Mutualistic interaction between dichloromethane- and chloromethane-degrading bacteria in an anaerobic mixed culture: Mutualistic degradation of chlorinated methanes
Abstract
The microbial mixed culture RM grows with dichloromethane (DCM) as the sole energy source generating acetate, methane, chloride and biomass as products. Chloromethane (CM) was not an intermediate during DCM utilization consistent with the observation that CM could not replace DCM as a growth substrate. Interestingly, cultures that received DCM and CM together degraded both compounds concomitantly. Transient hydrogen (H2) formation reaching a maximum concentration of 205 ± 13 ppmv was observed in cultures growing with DCM, and the addition of exogenous H2 at concentrations exceeding 3000 ppmv impeded DCM degradation. In contrast, CM degradation in culture RM had a strict requirement for H2. Following five consecutive transfers on CM and H2, Acetobacterium 16S rRNA gene sequences dominated the culture and the DCM-degrader Candidatus Dichloromethanomonas elyunquensis was eliminated, consistent with the observation that the culture lost the ability to degrade DCM. These findings demonstrate that culture RM harbours different populations responsible for anaerobic DCM and CM metabolism, and further imply that the DCM and CM degradation pathways are mechanistically distinct. H2 generated during DCM degradation is consumed by the hydrogenotrophic CM degrader, or may fuel other hydrogenotrophic processes, including organohalide respiration, methanogenesis and H2/CO2 reductive acetogenesis.
- Authors:
-
- Univ. of Tennessee, Knoxville, TN (United States)
- Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Eberhard Karls Univ., Tubingen (Germany)
- Parsons, Denver, CO (United States)
- Corporate Remediation Group, E. I. DuPont de Nemours and Company, Wilmington, DE (United States)
- The Chemours Company, Wilmington, DE (United States)
- Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1474542
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Environmental Microbiology
- Additional Journal Information:
- Journal Volume: 19; Journal Issue: 11; Journal ID: ISSN 1462-2912
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Chen, Gao, Kleindienst, Sara, Griffiths, Daniel R., Mack, E. Erin, Seger, Edward S., and Löffler, Frank E.. Mutualistic interaction between dichloromethane- and chloromethane-degrading bacteria in an anaerobic mixed culture: Mutualistic degradation of chlorinated methanes. United States: N. p., 2017.
Web. doi:10.1111/1462-2920.13945.
Chen, Gao, Kleindienst, Sara, Griffiths, Daniel R., Mack, E. Erin, Seger, Edward S., & Löffler, Frank E.. Mutualistic interaction between dichloromethane- and chloromethane-degrading bacteria in an anaerobic mixed culture: Mutualistic degradation of chlorinated methanes. United States. https://doi.org/10.1111/1462-2920.13945
Chen, Gao, Kleindienst, Sara, Griffiths, Daniel R., Mack, E. Erin, Seger, Edward S., and Löffler, Frank E.. Mon .
"Mutualistic interaction between dichloromethane- and chloromethane-degrading bacteria in an anaerobic mixed culture: Mutualistic degradation of chlorinated methanes". United States. https://doi.org/10.1111/1462-2920.13945. https://www.osti.gov/servlets/purl/1474542.
@article{osti_1474542,
title = {Mutualistic interaction between dichloromethane- and chloromethane-degrading bacteria in an anaerobic mixed culture: Mutualistic degradation of chlorinated methanes},
author = {Chen, Gao and Kleindienst, Sara and Griffiths, Daniel R. and Mack, E. Erin and Seger, Edward S. and Löffler, Frank E.},
abstractNote = {The microbial mixed culture RM grows with dichloromethane (DCM) as the sole energy source generating acetate, methane, chloride and biomass as products. Chloromethane (CM) was not an intermediate during DCM utilization consistent with the observation that CM could not replace DCM as a growth substrate. Interestingly, cultures that received DCM and CM together degraded both compounds concomitantly. Transient hydrogen (H2) formation reaching a maximum concentration of 205 ± 13 ppmv was observed in cultures growing with DCM, and the addition of exogenous H2 at concentrations exceeding 3000 ppmv impeded DCM degradation. In contrast, CM degradation in culture RM had a strict requirement for H2. Following five consecutive transfers on CM and H2, Acetobacterium 16S rRNA gene sequences dominated the culture and the DCM-degrader Candidatus Dichloromethanomonas elyunquensis was eliminated, consistent with the observation that the culture lost the ability to degrade DCM. These findings demonstrate that culture RM harbours different populations responsible for anaerobic DCM and CM metabolism, and further imply that the DCM and CM degradation pathways are mechanistically distinct. H2 generated during DCM degradation is consumed by the hydrogenotrophic CM degrader, or may fuel other hydrogenotrophic processes, including organohalide respiration, methanogenesis and H2/CO2 reductive acetogenesis.},
doi = {10.1111/1462-2920.13945},
journal = {Environmental Microbiology},
number = 11,
volume = 19,
place = {United States},
year = {2017},
month = {10}
}
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Works referenced in this record:
Hydrogen concentrations as an indicator of the predominant terminal electron-accepting reactions in aquatic sediments
journal, December 1988
- Lovley, Derek R.; Goodwin, Steve
- Geochimica et Cosmochimica Acta, Vol. 52, Issue 12
A review of bacterial methyl halide degradation: biochemistry, genetics and molecular ecology
journal, April 2002
- McDonald, I. R.; Warner, K. L.; McAnulla, C.
