The corrinoid cofactor of reductive dehalogenases affects dechlorination rates and extents in organohalide-respiring Dehalococcoides mccartyi
Abstract
Corrinoid auxotrophic organohalide-respiring Dehalococcoides mccartyi (Dhc) strains are keystone bacteria for reductive dechlorination of toxic and carcinogenic chloroorganic contaminants. We demonstrate that the lower base attached to the essential corrinoid cofactor of reductive dehalogenase (RDase) enzyme systems modulates dechlorination activity and affects the vinyl chloride (VC) RDases BvcA and VcrA differently. Amendment of 5,6-dimethylbenzimidazolyl-cobamide (DMB-Cba) to Dhc strain BAV1 and strain GT cultures supported cis-1,2-dichloroethene-to-ethene reductive dechlorination at rates of 107.0 (±12.0) μM and 67.4 (±1.4) μM Cl- released per day, respectively. Strain BAV1, expressing the BvcA RDase, reductively dechlorinated VC to ethene, although at up to fivefold lower rates in cultures amended with cobamides carrying 5-methylbenzimidazole (5-MeBza), 5-methoxybenzimidazole (5-OMeBza) or benzimidazole (Bza) as the lower base. In contrast, strain GT harboring the VcrA RDase failed to grow and dechlorinate VC to ethene in medium amended with 5-OMeBza-Cba or Bza-Cba. The amendment with DMB to inactive strain GT cultures restored the VC-to-ethene-dechlorinating phenotype and intracellular DMB-Cba was produced, demonstrating cobamide uptake and remodeling. The distinct responses of Dhc strains with BvcA versus VcrA RDases to different cobamides implicate that the lower base exerts control over Dhc reductive dechlorination rates and extents (that is, detoxification), and therefore the dynamics of Dhcmore »
- Authors:
-
- Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Univ. of Tennessee, Knoxville, TN (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1468287
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The ISME Journal
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 5; Journal ID: ISSN 1751-7362
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Yan, Jun, Şimşir, Burcu, Farmer, Abigail T., Bi, Meng, Yang, Yi, Campagna, Shawn R., and Löffler, Frank E. The corrinoid cofactor of reductive dehalogenases affects dechlorination rates and extents in organohalide-respiring Dehalococcoides mccartyi. United States: N. p., 2015.
Web. doi:10.1038/ismej.2015.197.
Yan, Jun, Şimşir, Burcu, Farmer, Abigail T., Bi, Meng, Yang, Yi, Campagna, Shawn R., & Löffler, Frank E. The corrinoid cofactor of reductive dehalogenases affects dechlorination rates and extents in organohalide-respiring Dehalococcoides mccartyi. United States. https://doi.org/10.1038/ismej.2015.197
Yan, Jun, Şimşir, Burcu, Farmer, Abigail T., Bi, Meng, Yang, Yi, Campagna, Shawn R., and Löffler, Frank E. Tue .
"The corrinoid cofactor of reductive dehalogenases affects dechlorination rates and extents in organohalide-respiring Dehalococcoides mccartyi". United States. https://doi.org/10.1038/ismej.2015.197. https://www.osti.gov/servlets/purl/1468287.
