Mineralization versus fermentation: evidence for two distinct anaerobic bacterial degradation pathways for dichloromethane

Chen, Gao; Fisch, Alexander R.; Gibson, Caleb M.; Erin Mack, E.; Seger, Edward S.; Campagna, Shawn R.; Löffler, Frank E.

doi:10.1038/s41396-019-0579-5

Mineralization versus fermentation: evidence for two distinct anaerobic bacterial degradation pathways for dichloromethane

Journal Article · Mon Jan 06 00:00:00 EST 2020 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-019-0579-5· OSTI ID:1606041

Chen, Gao ^[1]; Fisch, Alexander R. ^[2]; Gibson, Caleb M. ^[2]; Erin Mack, E. ^[3]; Seger, Edward S. ^[4]; Campagna, Shawn R. ^[2]; ^[5]

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)

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.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1606041

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 4 Vol. 14; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (56)

Growth in stratospheric chlorine from short‐lived chemicals not controlled by the Montreal Protocol Hossaini, R.; Chipperfield, M. P.; Saiz‐Lopez, A. Geophysical Research Letters, Vol. 42, Issue 11 https://doi.org/10.1002/2015GL063783	journal	June 2015
Dichloromethane utilized by an anaerobic mixed culture: acetogenesis and methanogenesis Stromeyer, Susanna A.; Winkelbauer, Wolfgang; Kohler, Herbert Biodegradation, Vol. 2, Issue 2 https://doi.org/10.1007/BF00114603	journal	January 1991
Methyl chloride metabolism of the strictly anaerobic, methyl chloride-utilizing homoacetogen strain MC Me�mer, Michael; Wohlfarth, Gert; Diekert, Gabriele Archives of Microbiology, Vol. 160, Issue 5 https://doi.org/10.1007/BF00252225	journal	November 1993
Microbes, enzymes and genes involved in dichloromethane utilization Leisinger, Thomas; Bader, Regula; Hermann, Ren� Biodegradation, Vol. 5, Issue 3-4 https://doi.org/10.1007/BF00696462	journal	December 1994
Isolation and characterization of Dehalobacterium formicoaceticum gen. nov. sp. nov., a strictly anaerobic bacterium utilizing dichloromethane as source of carbon and energy Mägli, Andreas; Wendt, Matthias; Leisinger, T. Archives of Microbiology, Vol. 166, Issue 2 https://doi.org/10.1007/s002030050362	journal	August 1996
The elusive roles of bacterial glutathione S- transferases: new lessons from genomes Pagni, S. Vuilleumier, M. Applied Microbiology and Biotechnology, Vol. 58, Issue 2 https://doi.org/10.1007/s00253-001-0836-0	journal	January 2002
A targeted metabolomic protocol for short-chain fatty acids and branched-chain amino acids Zheng, Xiaojiao; Qiu, Yunping; Zhong, Wei Metabolomics, Vol. 9, Issue 4 https://doi.org/10.1007/s11306-013-0500-6	journal	February 2013
The production and global distribution of emissions of trichloroethene, tetrachloroethene and dichloromethane over the period 1988–1992 McCulloch, Archie; Midgley, Pauline M. Atmospheric Environment, Vol. 30, Issue 4 https://doi.org/10.1016/1352-2310(09)50032-5	journal	February 1996
Glycine synthase of the purinolytic bacterium, Clostridium acidiurici. Purification of the glycine-CO2 exchange system. Gariboldi, R. T.; Drake, H. L. Journal of Biological Chemistry, Vol. 259, Issue 10 https://doi.org/10.1016/S0021-9258(20)82108-5	journal	May 1984
Enrichment, Cultivation, and Detection of Reductively Dechlorinating Bacteria Löffler, Frank E.; Sanford, Robert A.; Ritalahti, Kirsti M. Methods in Enzymology https://doi.org/10.1016/S0076-6879(05)97005-5	book	January 2005
Chloromethane and dichloromethane in the tropical Atlantic Ocean Kolusu, Seshagiri Rao; Schlünzen, K. Heinke; Grawe, David Atmospheric Environment, Vol. 150 https://doi.org/10.1016/j.atmosenv.2016.11.037	journal	February 2017
Determination of chloromethane and dichloromethane in a tropical terrestrial mangrove forest in Brazil by measurements and modelling Kolusu, S. R.; Schlünzen, K. H.; Grawe, D. Atmospheric Environment, Vol. 173 https://doi.org/10.1016/j.atmosenv.2017.10.057	journal	January 2018
