Skip to main content
Log in

The roles of methanogens and acetogens in dechlorination of trichloroethene using different electron donors

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

We evaluated the effects of methanogens and acetogens on the function and structure of microbial communities doing reductive dechlorination of trichloroethene (TCE) by adding four distinct electron donors: lactate, a fermentable organic; acetate, a non-fermentable organic; methanol, a fermentable 1-C (carbon) organic; and hydrogen gas (H2), the direct electron donor for reductive dechlorination by Dehalococcoides. The fermentable electron donors had faster dechlorination rates, more complete dechlorination, and higher bacterial abundances than the non-fermentable electron donors during short-term tests. Phylotypes of Dehalococcoides were relatively abundant (≥9 %) for the cultures fed with fermentable electron donors but accounted for only ~1–2 % of the reads for the cultures fed by the non-fermentable electron donors. Routing electrons to methanogenesis and a low ratio of Dehalococcoides/methanogenesis (Dhc/mcrA) were associated with slow and incomplete reductive dechlorination with methanol and H2. When fermentable substrates were applied as electron donors, a Dhc/mcrA ratio ≥6.4 was essential to achieve fast and complete dechlorination of TCE to ethene. When methanogenesis was suppressed using 2-bromoethanesulfonate (BES), achieving complete dechlorination of TCE to ethane required a minimum abundance of the mcrA gene. Methanobacterium appeared to be important for maintaining a high dechlorination rate, probably by providing Dehalococcoides with cofactors other than vitamin B12. Furthermore, the presence of homoacetogens also was important to maintain a high dechlorination rate, because they provided acetate as Dehalococcoides’s obligatory carbon source and possibly cofactors.

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

Similar content being viewed by others

References

  • Abelson PH (1990) Inefficient remediation of ground-water pollution. Science 250:733

    Article  CAS  Google Scholar 

  • Amos BK, Christ JA, Abriola LM, Pennell KD, Loeffler FE (2007) Experimental evaluation and mathematical modeling of microbially enhanced tetrachloroethene (PCE) dissolution. Environ Sci Technol 41:963–970

    Article  CAS  Google Scholar 

  • Aulenta F, Majone M, Verbo P, Tandoi V (2002) Complete dechlorination of tetrachloroethene to ethene in presence of methanogenesis and acetogenesis by an anaerobic sediment microcosm. Biodegradation 13:411–424

    Article  CAS  Google Scholar 

  • Aulenta F, Gossett JM, Papini MP, Rossetti S, Majone M (2005) Comparative study of methanol, butyrate, and hydrogen as electron donors for long-term dechlorination of tetrachloroethene in mixed anaerobic cultures. Biotechnol Bioeng 91:743–753

    Article  CAS  Google Scholar 

  • Aulenta F, Pera A, Rossetti S, Papini MP, Majone M (2007) Relevance of side reactions in anaerobic reductive dehalogenation microcosms amended with different electron donors. Water Res 41:27–38

    Article  CAS  Google Scholar 

  • Azizian MF, Marshall IPG, Behres S, Spormann AM, Semprini L (2010) Comparison of lactate, formate, and propionate as hydrogen donors for the reductive dehalogenation of trichloroethene in a continuous-flow column. J Contam Hydrol 113:77–92

    Article  CAS  Google Scholar 

  • Ballapragada BS, Stensel DH, Puhakka JA, Ferguson JF (1997) Effect of hydrogen on reductive dechlorination of chlorinated ethenes. Environ Sci Technol 31:1728–1734

    Article  CAS  Google Scholar 

  • Bennett P, Gandhi D, Warner S, Bussey J (2007) In situ reductive dechlorination of chlorinated ethenes in high nitrate groundwater. J Hazard Mater 149:568–573

    Article  CAS  Google Scholar 

  • Carr SC, Hughes JB (1998) Enrichment of high rate PCE dechlorination and comparative study of lactate, methanol, and hydrogen as electron donors to sustain activity. Environ Sci Technol 32:1817–1824

    Article  CAS  Google Scholar 

  • Chiu PC, Lee M (2001) 2-Bromoethanesulfonate affects bacteria in a trichloroethene-dechlorinating culture. Appl Environ Microbiol 67:2371–2374

    Article  CAS  Google Scholar 

  • Cupples AM, Spormann AM, McCarty PL (2003) Growth of a “Dehalococcoids”-like microorganisms on vinyl chloride and cis-dichloroethene as electron acceptors as determined by competitive PCR. Appl Environ Microbiol 69:953–959