@article{osti_1468287,
title = {The corrinoid cofactor of reductive dehalogenases affects dechlorination rates and extents in organohalide-respiring Dehalococcoides mccartyi},
author = {Yan, Jun and Şimşir, Burcu and Farmer, Abigail T. and Bi, Meng and Yang, Yi and Campagna, Shawn R. and Löffler, Frank E.},
abstractNote = {Corrinoid auxotrophic organohalide-respiring Dehalococcoides mccartyi (Dhc) strains are keystone bacteria for reductive dechlorination of toxic and carcinogenic chloroorganic contaminants. We demonstrate that the lower base attached to the essential corrinoid cofactor of reductive dehalogenase (RDase) enzyme systems modulates dechlorination activity and affects the vinyl chloride (VC) RDases BvcA and VcrA differently. Amendment of 5,6-dimethylbenzimidazolyl-cobamide (DMB-Cba) to Dhc strain BAV1 and strain GT cultures supported cis-1,2-dichloroethene-to-ethene reductive dechlorination at rates of 107.0 (±12.0) μM and 67.4 (±1.4) μM Cl- released per day, respectively. Strain BAV1, expressing the BvcA RDase, reductively dechlorinated VC to ethene, although at up to fivefold lower rates in cultures amended with cobamides carrying 5-methylbenzimidazole (5-MeBza), 5-methoxybenzimidazole (5-OMeBza) or benzimidazole (Bza) as the lower base. In contrast, strain GT harboring the VcrA RDase failed to grow and dechlorinate VC to ethene in medium amended with 5-OMeBza-Cba or Bza-Cba. The amendment with DMB to inactive strain GT cultures restored the VC-to-ethene-dechlorinating phenotype and intracellular DMB-Cba was produced, demonstrating cobamide uptake and remodeling. The distinct responses of Dhc strains with BvcA versus VcrA RDases to different cobamides implicate that the lower base exerts control over Dhc reductive dechlorination rates and extents (that is, detoxification), and therefore the dynamics of Dhc strains with discrete reductive dechlorination capabilities. Furthermore, these findings emphasize that the role of the corrinoid/lower base synthesizing community must be understood to predict strain-specific Dhc activity and achieve efficacious contaminated site cleanup.},
doi = {10.1038/ismej.2015.197},
journal = {The ISME Journal},
number = 5,
volume = 10,
place = {United States},
year = {Tue Nov 10 00:00:00 EST 2015},
month = {Tue Nov 10 00:00:00 EST 2015}
}
Web of Science
Works referenced in this record:
Overview of organohalide-respiring bacteria and a proposal for a classification system for reductive dehalogenases
journal, April 2013
- Hug, Laura A.; Maphosa, Farai; Leys, David
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1616
Biochemical and EPR-Spectroscopic Investigation into Heterologously Expressed Vinyl Chloride Reductive Dehalogenase (VcrA) from Dehalococcoides mccartyi Strain VS
journal, March 2015
- Parthasarathy, Anutthaman; Stich, Troy A.; Lohner, Svenja T.
- Journal of the American Chemical Society, Vol. 137, Issue 10
Harnessing microbial activities for environmental cleanup
journal, June 2006
- Löffler, Frank E.; Edwards, Elizabeth A.
- Current Opinion in Biotechnology, Vol. 17, Issue 3
A Different Mechanism for the Reductive Dechlorination of Chlorinated Ethenes: Kinetic and Spectroscopic Evidence
journal, August 1998
- Lesage, Suzanne; Brown, Susan; Millar, Kelly
- Environmental Science & Technology, Vol. 32, Issue 15
Molecular Identification of the Catabolic Vinyl Chloride Reductase from Dehalococcoides sp. Strain VS and Its Environmental Distribution
journal, August 2004
- Muller, J. A.; Rosner, B. M.; von Abendroth, G.
- Applied and Environmental Microbiology, Vol. 70, Issue 8
Microbial production of vitamin B 12
journal, March 2002
- Martens, H. Barg, M. Warren, D. Jah, J. -H.
- Applied Microbiology and Biotechnology, Vol. 58, Issue 3
Genetic Identification of a Putative Vinyl Chloride Reductase in Dehalococcoides sp. Strain BAV1
journal, October 2004
- Krajmalnik-Brown, R.; Holscher, T.; Thomson, I. N.
