Mineralization versus fermentation: evidence for two distinct anaerobic bacterial degradation pathways for dichloromethane
Abstract
Dichloromethane (DCM) is an anthropogenic pollutant with ozone destruction potential that is also formed naturally. Under anoxic conditions, fermentation of DCM to acetate and formate has been reported in axenic culture Dehalobacterium formicoaceticum, and to acetate, H2 and CO2 in mixed culture RM, which harbors the DCM degrader ‘Candidatus Dichloromethanomonas elyunquensis’. RM cultures produced 28.1 ± 2.3 μmol of acetate from 155.6 ± 9.3 μmol DCM, far less than the one third (i.e., about 51.9 µmol) predicted based on the assumed fermentation model, and observed in cultures of Dehalobacterium formicoaceticum. Temporal metabolite analyses using gas chromatography-mass spectrometry (GC-MS) and nuclear magnetic resonance (NMR) spectroscopy revealed that no 13C-labeled acetate was formed in 13C-DCM-grown RM cultures, indicating acetate was not a direct product of DCM metabolism. The data were reconciled with DCM mineralization and H2 consumption via CO2 reduction to acetate and methane by homoacetogenic and methanogenic partner populations, respectively. In contrast, Dehalobacterium formicoaceticum produced 13C-labeled acetate and formate from 13C-DCM, consistent with a fermentation pathway. Free energy change calculations predicted that organisms with the mineralization pathway are the dominant DCM consumers in environments with H2 <100 ppmv. These findings have implications for carbon and electron flow in environments where DCMmore »
- Authors:
-
- Univ. of Tennessee, Knoxville, TN (United States). Center for Environmental Biotechnology and Dept. of Civil and Environmental Engineering
- Univ. of Tennessee, Knoxville, TN (United States). Dept. of Chemistry
- Corteva Agriscience, Wilmington, DE (United States)
- The Chemours Company, Wilmington, DE (United States). Chemours Corporate Remediation Group
- Univ. of Tennessee, Knoxville, TN (United States). Center for Environmental Biotechnology, Dept. of Civil and Environmental Engineering, Dept. of Chemistry, Dept. of Microbiology, and Dept. of Biosystems; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Joint Institute for Computational Sciences (JIBS)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1606041
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The ISME Journal
- Additional Journal Information:
- Journal Volume: 14; Journal Issue: 4; Journal ID: ISSN 1751-7362
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Chen, Gao, Fisch, Alexander R., Gibson, Caleb M., Erin Mack, E., Seger, Edward S., Campagna, Shawn R., and Löffler, Frank E. Mineralization versus fermentation: evidence for two distinct anaerobic bacterial degradation pathways for dichloromethane. United States: N. p., 2020.
Web. doi:10.1038/s41396-019-0579-5.
Chen, Gao, Fisch, Alexander R., Gibson, Caleb M., Erin Mack, E., Seger, Edward S., Campagna, Shawn R., & Löffler, Frank E. Mineralization versus fermentation: evidence for two distinct anaerobic bacterial degradation pathways for dichloromethane. United States. https://doi.org/10.1038/s41396-019-0579-5
Chen, Gao, Fisch, Alexander R., Gibson, Caleb M., Erin Mack, E., Seger, Edward S., Campagna, Shawn R., and Löffler, Frank E. Mon .
"Mineralization versus fermentation: evidence for two distinct anaerobic bacterial degradation pathways for dichloromethane". United States. https://doi.org/10.1038/s41396-019-0579-5. https://www.osti.gov/servlets/purl/1606041.