    Article  CAS  Google Scholar 

  • De Wildeman S, Diekert G, van Langenhove H, Verstraete W (2003) Stereoselective microbial dehalorespiration with vicinal dechlorinated alkanes. Appl Environ Microbiol 69:5643–5647

    Article  Google Scholar 

  • Delgado AG, Parameswaran P, Fajardo-Williams D, Halden RU, Krajmalnik-Brown R (2012) Role of bicarbonate as a pH buffer and electron sink in microbial dechlorination of chloroethene. Microb Cell Fact 11:128

    Article  CAS  Google Scholar 

  • Duhamel M, Edwards EA (2007) Growth and yields of dechlorinators, acetogens, and methanogens during reductive dechlorination of chlorinated ethenes and dihaloelimination of 1,2-dichloroethene. Environ Sci Technol 41:2303–2310

    Article  CAS  Google Scholar 

  • Duhamel M, Mo K, Edwards EA (2004) Characterization of a highly enriched Dehalococcoides-containing culture that grows on vinyl chloride and trichloroethene. Appl Environ Microbiol 70:5538–5545

    Article  CAS  Google Scholar 

  • El Fantroussi S, Naveau H, Agathos SN (1998) Anaerobic dechlorinating bacteria. Biotechnol Progr 14:167–188

    Article  CAS  Google Scholar 

  • US Environmental Protection Agency (2000) "Trichloroethylene Hazard Summary." http://www.epa.gov/ttn/atw/hlthef/tri-ethy.html.

  • US Environmental Protection Agency (2007) National Primary Drinking Water Regulations. http://water.epa.gov/drink/contaminants/index.cfm

  • Fennell DE, Gossett JM (2003) Microcosms for site-specific evaluation of enhanced biological reductive dehalogenation. In: Haggblom M, Bossert ID (eds) Dehalogenation, microbial processes and environmental applications. Kluwer Academic Publishers, Boston, pp 385–420

    Google Scholar 

  • Fennell DE, Gossett JM, Zinder SH (1997) Comparison of butyric acid, ethanol, lactic acid, and propionic acid as hydrogen donors for the reductive dechlorination of tetrachloroethene. Environ Sci Technol 31:918–926

    Article  CAS  Google Scholar 

  • Freeborn RA, West KA, Bhupathiraju VK, Chauhan S, Rham BG, Richardson RE, Alvarez-Cohen L (2005) Phylogenetic analysis of TCE-dechlorinating consortia enriched on a variety of electron donors. Environ Sci Technol 39:8358–8368

    Article  CAS  Google Scholar 

  • He JZ, Sung Y, Dollhopf ME, Fathepure BZ, Tiedje JM, Loeffler FE (2002) Acetate versus hydrogen as direct electron donor to stimulate the microbial reductive dechlorination process at chloroethene-contaminated sites. Environ Sci Technol 36:3945–3952

    Article  CAS  Google Scholar 

  • He JZ, Ritalahti KM, Yang KL, Koenigsberg SS, Loeffler FE (2003) Detoxification of vinyl chloride to ethane coupled to growth of an anaerobic bacterium. Nature 424:62–65

    Article  CAS  Google Scholar 

  • He JZ, Sung Y, Krajmalnik-Brown R, Ritalahti KM, Loeffler FE (2005) Isolation and characterization of Dehalococcoides sp. strain FL2, a trichloroethene (TCE)- and 1,2-dichloroethene-respiring anaerobe. Environ Microbiol 7:1442–1450

    Article  CAS  Google Scholar 

  • He JZ, Holmes VF, Lee PKH, Alvarez-Cohen L (2007) Influence of vitamin B-12 and cocultures on the growth of Dehalococcoides isolates in defined medium. Appl Environ Microbiol 73:2847–2853

    Article  CAS  Google Scholar 

  • Heimann A, Friis AK, Jakobsen R (2005) Effects of sulfate on anaerobic chloroethene degradation by an enriched culture under transient and steady-state hydrogen supply. Water Res 39:3579–3586

    Article  CAS  Google Scholar 

  • Heimann AC, Friis AK, Scheutz C, Jakobsen R (2007) Dynamics of reductive TCE dehalogenation in two distinct H2 supply scenarios and at various temperatures. Biodegradation 18:167–179

    Article  CAS  Google Scholar 

  • Holliger C, Schraa G, Stupperich E, Stams AJM, Zehnder AJB (1992a) Evidence for the involvement of corrinoids and factor F430 in the reductive Dechlorination of 1,2-dichloroethane by Methanosarcina barkeri. J Bacteriol 174:4427–4434