[NiFe] hydrogenases: A common active site for hydrogen metabolism under diverse conditions Shafaat, Hannah S.; Rüdiger, Olaf; Ogata, Hideaki Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 8-9 https://doi.org/10.1016/j.bbabio.2013.01.015	journal	August 2013
Acetogenesis and the Wood–Ljungdahl pathway of CO₂ fixation Ragsdale, Stephen W.; Pierce, Elizabeth Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1784, Issue 12, p. 1873-1898 https://doi.org/10.1016/j.bbapap.2008.08.012	journal	December 2008
Integration of organohalide-respiring bacteria and nanoscale zero-valent iron (Bio-nZVI-RD): A perfect marriage for the remediation of organohalide pollutants? Wang, Shanquan; Chen, Siyuan; Wang, Yu Biotechnology Advances, Vol. 34, Issue 8 https://doi.org/10.1016/j.biotechadv.2016.10.004	journal	December 2016
Molecular and carbon isotopic characterization of an anaerobic stable enrichment culture containing Dehalobacterium sp. during dichloromethane fermentation Trueba-Santiso, Alba; Parladé, Eloi; Rosell, Mònica Science of The Total Environment, Vol. 581-582 https://doi.org/10.1016/j.scitotenv.2016.12.174	journal	March 2017
‘ Candidatus Dichloromethanomonas elyunquensis’ gen. nov., sp. nov., a dichloromethane-degrading anaerobe of the Peptococcaceae family Kleindienst, Sara; Higgins, Steven A.; Tsementzi, Despina Systematic and Applied Microbiology, Vol. 40, Issue 3 https://doi.org/10.1016/j.syapm.2016.12.001	journal	April 2017
Dual Carbon–Chlorine Isotope Analysis Indicates Distinct Anaerobic Dichloromethane Degradation Pathways in Two Members of Peptococcaceae Chen, Gao; Shouakar-Stash, Orfan; Phillips, Elizabeth Environmental Science & Technology, Vol. 52, Issue 15 https://doi.org/10.1021/acs.est.8b01583	journal	June 2018
Growth Characteristics and Thermodynamics of Syntrophic Acetate Oxidizers Westerholm, Maria; Dolfing, Jan; Schnürer, Anna Environmental Science & Technology, Vol. 53, Issue 9 https://doi.org/10.1021/acs.est.9b00288	journal	April 2019
Hydrogenases Lubitz, Wolfgang; Ogata, Hideaki; Rüdiger, Olaf Chemical Reviews, Vol. 114, Issue 8 https://doi.org/10.1021/cr4005814	journal	March 2014
Reductive Dechlorination of cis -1,2-Dichloroethene and Vinyl Chloride by “ Dehalococcoides ethenogenes ” Maymó-Gatell, Xavier; Nijenhuis, Ivonne; Zinder, Stephen H. Environmental Science & Technology, Vol. 35, Issue 3 https://doi.org/10.1021/es001285i	journal	February 2001
Chlorinated Solvents in Groundwater of the United States Moran, Michael J.; Zogorski, John S.; Squillace, Paul J. Environmental Science & Technology, Vol. 41, Issue 1 https://doi.org/10.1021/es061553y	journal	January 2007
Bioaugmentation with Distinct Dehalobacter Strains Achieves Chloroform Detoxification in Microcosms Justicia-Leon, Shandra D.; Higgins, Steven; Mack, E. Erin Environmental Science & Technology, Vol. 48, Issue 3 https://doi.org/10.1021/es403582f	journal	January 2014
Relative Contributions of Dehalobacter and Zerovalent Iron in the Degradation of Chlorinated Methanes Lee, Matthew; Wells, Eliza; Wong, Yie Kuan Environmental Science & Technology, Vol. 49, Issue 7 https://doi.org/10.1021/es5052364	journal	March 2015
Composite global emissions of reactive chlorine from anthropogenic and natural sources: Reactive Chlorine Emissions Inventory Keene, William. C.; Khalil, M. Aslam K.; Erickson, David. J. Journal of Geophysical Research: Atmospheres, Vol. 104, Issue D7 https://doi.org/10.1029/1998JD100084	journal	April 1999
CO2 fixation by anaerobic non-photosynthetic mixotrophy for improved carbon conversion Jones, Shawn W.; Fast, Alan G.; Carlson, Ellinor D. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12800	journal	September 2016
The increasing threat to stratospheric ozone from dichloromethane Hossaini, Ryan; Chipperfield, Martyn P.; Montzka, Stephen A. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15962	journal	June 2017