- Applied and Environmental Microbiology, Vol. 70, Issue 10
Guided cobalamin biosynthesis supports Dehalococcoides mccartyi reductive dechlorination activity
journal, April 2013
- Yan, Jun; Im, Jeongdae; Yang, Yi
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1616
Solvent exposures and parkinson disease risk in twins
journal, November 2011
- Goldman, Samuel M.; Quinlan, Patricia J.; Ross, G. Webster
- Annals of Neurology, Vol. 71, Issue 6
Methyladeninylcobamide functions as the cofactor of methionine synthase in a Cyanobacterium, Spirulina platensis NIES-39
journal, June 2010
- Tanioka, Yuri; Miyamoto, Emi; Yabuta, Yukinori
- FEBS Letters, Vol. 584, Issue 14
Comparison of Butyric Acid, Ethanol, Lactic Acid, and Propionic Acid as Hydrogen Donors for the Reductive Dechlorination of Tetrachloroethene
journal, March 1997
- Fennell, Donna E.; Gossett, James M.; Zinder, Stephen H.
- Environmental Science & Technology, Vol. 31, Issue 3
Organohalide respiration: microbes breathing chlorinated molecules
journal, April 2013
- Leys, David; Adrian, Lorenz; Smidt, Hauke
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1616
Unexpected Specificity of Interspecies Cobamide Transfer from Geobacter spp. to Organohalide-Respiring Dehalococcoides mccartyi Strains
journal, July 2012
- Yan, Jun; Ritalahti, Kirsti M.; Wagner, Darlene D.
- Applied and Environmental Microbiology, Vol. 78, Issue 18
Vinyl chloride: still a cause for concern.
journal, July 2000
- Kielhorn, J.; Melber, C.; Wahnschaffe, U.
- Environmental Health Perspectives, Vol. 108, Issue 7
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
Vitamin B12-derivatives—enzyme cofactors and ligands of proteins and nucleic acids
journal, January 2011
- Gruber, Karl; Puffer, Barbara; Kräutler, Bernhard
- Chemical Society Reviews, Vol. 40, Issue 8
The Genetic Basis for Bacterial Mercury Methylation
journal, February 2013
- Parks, J. M.; Johs, A.; Podar, M.
- Science, Vol. 339, Issue 6125, p. 1332-1335
Discovery of epoxyqueuosine (oQ) reductase reveals parallels between halorespiration and tRNA modification
journal, April 2011
- Miles, Z. D.; McCarty, R. M.; Molnar, G.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 18
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
Determination of Vitamin B12 with a Mutant Strain of Escherichia coli
journal, November 1951
- Burkholder, P. R.
- Science, Vol. 114, Issue 2966
Mammalian Methylmalonyl Isomerase and Vitamin b12 Coenzymes
journal, October 1960
- Lengyel, P.; Mazumder, R.; Ochoa, S.
- Proceedings of the National Academy of Sciences, Vol. 46, Issue 10
Sustainable Growth of Dehalococcoides mccartyi 195 by Corrinoid Salvaging and Remodeling in Defined Lactate-Fermenting Consortia
journal, January 2014
- Men, Yujie; Seth, Erica C.; Yi, Shan
- Applied and Environmental Microbiology, Vol. 80, Issue 7
Isolation of a Bacterium That Reductively Dechlorinates Tetrachloroethene to Ethene
journal, June 1997
- Maymo-Gatell, X.
- Science, Vol. 276, Issue 5318
Reductive dehalogenase structure suggests a mechanism for B12-dependent dehalogenation
journal, October 2014
- Payne, Karl A. P.; Quezada, Carolina P.; Fisher, Karl
- Nature, Vol. 517, Issue 7535
Quantitative PCR Confirms Purity of Strain GT, a Novel Trichloroethene-to-Ethene-Respiring Dehalococcoides Isolate
journal, March 2006
- Sung, Y.; Ritalahti, K. M.; Apkarian, R. P.
- Applied and Environmental Microbiology, Vol. 72, Issue 3
Reduction dechlorination of carbon tetrachloride by cobalamin(II) in the presence of dithiothreitol: mechanistic study, effect of redox potential and pH
journal, February 1994
- Assaf-Anid, Nada.; Hayes, Kim F.; Vogel, Timothy M.