    CAS  Google Scholar 

  • Holliger C, Kengen SWM, Schraa G, Stams AJM, Zehnder AJB (1992b) Methyl-coenzyme M reductase of Methanobacterium thermoautotrophicum ΔH catalyzes the reductive dechlorination of 1,2-dichloroethane to ethylene and chloroethane. J Bacteriol 174:4435–4443

    CAS  Google Scholar 

  • Johnson DR, Nemir A, Andersen GL, Zinder SH, Alvarez-Cohen L (2009) Transcriptomic microarray analysis of corrinoid responsive genes in Dehalococcoides ethengenes strain 195. FEMS Microbiol Lett 294:198–206

    Article  CAS  Google Scholar 

  • Kranzioch I, Stoll C, Holbach A, Chen H, Wang LJ, Zheng BH, Norra S, Bi YH, Schramm KW, Tiehm A (2013) Dechlorination and organohalide-respiring bacteria dynamics in sediment samples of the Yangtze Three Gorges Reservoir. Environ Sci Pollut Res 20:7046–7056

    Article  CAS  Google Scholar 

  • Krumholz LR (1997) Desulfuromonas chloroethenica sp. nov. uses tetrachloroethylene and trichloroethylene as electron acceptors. Int J Syst Bateriol 47:1262–1263

    Article  CAS  Google Scholar 

  • Lai CY, Yang X, Tang Y, Rittmann BE, Zhao HP (2014) Nitrate shaped selenate reducing microbial community in a hydrogen-based biofilm reactor. Environ Sci Technol 48:3395–3402

    Article  CAS  Google Scholar 

  • Lee LS, Bae JH, McCarty PL (2007) Comparison between acetate and hydrogen as electron donors and implications for the reductive dehalogenation of PCE and TCE. J Contam Hydrol 94:76–85

    Article  CAS  Google Scholar 

  • Lendvay JM, Loeffler FE, Dollhopf M, Aiello MR, Daniels G, Fathepure BZ, Gebhard M, Heine R, Helton R, Shi J, Krajmalnik-Brown R, Major D, Jr L, Barcelona MJ, Petrovskis E, Hickey R, Tiedje JM, Adrianes P (2003) Bioreactive barriers: a comparison of bioaugmentation and biostimulation for chlorinated solvent remediation. Environ Sci Technol 37:1422–1431

    Article  CAS  Google Scholar 

  • Lock EA, Reed CJ (2006) Trichloroethylene: mechanisms of renal toxicity and renal cancer and relevance to risk assessment. Toxicol Sci 91:313–331

    Article  CAS  Google Scholar 

  • Loeffler FE, Ritalahti KM, Tiedje JM (1997) Dechlorination of chloroethenes is inhibited by 2-bromoethanesulfonate in the absence of methanogens. Appl Environ Microbiol 63:4982–4985

    Google Scholar 

  • Ma X, Novak PJ, Clapp LW, Semmens MJ, Hozalski RM (2003) Evaluation of polyethylene hollow-fiber membranes for hydrogen delivery to support reductive dechlorination in a soil column. Water Res 37:2905–2918

    Article  CAS  Google Scholar 

  • Maeda H, Fujimoto C, Haruki Y, Maeda T, Kokeguchi S, Petelin M, Arai H, Tanimoto I, Nishimura F, Takashiba S (2003) Quantitative real-time PCR using TaqMan and SYBR Green for Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, Prevotella intermedia, tetQ gene and total bacteria. FEMS Immunol Med Mic 39:81–86

    Article  CAS  Google Scholar 

  • Maymo-Gatell X, Tandoi V, Gossett JM, Zinder SH (1995) Characterization of an H2-utilizing enrichment culture that reductively dechlorinates tetrachloroethene to vinyl chloride and ethene in the absence of methanogenesis and acetogenesis. Appl Environ Microbiol 61:3928–3933

    CAS  Google Scholar 

  • Men Y, Feil H, VerBerkmoes NC, Shah MB, Johnson DR, Lee PKH, West KA, Zinder SH, Andersen GL, Alvarez-Cohen L (2012) Sustainable syntrophic growth of Dehaloccoides ethenogenes strain 195 with Desulfovibrio vulgaris Hildenborough and Methanobacterium congolense: global transcriptomic and proteomic analysis. ISME J 6:410–421

    Article  CAS  Google Scholar 

  • Men Y, Lee PKH, Harding KC, Alvarez-Cohen L (2013) Characterization of four TCE-dechlorinating microbial enrichments grown with different cobalamin stress and methanogenic conditions. Appl Microbial Biotechnol 97:6439–6450

