholar 

  • Zhao L et al (2018b) Co-contaminant effects on 1,4-dioxane biodegradation in packed soil column flow-through systems. Environ Pollut 243:573–581. https://doi.org/10.1016/j.envpol.2018.09.018

    Article  CAS  PubMed  Google Scholar 

  • Zhou K, Qiao K, Edgar S, Stephanopoulos G (2015) Distributing a metabolic pathway among a microbial consortium enhances production of natural products. Nat Biotechnol 33:377

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Nos. 41630637 and 41721001).

Author information

Authors and Affiliations

  1. MOE Laboratory of Biosystem Homeostasis and Protection, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, 310058, China

    Hui Huang, Minbo Qi, Zubi Liu, Haixia Wang & Zhenmei Lu

  2. Hangzhou Environmental Monitoring Center Station, Hangzhou, China

    Haixia Yu

Authors
  1. Hui Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Haixia Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Minbo Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zubi Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Haixia Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhenmei Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhenmei Lu.

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 (PDF 379 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, H., Yu, H., Qi, M. et al. Enrichment and characterization of a highly efficient tetrahydrofuran-degrading bacterial culture. Biodegradation 30, 467–479 (2019). https://doi.org/10.1007/s10532-019-09888-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10532-019-09888-5

Keywords

Search

Navigation