CO2 conversion to methane and biomass in obligate methylotrophic methanogens in marine sediments Yin, Xiuran; Wu, Weichao; Maeke, Mara The ISME Journal, Vol. 13, Issue 8 https://doi.org/10.1038/s41396-019-0425-9	journal	April 2019
The mechanism of inhibition by H2 of H2-evolution by hydrogenases Fourmond, Vincent; Baffert, Carole; Sybirna, Kateryna Chemical Communications, Vol. 49, Issue 61 https://doi.org/10.1039/c3cc43297a	journal	January 2013
Control on rate and pathway of anaerobic organic carbon degradation in the seabed Beulig, F.; Røy, H.; Glombitza, C. Proceedings of the National Academy of Sciences, Vol. 115, Issue 2 https://doi.org/10.1073/pnas.1715789115	journal	December 2017
Life with Carbon Monoxide Ragsdale, Stephen W. Critical Reviews in Biochemistry and Molecular Biology, Vol. 39, Issue 3 https://doi.org/10.1080/10409230490496577	journal	January 2004
Methanogenesis and the Wood–Ljungdahl Pathway: An Ancient, Versatile, and Fragile Association Borrel, Guillaume; Adam, Panagiotis S.; Gribaldo, Simonetta Genome Biology and Evolution, Vol. 8, Issue 6 https://doi.org/10.1093/gbe/evw114	journal	May 2016
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 Müller, Jochen A.; Fullerton, Heather; Zinder, Stephen H. International Journal of Systematic and Evolutionary Microbiology, Vol. 65, Issue 6 https://doi.org/10.1099/ijs.0.000308	journal	June 2015
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 Loffler, F. E.; Yan, J.; Ritalahti, K. M. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 2 https://doi.org/10.1099/ijs.0.034926-0	journal	April 2012
Mutualistic interaction between dichloromethane- and chloromethane-degrading bacteria in an anaerobic mixed culture: Mutualistic degradation of chlorinated methanes Chen, Gao; Kleindienst, Sara; Griffiths, Daniel R. Environmental Microbiology, Vol. 19, Issue 11 https://doi.org/10.1111/1462-2920.13945	journal	October 2017
Methanol metabolism in the acetogenic bacterium Acetobacterium woodii Kremp, Florian; Poehlein, Anja; Daniel, Rolf Environmental Microbiology, Vol. 20, Issue 12 https://doi.org/10.1111/1462-2920.14356	journal	October 2018
Microbial syntrophy: interaction for the common good Morris, Brandon E. L.; Henneberger, Ruth; Huber, Harald FEMS Microbiology Reviews, Vol. 37, Issue 3 https://doi.org/10.1111/1574-6976.12019	journal	May 2013
Hydrogen or formate: Alternative key players in methanogenic degradation: Hydrogen/formate as interspecies electron carriers Schink, Bernhard; Montag, Dominik; Keller, Anja Environmental Microbiology Reports, Vol. 9, Issue 3 https://doi.org/10.1111/1758-2229.12524	journal	March 2017
Complete chloroform dechlorination by organochlorine respiration and fermentation: Microbial chloroform metabolism Lee, Matthew; Low, Adrian; Zemb, Olivier Environmental Microbiology, Vol. 14, Issue 4 https://doi.org/10.1111/j.1462-2920.2011.02656.x	journal	November 2011
Evidence for methanogenic Archaea and homoacetogenic Bacteria in deep granitic rock aquifers Kotelnikova, Svetlana; Pedersen, Karsten FEMS Microbiology Reviews, Vol. 20, Issue 3-4 https://doi.org/10.1111/j.1574-6976.1997.tb00319.x	journal	July 1997
Energetics of syntrophic cooperation in methanogenic degradation. Schink, B. Microbiology and molecular biology reviews : MMBR, Vol. 61, Issue 2 https://doi.org/10.1128/.61.2.262-280.1997	journal	January 1997
Energetics and Application of Heterotrophy in Acetogenic Bacteria Schuchmann, Kai; Müller, Volker Applied and Environmental Microbiology, Vol. 82, Issue 14 https://doi.org/10.1128/AEM.00882-16	journal	May 2016
Proteogenomics Reveals Novel Reductive Dehalogenases and Methyltransferases Expressed during Anaerobic Dichloromethane Metabolism Kleindienst, Sara; Chourey, Karuna; Chen, Gao Applied and Environmental Microbiology, Vol. 85, Issue 6 https://doi.org/10.1128/AEM.02768-18	journal	January 2019