    Article  CAS  Google Scholar 

  • Panagiotakis I, Mamais D, Pantazidou M, Marneri M, Parapouli M, Hatziloukas E, Tandoi V (2007) Dechlorinating ability of TCE-fed microcosms with different electron donors. J Hazard Mater 149:582–589

    Article  CAS  Google Scholar 

  • Parameswaran P, Torres CI, Lee HS, Rittmann BE, Krajmalnik-Brown R (2011) Hydrogen consumption in microbial electrochemical systems (MXCs): the role of homo-acetogenic bacteria. Bioresource Technol 102:263–271

    Article  CAS  Google Scholar 

  • Raskin L, Stromley JM, Rittmann BE, Stahl DA (1994) Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens. Appl Environ Microbiol 60:1232–1240

    CAS  Google Scholar 

  • Smidt H, de Vos WM (2004) Anaerobic microbial dehalogenation. Annu Rev Microbiol 58:43–73

    Article  CAS  Google Scholar 

  • Stupperich E, Eisinger HJ, Krautler B (1988) Diversity of corrinoids in acetogenic bacteria-P-Cresolylcobamide from Sporomusa ovata, 5-methoxy-6-methylbenzimidazolycobamide from Clostridium formicoaceticum and vitamin B from Acetobacterium woodii. Eur J Biochem 172:459–464

    Article  CAS  Google Scholar 

  • Sung Y, Ritalahti KM, Apkarian RP, Loeffler FE (2006) Quantitative PCR confirms purity of strain GT, a novel trichloroethene-to-ethene-respiring Dehalococcoides isolate. Appl Environ Microbiol 72:1980–1987

    Article  CAS  Google Scholar 

  • Tang YJ, Yi S, Zhuang WQ, Zinder SH, Keasling JD, Alvarez-Cohen L (2009) Investigation of carbon metabolism in “Dehalococcoides ethenogenes” strain 195 by use of isotopomer and transcriptomic analyses. J Bacteriol 191:5224–5231

    Article  CAS  Google Scholar 

  • Wei N, Finneran KT (2013) Low and high acetate amendments are equally as effective at promoting complete dechlorination of trichloroethylene (TCE). Biodegradation 24:413–425

    Article  CAS  Google Scholar 

  • Yan J, Ritalahti KM, Wagner DD, Loeffler FE (2012) Unexpected specificity of interspecies cobamide transfer from Geobacter spp. to organohalde-respiring Dehalococcoides mccartyi strains. Appl Environ Microbiol 78:6630–6636

    Article  CAS  Google Scholar 

  • Yang Y, McCarty PL (1998) Competition for hydrogen within a chlorinated solvent dehalogenating anaerobic mixed culture. Environ Sci Technol 32:3591–3597

    Article  CAS  Google Scholar 

  • Yang Y, McCarty PL (2002) Comparison between donor substrates for biologically enhanced tetrachloroethene DNAPL dissolution. Environ Sci Technol 36:3400–3404

    Article  CAS  Google Scholar 

  • Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89:670–679

    Article  CAS  Google Scholar 

  • Zhao HP, Van Ginkel S, Kang D-W, Rittmann BE, Krajmalnik-Brown R (2011) Interactions between perchlorate and nitrate reductions in the biofilm of a hydrogen-based membrane biofilm reactor. Environ Sci Technol 45:10155–10162

    Article  CAS  Google Scholar 

  • Ziv-El M, Delgado AG, Yao Y, Kang DW, Nelson KG, Halden RU, Krajmalnik-Brown R (2011) Development and characterization of DehaloR^2, a novel anaerobic microbial consortium performing rapid dechlorination of TCE to ethene. Appl Microbiol Biotechnol 92:1063–1071

    Article  CAS  Google Scholar 

  • Ziv-El M, Popat SC, Parameswaran P, Kang DW, Alexandra P, Halden RU, Rittmann BE, Krajmalnik-Brown R (2012) Using electron balances and molecular techniques to assess trichloroethene-induced shifts to a dechlorinating microbial community. Biotechnol Bioengineer 109:2230–2239

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the “National Natural Science Foundation of China (Grant No. 21107091, and 21377109)” and the “Fundamental Research Funds for the Central Universities (2014FZA6008).” We thank Dr. Andreas Tiehm from TZW for kindly providing the culture for the research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to He-Ping Zhao.

Additional information

Responsible editor: Gerald Thouand

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 267 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wen, LL., Zhang, Y., Pan, YW. et al. The roles of methanogens and acetogens in dechlorination of trichloroethene using different electron donors. Environ Sci Pollut Res 22, 19039–19047 (2015). https://doi.org/10.1007/s11356-015-5117-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-5117-z

Keywords

Navigation