- Environmental Microbiology, Vol. 4, Issue 4
Anaerobic Microbial Dehalogenation
journal, October 2004
- Smidt, Hauke; de Vos, Willem M.
- Annual Review of Microbiology, Vol. 58, Issue 1
A corrinoid-dependent catabolic pathway for growth of a Methylobacterium strain with chloromethane
journal, April 1999
- Vannelli, T.; Messmer, M.; Studer, A.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 8
Natural Attenuation in Streambed Sediment Receiving Chlorinated Solvents from Underlying Fracture Networks
journal, April 2017
- Şimşir, Burcu; Yan, Jun; Im, Jeongdae
- Environmental Science & Technology, Vol. 51, Issue 9
Studies on methyl chloride dehalogenase and O -demethylase in cell extracts of the homoacetogen strain MC based on a newly developed coupled enzyme assay
journal, January 1996
- Meßmer, Michael; Reinhardt, Simone; Wohlfarth, Gert
- Archives of Microbiology, Vol. 165, Issue 1
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
Bacterial growth with chlorinated methanes.
journal, June 1995
- Leisinger, T.; Braus-Stromeyer, S. A.
- Environmental Health Perspectives, Vol. 103, Issue suppl 5
Hydrogen Concentrations in Sulfate-Reducing Estuarine Sediments during PCE Dehalogenation
journal, December 2001
- Mazur, Christopher S.; Jones, W. Jack
- Environmental Science & Technology, Vol. 35, Issue 24
The global chloromethane cycle: biosynthesis, biodegradation and metabolic role (1982 to January 2000)
journal, January 2000
- Harper, David B.
- Natural Product Reports, Vol. 17, Issue 4
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB
journal, July 2006
- DeSantis, T. Z.; Hugenholtz, P.; Larsen, N.
- Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072
O-Demethylase from Acetobacterium dehalogenans . Substrate specificity and function of the participating proteins
journal, May 1998
- Kaufmann, Franz; Wohlfarth, Gert; Diekert, Gabriele
- European Journal of Biochemistry, Vol. 253, Issue 3
Natural methyl bromide and methyl chloride emissions from coastal salt marshes
journal, January 2000
- Rhew, Robert C.; Miller, Benjamin R.; Weiss, Ray F.
- Nature, Vol. 403, Issue 6767
Novel insights into the bioenergetics of mixed-acid fermentation: Can hydrogen and proton cycles combine to help maintain a proton motive force?: BIOENERGETICS OF MIXED-ACID FERMENTATION
journal, December 2013
- Trchounian, Armen; Gary Sawers, R.
- IUBMB Life, Vol. 66, Issue 1
Draft Genome Sequence of a Strictly Anaerobic Dichloromethane-Degrading Bacterium
journal, March 2016
- Kleindienst, Sara; Higgins, Steven A.; Tsementzi, Despina
- Genome Announcements, Vol. 4, Issue 2
Bacterial formate hydrogenlyase complex
journal, August 2014
- McDowall, J. S.; Murphy, B. J.; Haumann, M.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 38
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
Isolation and characterization of Dehalobacter sp. strain UNSWDHB capable of chloroform and chlorinated ethane respiration : Isolation and characterization of
journal, April 2016
- Wong, Yie K.; Holland, Sophie I.; Ertan, Haluk
- Environmental Microbiology, Vol. 18, Issue 9
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
QIIME allows analysis of high-throughput community sequencing data
journal, April 2010
- Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
- Nature Methods, Vol. 7, Issue 5
Dichloromethane Fermentation by a Dehalobacter sp. in an Enrichment Culture Derived from Pristine River Sediment
journal, December 2011
- Justicia-Leon, Shandra D.; Ritalahti, Kirsti M.; Mack, E. Erin
- Applied and Environmental Microbiology, Vol. 78, Issue 4
Experimental Evaluation and Mathematical Modeling of Microbially Enhanced Tetrachloroethene (PCE) Dissolution
journal, February 2007
- Amos, Benjamin K.; Christ, John A.; Abriola, Linda M.