- Environmental Science & Technology, Vol. 28, Issue 2
Detoxification of vinyl chloride to ethene coupled to growth of an anaerobic bacterium
journal, July 2003
- He, Jianzhong; Ritalahti, Kirsti M.; Yang, Kun-Lin
- Nature, Vol. 424, Issue 6944
Substrate-induced transmembrane signaling in the cobalamin transporter BtuB
journal, March 2003
- Chimento, David P.; Mohanty, Arun K.; Kadner, Robert J.
- Nature Structural & Molecular Biology, Vol. 10, Issue 5
Functional Characterization of Reductive Dehalogenases by Using Blue Native Polyacrylamide Gel Electrophoresis
journal, November 2012
- Tang, Shuiquan; Chan, Winnie W. M.; Fletcher, Kelly E.
- Applied and Environmental Microbiology, Vol. 79, Issue 3
Inefficient remediation of ground-water pollution
journal, November 1990
- Abelson, P.
- Science, Vol. 250, Issue 4982
Human Gut Microbes Use Multiple Transporters to Distinguish Vitamin B12 Analogs and Compete in the Gut
journal, January 2014
- Degnan, Patrick H.; Barry, Natasha A.; Mok, Kenny C.
- Cell Host & Microbe, Vol. 15, Issue 1
Transformation of Carbon Tetrachloride by Reduced Vitamin B 12 in Aqueous Cysteine Solution
journal, January 1996
- Chiu, Pei-Chun; Reinhard, Martin
- Environmental Science & Technology, Vol. 30, Issue 6
Structural basis for organohalide respiration
journal, October 2014
- Bommer, Martin; Kunze, Cindy; Fesseler, Jochen
- Science, Vol. 346, Issue 6208
Identification and quantitation of cobalamin and cobalamin analogues in human feces
journal, May 2008
- Allen, Robert H.; Stabler, Sally P.
- The American Journal of Clinical Nutrition, Vol. 87, Issue 5
Localized Plasticity in the Streamlined Genomes of Vinyl Chloride Respiring Dehalococcoides
journal, November 2009
- McMurdie, Paul J.; Behrens, Sebastian F.; Müller, Jochen A.
- PLoS Genetics, Vol. 5, Issue 11
Exogenous 5,6-dimethylbenzimidazole caused production of a non-functional tetrachloroethene reductive dehalogenase in Sulfurospirillum multivorans : DMB affects PCE dechlorination in
journal, October 2013
- Keller, Sebastian; Ruetz, Markus; Kunze, Cindy
- Environmental Microbiology, Vol. 16, Issue 11
Identification of specific corrinoids reveals corrinoid modification in dechlorinating microbial communities: Corrinoids in dechlorinating communities
journal, June 2014
- Men, Yujie; Seth, Erica C.; Yi, Shan
- Environmental Microbiology, Vol. 17, Issue 12
Corrinoids in anaerobic bacteria
journal, December 1990
- Stupperich, Erhard; Eisinger, Hans-Jürgen; Schurr, Sabine
- FEMS Microbiology Letters, Vol. 87, Issue 3-4
Isolation and Properties of Crystalline Cobamide Coenzymes Containing Benzimidazole or 5,6-Dimethylbenzimidazole
journal, February 1960
- Barker, H. A.; Smyth, R. D.; Weissbach, H.
- Journal of Biological Chemistry, Vol. 235, Issue 2
The use of Lactobacillus Leichmannii in the Estimation of Vitamin b12 Activity
journal, May 1950
- Thompson, H. T.; Dietrich, L. S.; Elvehjem, C. A.
