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Title: 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 » is introduced through natural production processes or anthropogenic activities.« less

Authors:
 [1];  [2];  [2];  [3];  [4];  [2]; ORCiD logo [5]
  1. Univ. of Tennessee, Knoxville, TN (United States). Center for Environmental Biotechnology and Dept. of Civil and Environmental Engineering
  2. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Chemistry
  3. Corteva Agriscience, Wilmington, DE (United States)
  4. The Chemours Company, Wilmington, DE (United States). Chemours Corporate Remediation Group
  5. 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}
}

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