- Environmental Science & Technology, Vol. 41, Issue 3
Diversity of corrinoids in acetogenic bacteria. P-Cresolylcobamide from Sporomusa ovata, 5-methoxy-6-methylbenzimidazolylcobamide from Clostridium formicoaceticum and vitamin B12 from Acetobacterium woodii
journal, March 1988
- Stupperich, Erhard; Eisinger, Hans Jurgen; Krautler, Bernhard
- European Journal of Biochemistry, Vol. 172, Issue 2
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample
journal, June 2010
- Caporaso, J. G.; Lauber, C. L.; Walters, W. A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
The capacity of hydrogenotrophic anaerobic bacteria to compete for traces of hydrogen depends on the redox potential of the terminal electron acceptor
journal, February 1988
- Cord-Ruwisch, Ralf; Seitz, Hans-J�rgen; Conrad, Ralf
- Archives of Microbiology, Vol. 149, Issue 4
Isolation and characterization of a methyl chloride utilizing, strictly anaerobic bacterium
journal, October 1991
- Traunecker, J�rgen; Preu�, Andrea; Diekert, Gabriele
- Archives of Microbiology, Vol. 156, Issue 5
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
Quantitative PCR Targeting 16S rRNA and Reductive Dehalogenase Genes Simultaneously Monitors Multiple Dehalococcoides Strains
journal, April 2006
- Ritalahti, K. M.; Amos, B. K.; Sung, Y.
- Applied and Environmental Microbiology, Vol. 72, Issue 4
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
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
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012
- Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
- The ISME Journal, Vol. 6, Issue 8
Better budgets for methyl halides?
journal, January 2000
- Butler, James H.
- Nature, Vol. 403, Issue 6767
Reductive dehalogenation of chlorinated C1-hydrocarbons mediated by corrinoids
journal, May 1989
- Krone, Ute E.; Thauer, Rudolf K.; Hogenkamp, Harry P. C.
- Biochemistry, Vol. 28, Issue 11
‘ 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
Search and clustering orders of magnitude faster than BLAST
journal, August 2010
- Edgar, Robert C.
- Bioinformatics, Vol. 26, Issue 19, p. 2460-2461
Hydrogen threshold concentrations in pure cultures of halorespiring bacteria and at a site polluted with chlorinated ethenes
journal, June 2004
- Luijten, Maurice L. G. C.; Roelofsen, Wim; Langenhoff, Alette A. M.
- Environmental Microbiology, Vol. 6, Issue 6
Stable carbon isotope fractionation during degradation of dichloromethane by methylotrophic bacteria
journal, January 2006
- Nikolausz, Marcell; Nijenhuis, Ivonne; Ziller, Katja
- Environmental Microbiology, Vol. 8, Issue 1
Biodegradation of dichloromethane and its utilization as a growth substrate under methanogenic conditions.
journal, January 1991
- Freedman, D. L.; Gossett, J. M.
- Applied and Environmental Microbiology, Vol. 57, Issue 10
Dichloromethane dehalogenase of Hyphomicrobium sp. strain DM2.
journal, January 1985
- Kohler-Staub, D.; Leisinger, T.
- Journal of Bacteriology, Vol. 162, Issue 2
Initial Characterization of a Reductive Dehalogenase from Desulfitobacterium chlororespirans Co23.
journal, January 1996
- Loffler, F. E.; Sanford, R. A.; Tiedje, J. M.
- Applied and environmental microbiology, Vol. 62, Issue 10
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
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
Energy conservation in chemotrophic anaerobic bacteria.
journal, January 1977
- Thauer, R. K.; Jungermann, K.; Decker, K.
- Bacteriological Reviews, Vol. 41, Issue 1
Works referencing / citing this record:
Mineralization versus fermentation: evidence for two distinct anaerobic bacterial degradation pathways for dichloromethane
journal, January 2020
- Chen, Gao; Fisch, Alexander R.; Gibson, Caleb M.
- The ISME Journal, Vol. 14, Issue 4