- Journal of Biological Chemistry, Vol. 184, Issue 1
Works referencing / citing this record:
Transient O2 pulses direct Fe crystallinity and Fe(III)-reducer gene expression within a soil microbiome
journal, October 2018
- Wilmoth, Jared Lee; Moran, Mary Ann; Thompson, Aaron
- Microbiome, Vol. 6, Issue 1
Targeted detection of Dehalococcoides mccartyi microbial protein biomarkers as indicators of reductive dechlorination activity in contaminated groundwater
journal, July 2019
- Solis, Manuel I. Villalobos; Abraham, Paul E.; Chourey, Karuna
- Scientific Reports, Vol. 9, Issue 1
An integrative overview of genomic, transcriptomic and proteomic analyses in organohalide respiration research
journal, January 2018
- Türkowsky, Dominique; Jehmlich, Nico; Diekert, Gabriele
- FEMS Microbiology Ecology, Vol. 94, Issue 3
Selective Utilization of Benzimidazolyl-Norcobamides as Cofactors by the Tetrachloroethene Reductive Dehalogenase of Sulfurospirillum multivorans
journal, January 2018
- Keller, Sebastian; Kunze, Cindy; Bommer, Martin
- Journal of Bacteriology, Vol. 200, Issue 8
Identification and characterization of a bacterial core methionine synthase
journal, February 2020
- Deobald, Darja; Hanna, Rafael; Shahryari, Shahab
- Scientific Reports, Vol. 10, Issue 1
Cobalamin Protection against Oxidative Stress in the Acidophilic Iron-oxidizing Bacterium Leptospirillum Group II CF-1
journal, May 2016
- Ferrer, Alonso; Rivera, Javier; Zapata, Claudia
- Frontiers in Microbiology, Vol. 7
Refined experimental annotation reveals conserved corrinoid autotrophy in chloroform-respiring Dehalobacter isolates
journal, November 2016
- Wang, Po-Hsiang; Tang, Shuiquan; Nemr, Kayla
- The ISME Journal, Vol. 11, Issue 3
Identification and characterization of a bacterial core methionine synthase
journal, February 2020
- Deobald, Darja; Hanna, Rafael; Shahryari, Shahab
- Scientific Reports, Vol. 10, Issue 1
Impact of iron- and/or sulfate-reduction on a cis -1,2-dichloroethene and vinyl chloride respiring bacterial consortium: experiments and model-based interpretation
journal, January 2020
- Murray, Alexandra; Maillard, Julien; Rolle, Massimo
- Environmental Science: Processes & Impacts, Vol. 22, Issue 3
Organohalide respiratory chains: composition, topology and key enzymes
journal, March 2018
- Schubert, Torsten; Adrian, Lorenz; Sawers, R. Gary
- FEMS Microbiology Ecology, Vol. 94, Issue 4
Uneven distribution of cobamide biosynthesis and dependence in bacteria predicted by comparative genomics
journal, November 2018
- Shelton, Amanda N.; Seth, Erica C.; Mok, Kenny C.
- The ISME Journal, Vol. 13, Issue 3
Grape pomace compost harbors organohalide-respiring Dehalogenimonas species with novel reductive dehalogenase genes
journal, August 2017
- Yang, Yi; Higgins, Steven A.; Yan, Jun
- The ISME Journal, Vol. 11, Issue 12
Sustained Dechlorination of Vinyl Chloride to Ethene in Dehalococcoides -Enriched Cultures Grown without Addition of Exogenous Vitamins and at Low pH
journal, August 2019
- Puentes Jácome, Luz A.; Wang, Po-Hsiang; Molenda, Olivia
- Environmental Science & Technology, Vol. 53, Issue 19
Guided cobamide biosynthesis for heterologous production of reductive dehalogenases
journal, December 2018
- Schubert, Torsten; Reuß, Stephan H.; Kunze, Cindy
- Microbial Biotechnology, Vol. 12, Issue 2
Purinyl-cobamide is a native prosthetic group of reductive dehalogenases
journal, November 2017
- Yan, Jun; Bi, Meng; Bourdon, Allen K.
- Nature Chemical Biology, Vol. 14, Issue 1