@article{osti_1606041,
title = {Mineralization versus fermentation: evidence for two distinct anaerobic bacterial degradation pathways for dichloromethane},
author = {Chen, Gao and Fisch, Alexander R. and Gibson, Caleb M. and Erin Mack, E. and Seger, Edward S. and Campagna, Shawn R. and Löffler, Frank E.},
abstractNote = {Dichloromethane (DCM) is an anthropogenic pollutant with ozone destruction potential that is also formed naturally. Under anoxic conditions, fermentation of DCM to acetate and formate has been reported in axenic culture Dehalobacterium formicoaceticum, and to acetate, H2 and CO2 in mixed culture RM, which harbors the DCM degrader ‘Candidatus Dichloromethanomonas elyunquensis’. RM cultures produced 28.1 ± 2.3 μmol of acetate from 155.6 ± 9.3 μmol DCM, far less than the one third (i.e., about 51.9 µmol) predicted based on the assumed fermentation model, and observed in cultures of Dehalobacterium formicoaceticum. Temporal metabolite analyses using gas chromatography-mass spectrometry (GC-MS) and nuclear magnetic resonance (NMR) spectroscopy revealed that no 13C-labeled acetate was formed in 13C-DCM-grown RM cultures, indicating acetate was not a direct product of DCM metabolism. The data were reconciled with DCM mineralization and H2 consumption via CO2 reduction to acetate and methane by homoacetogenic and methanogenic partner populations, respectively. In contrast, Dehalobacterium formicoaceticum produced 13C-labeled acetate and formate from 13C-DCM, consistent with a fermentation pathway. Free energy change calculations predicted that organisms with the mineralization pathway are the dominant DCM consumers in environments with H2 <100 ppmv. These findings have implications for carbon and electron flow in environments where DCM is introduced through natural production processes or anthropogenic activities.},
doi = {10.1038/s41396-019-0579-5},
journal = {The ISME Journal},
number = 4,
volume = 14,
place = {United States},
year = {Mon Jan 06 00:00:00 EST 2020},
month = {Mon Jan 06 00:00:00 EST 2020}
}
Web of Science
Works referenced in this record:
Acetogenesis and the Wood–Ljungdahl pathway of CO2 fixation
journal, December 2008
- Ragsdale, Stephen W.; Pierce, Elizabeth
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1784, Issue 12, p. 1873-1898
Anaerobic Microbial Dehalogenation
journal, October 2004
- Smidt, Hauke; de Vos, Willem M.
- Annual Review of Microbiology, Vol. 58, Issue 1
Acetogenesis in the Energy-Starved Deep Biosphere – A Paradox?
journal, January 2012
- Lever, Mark Alexander
- Frontiers in Microbiology, Vol. 2
The production and global distribution of emissions of trichloroethene, tetrachloroethene and dichloromethane over the period 1988–1992
journal, February 1996
- McCulloch, Archie; Midgley, Pauline M.
- Atmospheric Environment, Vol. 30, Issue 4
Reductive Dechlorination of cis -1,2-Dichloroethene and Vinyl Chloride by “ Dehalococcoides ethenogenes ”
journal, February 2001
- Maymó-Gatell, Xavier; Nijenhuis, Ivonne; Zinder, Stephen H.
- Environmental Science & Technology, Vol. 35, Issue 3
Energetics and Application of Heterotrophy in Acetogenic Bacteria
journal, May 2016
- Schuchmann, Kai; Müller, Volker
- Applied and Environmental Microbiology, Vol. 82, Issue 14
Hydrogen or formate: Alternative key players in methanogenic degradation: Hydrogen/formate as interspecies electron carriers
journal, March 2017
- Schink, Bernhard; Montag, Dominik; Keller, Anja
- Environmental Microbiology Reports, Vol. 9, Issue 3
Increasing concentrations of dichloromethane, CH 2 Cl 2 , inferred from CARIBIC air samples collected 1998–2012
journal, January 2015
- Leedham Elvidge, E. C.; Oram, D. E.; Laube, J. C.
- Atmospheric Chemistry and Physics, Vol. 15, Issue 4
Integration of organohalide-respiring bacteria and nanoscale zero-valent iron (Bio-nZVI-RD): A perfect marriage for the remediation of organohalide pollutants?
journal, December 2016
- Wang, Shanquan; Chen, Siyuan; Wang, Yu
- Biotechnology Advances, Vol. 34, Issue 8
A targeted metabolomic protocol for short-chain fatty acids and branched-chain amino acids
journal, February 2013
- Zheng, Xiaojiao; Qiu, Yunping; Zhong, Wei
- Metabolomics, Vol. 9, Issue 4
Evidence for methanogenic Archaea and homoacetogenic Bacteria in deep granitic rock aquifers
journal, July 1997
- Kotelnikova, Svetlana; Pedersen, Karsten
- FEMS Microbiology Reviews, Vol. 20, Issue 3-4
Dual Carbon–Chlorine Isotope Analysis Indicates Distinct Anaerobic Dichloromethane Degradation Pathways in Two Members of Peptococcaceae
journal, June 2018
- Chen, Gao; Shouakar-Stash, Orfan; Phillips, Elizabeth
- Environmental Science & Technology, Vol. 52, Issue 15
A targeted metabolomic protocol for short-chain fatty acids and branched-chain amino acids
text, January 2013
- Yunping, Qiu,; Wei, Jia,; Qiong, Li,
- The University of North Carolina at Chapel Hill University Libraries
Isolation and characterization of Dehalobacterium formicoaceticum gen. nov. sp. nov., a strictly anaerobic bacterium utilizing dichloromethane as source of carbon and energy
journal, August 1996
- Mägli, Andreas; Wendt, Matthias; Leisinger, T.
