DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: 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 » 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.« less

Authors:
 [1];  [2];  [2];  [2];  [2];  [2]; ORCiD logo [1]
  1. Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  2. 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}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 44 works
Citation information provided by
Web of Science

Save / Share:

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
  • DOI: 10.1098/rstb.2012.0322

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
  • DOI: 10.1021/ja511653d

Harnessing microbial activities for environmental cleanup
journal, June 2006


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
  • DOI: 10.1021/es970959v

Molecular Identification of the Catabolic Vinyl Chloride Reductase from Dehalococcoides sp. Strain VS and Its Environmental Distribution
journal, August 2004


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
  • DOI: 10.1007/s00253-001-0902-7

Genetic Identification of a Putative Vinyl Chloride Reductase in Dehalococcoides sp. Strain BAV1
journal, October 2004


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
  • DOI: 10.1098/rstb.2012.0320

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
  • DOI: 10.1002/ana.22629

Methyladeninylcobamide functions as the cofactor of methionine synthase in a Cyanobacterium, Spirulina platensis NIES-39
journal, June 2010


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
  • DOI: 10.1021/es960756r

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
  • DOI: 10.1098/rstb.2012.0316

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
  • DOI: 10.1128/AEM.01535-12

Vinyl chloride: still a cause for concern.
journal, July 2000

  • Kielhorn, J.; Melber, C.; Wahnschaffe, U.
  • Environmental Health Perspectives, Vol. 108, Issue 7
  • DOI: 10.1289/ehp.00108579

Quantitative PCR Targeting 16S rRNA and Reductive Dehalogenase Genes Simultaneously Monitors Multiple Dehalococcoides Strains
journal, April 2006


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
  • DOI: 10.1039/c1cs15118e

The Genetic Basis for Bacterial Mercury Methylation
journal, February 2013


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
  • DOI: 10.1073/pnas.1018636108

Determination of Vitamin B12 with a Mutant Strain of Escherichia coli
journal, November 1951


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
  • DOI: 10.1073/pnas.46.10.1312

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
  • DOI: 10.1128/AEM.03477-13

Isolation of a Bacterium That Reductively Dechlorinates Tetrachloroethene to Ethene
journal, June 1997


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
  • DOI: 10.1038/nature13901

Quantitative PCR Confirms Purity of Strain GT, a Novel Trichloroethene-to-Ethene-Respiring Dehalococcoides Isolate
journal, March 2006


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
  • DOI: 10.1021/es00051a010

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
  • DOI: 10.1038/nature01717

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
  • DOI: 10.1038/nsb914

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
  • DOI: 10.1128/AEM.01873-12

Inefficient remediation of ground-water pollution
journal, November 1990


Human Gut Microbes Use Multiple Transporters to Distinguish Vitamin B12 Analogs and Compete in the Gut
journal, January 2014


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
  • DOI: 10.1021/es950477o

Structural basis for organohalide respiration
journal, October 2014


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
  • DOI: 10.1093/ajcn/87.5.1324

Localized Plasticity in the Streamlined Genomes of Vinyl Chloride Respiring Dehalococcoides
journal, November 2009


Corrinoids in anaerobic bacteria
journal, December 1990


Isolation and Properties of Crystalline Cobamide Coenzymes Containing Benzimidazole or 5,6-Dimethylbenzimidazole
journal, February 1960


The use of Lactobacillus Leichmannii in the Estimation of Vitamin b12 Activity
journal, May 1950


Works referencing / citing this record:

Transient O2 pulses direct Fe crystallinity and Fe(III)-reducer gene expression within a soil microbiome
journal, October 2018


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
  • DOI: 10.1038/s41598-019-46901-6

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
  • DOI: 10.1093/femsec/fiy013

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
  • DOI: 10.1128/jb.00584-17

Identification and characterization of a bacterial core methionine synthase
journal, February 2020


Cobalamin Protection against Oxidative Stress in the Acidophilic Iron-oxidizing Bacterium Leptospirillum Group II CF-1
journal, May 2016


Refined experimental annotation reveals conserved corrinoid autotrophy in chloroform-respiring Dehalobacter isolates
journal, November 2016


Identification and characterization of a bacterial core methionine synthase
journal, February 2020


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
  • DOI: 10.1039/c9em00544g

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
  • DOI: 10.1093/femsec/fiy035

Uneven distribution of cobamide biosynthesis and dependence in bacteria predicted by comparative genomics
journal, November 2018


Grape pomace compost harbors organohalide-respiring Dehalogenimonas species with novel reductive dehalogenase genes
journal, August 2017


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
  • DOI: 10.1021/acs.est.9b02339

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
  • DOI: 10.1111/1751-7915.13339

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
  • DOI: 10.1038/nchembio.2512