Dichloromethane Fermentation by a Dehalobacter sp. in an Enrichment Culture Derived from Pristine River Sediment Justicia-Leon, Shandra D.; Ritalahti, Kirsti M.; Mack, E. Erin Applied and Environmental Microbiology, Vol. 78, Issue 4 https://doi.org/10.1128/AEM.07325-11	journal	December 2011
Biodegradation of dichloromethane and its utilization as a growth substrate under methanogenic conditions. Freedman, D. L.; Gossett, J. M. Applied and Environmental Microbiology, Vol. 57, Issue 10 https://doi.org/10.1128/AEM.57.10.2847-2857.1991	journal	January 1991
Acetogenesis from dichloromethane by a two-component mixed culture comprising a novel bacterium. Magli, A.; Rainey, F. A.; Leisinger, T. Applied and environmental microbiology, Vol. 61, Issue 8 https://doi.org/10.1128/AEM.61.8.2943-2949.1995	journal	January 1995
Metabolism of Dichloromethane by the Strict Anaerobe Dehalobacterium formicoaceticum Mägli, Andreas; Messmer, Michael; Leisinger, Thomas Applied and Environmental Microbiology, Vol. 64, Issue 2 https://doi.org/10.1128/AEM.64.2.646-650.1998	journal	January 1998
Fraction of Electrons Consumed in Electron Acceptor Reduction and Hydrogen Thresholds as Indicators of Halorespiratory Physiology Löffler, Frank E.; Tiedje, James M.; Sanford, Robert A. Applied and Environmental Microbiology, Vol. 65, Issue 9 https://doi.org/10.1128/AEM.65.9.4049-4056.1999	journal	January 1999
Quantitative PCR Targeting 16S rRNA and Reductive Dehalogenase Genes Simultaneously Monitors Multiple Dehalococcoides Strains Ritalahti, K. M.; Amos, B. K.; Sung, Y. Applied and Environmental Microbiology, Vol. 72, Issue 4 https://doi.org/10.1128/AEM.72.4.2765-2774.2006	journal	April 2006
Draft Genome Sequence of a Strictly Anaerobic Dichloromethane-Degrading Bacterium Kleindienst, Sara; Higgins, Steven A.; Tsementzi, Despina Genome Announcements, Vol. 4, Issue 2 https://doi.org/10.1128/genomeA.00037-16	journal	March 2016
Anaerobic Microbial Dehalogenation Smidt, Hauke; de Vos, Willem M. Annual Review of Microbiology, Vol. 58, Issue 1 https://doi.org/10.1146/annurev.micro.58.030603.123600	journal	October 2004
A targeted metabolomic protocol for short-chain fatty acids and branched-chain amino acids Yunping, Qiu,; Wei, Jia,; Qiong, Li, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/c4kt-fr56	text	January 2013
The increasing threat to stratospheric ozone from dichloromethane. Hossaini, Ryan; Chipperfield, Martyn P.; Montzka, Stephen A. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.21715	text	January 2017
Methanol conversion in high-rate anaerobic reactors Weijma, J.; Stams, A. J. M. Water Science and Technology, Vol. 44, Issue 8 https://doi.org/10.2166/wst.2001.0452	journal	October 2001
Acetogenesis in the Energy-Starved Deep Biosphere – A Paradox? Lever, Mark Alexander Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00284	journal	January 2012
Increasing concentrations of dichloromethane, CH ₂ Cl ₂ , inferred from CARIBIC air samples collected 1998–2012 Leedham Elvidge, E. C.; Oram, D. E.; Laube, J. C. Atmospheric Chemistry and Physics, Vol. 15, Issue 4 https://doi.org/10.5194/acp-15-1939-2015	journal	January 2015

Similar Records

Dual Carbon–Chlorine Isotope Analysis Indicates Distinct Anaerobic Dichloromethane Degradation Pathways in Two Members of Peptococcaceae

Journal Article · Wed Jul 04 20:00:00 EDT 2018 · Environmental Science and Technology · OSTI ID:1474553

Mutualistic interaction between dichloromethane- and chloromethane-degrading bacteria in an anaerobic mixed culture: Mutualistic degradation of chlorinated methanes

Journal Article · Sun Oct 01 20:00:00 EDT 2017 · Environmental Microbiology · OSTI ID:1474542

Anaerobic Microbial Metabolism of Dichloroacetate

Journal Article · Mon Apr 26 20:00:00 EDT 2021 · mBio (Online) · OSTI ID:1817372

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Mineralization versus fermentation: evidence for two distinct anaerobic bacterial degradation pathways for dichloromethane

Citation Formats

References (56)

Similar Records

Related Subjects