- Archives of Microbiology, Vol. 166, Issue 2
Methanol conversion in high-rate anaerobic reactors
journal, October 2001
- Weijma, J.; Stams, A. J. M.
- Water Science and Technology, Vol. 44, Issue 8
Bioaugmentation with Distinct Dehalobacter Strains Achieves Chloroform Detoxification in Microcosms
journal, January 2014
- Justicia-Leon, Shandra D.; Higgins, Steven; Mack, E. Erin
- Environmental Science & Technology, Vol. 48, Issue 3
Dichloromethane utilized by an anaerobic mixed culture: acetogenesis and methanogenesis
journal, January 1991
- Stromeyer, Susanna A.; Winkelbauer, Wolfgang; Kohler, Herbert
- Biodegradation, Vol. 2, Issue 2
Growth Characteristics and Thermodynamics of Syntrophic Acetate Oxidizers
journal, April 2019
- Westerholm, Maria; Dolfing, Jan; Schnürer, Anna
- Environmental Science & Technology, Vol. 53, Issue 9
‘ Candidatus Dichloromethanomonas elyunquensis’ gen. nov., sp. nov., a dichloromethane-degrading anaerobe of the Peptococcaceae family
journal, April 2017
- Kleindienst, Sara; Higgins, Steven A.; Tsementzi, Despina
- Systematic and Applied Microbiology, Vol. 40, Issue 3
Dehalococcoides mccartyi gen. nov., sp. nov., obligately organohalide-respiring anaerobic bacteria relevant to halogen cycling and bioremediation, belong to a novel bacterial class, Dehalococcoidia classis nov., order Dehalococcoidales ord. nov. and family Dehalococcoidaceae fam. nov., within the phylum Chloroflexi
journal, April 2012
- Loffler, F. E.; Yan, J.; Ritalahti, K. M.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 2
Relative Contributions of Dehalobacter and Zerovalent Iron in the Degradation of Chlorinated Methanes
journal, March 2015
- Lee, Matthew; Wells, Eliza; Wong, Yie Kuan
- Environmental Science & Technology, Vol. 49, Issue 7
Mutualistic interaction between dichloromethane- and chloromethane-degrading bacteria in an anaerobic mixed culture: Mutualistic degradation of chlorinated methanes
journal, October 2017
- Chen, Gao; Kleindienst, Sara; Griffiths, Daniel R.
- Environmental Microbiology, Vol. 19, Issue 11
The increasing threat to stratospheric ozone from dichloromethane
journal, June 2017
- Hossaini, Ryan; Chipperfield, Martyn P.; Montzka, Stephen A.
- Nature Communications, Vol. 8, Issue 1
Microbial syntrophy: interaction for the common good
journal, May 2013
- Morris, Brandon E. L.; Henneberger, Ruth; Huber, Harald
- FEMS Microbiology Reviews, Vol. 37, Issue 3
Methyl chloride metabolism of the strictly anaerobic, methyl chloride-utilizing homoacetogen strain MC
journal, November 1993
- Me�mer, Michael; Wohlfarth, Gert; Diekert, Gabriele
- Archives of Microbiology, Vol. 160, Issue 5
Energetics of syntrophic cooperation in methanogenic degradation.
journal, January 1997
- Schink, B.
- Microbiology and molecular biology reviews : MMBR, Vol. 61, Issue 2
Life with Carbon Monoxide
journal, January 2004
- Ragsdale, Stephen W.
- Critical Reviews in Biochemistry and Molecular Biology, Vol. 39, Issue 3
Composite global emissions of reactive chlorine from anthropogenic and natural sources: Reactive Chlorine Emissions Inventory
journal, April 1999
- Keene, William. C.; Khalil, M. Aslam K.; Erickson, David. J.
- Journal of Geophysical Research: Atmospheres, Vol. 104, Issue D7
Complete chloroform dechlorination by organochlorine respiration and fermentation: Microbial chloroform metabolism
journal, November 2011
- Lee, Matthew; Low, Adrian; Zemb, Olivier
- Environmental Microbiology, Vol. 14, Issue 4
Methanol metabolism in the acetogenic bacterium Acetobacterium woodii
journal, October 2018
- Kremp, Florian; Poehlein, Anja; Daniel, Rolf
- Environmental Microbiology, Vol. 20, Issue 12
[NiFe] hydrogenases: A common active site for hydrogen metabolism under diverse conditions
journal, August 2013
- Shafaat, Hannah S.; Rüdiger, Olaf; Ogata, Hideaki
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 8-9
Determination of chloromethane and dichloromethane in a tropical terrestrial mangrove forest in Brazil by measurements and modelling
journal, January 2018
- Kolusu, S. R.; Schlünzen, K. H.; Grawe, D.
- Atmospheric Environment, Vol. 173
Control on rate and pathway of anaerobic organic carbon degradation in the seabed
journal, December 2017
- Beulig, F.; Røy, H.; Glombitza, C.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 2
Methanogenesis and the Wood–Ljungdahl Pathway: An Ancient, Versatile, and Fragile Association
journal, May 2016
- Borrel, Guillaume; Adam, Panagiotis S.; Gribaldo, Simonetta
- Genome Biology and Evolution, Vol. 8, Issue 6
Chloromethane and dichloromethane in the tropical Atlantic Ocean
journal, February 2017
- Kolusu, Seshagiri Rao; Schlünzen, K. Heinke; Grawe, David
- Atmospheric Environment, Vol. 150
Growth in stratospheric chlorine from short‐lived chemicals not controlled by the Montreal Protocol
journal, June 2015
- Hossaini, R.; Chipperfield, M. P.; Saiz‐Lopez, A.
- Geophysical Research Letters, Vol. 42, Issue 11
Molecular and carbon isotopic characterization of an anaerobic stable enrichment culture containing Dehalobacterium sp. during dichloromethane fermentation
journal, March 2017
- Trueba-Santiso, Alba; Parladé, Eloi; Rosell, Mònica
- Science of The Total Environment, Vol. 581-582
Chlorinated Solvents in Groundwater of the United States
journal, January 2007
- Moran, Michael J.; Zogorski, John S.; Squillace, Paul J.
- Environmental Science & Technology, Vol. 41, Issue 1
The increasing threat to stratospheric ozone from dichloromethane.
text, January 2017
- Hossaini, Ryan; Chipperfield, Martyn P.; Montzka, Stephen A.
- Apollo - University of Cambridge Repository
CO2 fixation by anaerobic non-photosynthetic mixotrophy for improved carbon conversion
journal, September 2016
- Jones, Shawn W.; Fast, Alan G.; Carlson, Ellinor D.
- Nature Communications, Vol. 7, Issue 1
The mechanism of inhibition by H2 of H2-evolution by hydrogenases
journal, January 2013
- Fourmond, Vincent; Baffert, Carole; Sybirna, Kateryna
- Chemical Communications, Vol. 49, Issue 61
The elusive roles of bacterial glutathione S- transferases: new lessons from genomes
journal, January 2002
- Pagni, S. Vuilleumier, M.
- Applied Microbiology and Biotechnology, Vol. 58, Issue 2
Fraction of Electrons Consumed in Electron Acceptor Reduction and Hydrogen Thresholds as Indicators of Halorespiratory Physiology
journal, January 1999
- Löffler, Frank E.; Tiedje, James M.; Sanford, Robert A.
- Applied and Environmental Microbiology, Vol. 65, Issue 9
Hydrogenases
journal, March 2014
- Lubitz, Wolfgang; Ogata, Hideaki; Rüdiger, Olaf
- Chemical Reviews, Vol. 114, Issue 8
CO2 conversion to methane and biomass in obligate methylotrophic methanogens in marine sediments
journal, April 2019
- Yin, Xiuran; Wu, Weichao; Maeke, Mara
- The ISME Journal, Vol. 13, Issue 8
Metabolism of Dichloromethane by the Strict Anaerobe Dehalobacterium formicoaceticum
journal, January 1998
- Mägli, Andreas; Messmer, Michael; Leisinger, Thomas
- Applied and Environmental Microbiology, Vol. 64, Issue 2
Glycine synthase of the purinolytic bacterium, Clostridium acidiurici. Purification of the glycine-CO2 exchange system.
journal, May 1984
- Gariboldi, R. T.; Drake, H. L.
- Journal of Biological Chemistry, Vol. 259, Issue 10
Dehalococcoides mccartyi gen. nov., sp. nov., obligately organohalide-respiring anaerobic bacteria relevant to halogen cycling and bioremediation, belong to a novel bacterial class, Dehalococcoidia classis nov., order Dehalococcoidales ord. nov. and family Dehalococcoidaceae fam. nov., within the phylum Chloroflexi
journal, June 2015
- Müller, Jochen A.; Fullerton, Heather; Zinder, Stephen H.
- International Journal of Systematic and Evolutionary Microbiology, Vol. 65, Issue 6