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Title: Quantitative Proteomic Analysis of Biological Processes and Responses of the Bacterium Desulfovibrio desulfuricans ND132 upon Deletion of Its Mercury Methylation Genes

Abstract

Recent studies of microbial mercury (Hg) methylation revealed a key gene pair, hgcAB, which is essential for methylmercury (MeHg) production in the environment. However, many aspects of the mechanism and biological processes underlying Hg methylation, as well as any additional physiological functions of the hgcAB genes, remain unknown. Here, quantitative proteomics are used to identify changes in potential functional processes related to hgcAB gene deletion in the Hg-methylating bacterium Desulfovibrio desulfuricans ND132. Global proteomics analyses indicate that the wild type and ΔhgcAB strains are similar with respect to the whole proteome and the identified number of proteins, but differ significantly in the abundance of specific proteins. The authors observe changes in the abundance of proteins related to the glycolysis pathway and one-carbon metabolism, suggesting that the hgcAB gene pair is linked to carbon metabolism. Unexpectedly, the authors find that the deletion of hgcAB significantly impacts a range of metal transport proteins, specifically membrane efflux pumps such as those associated with heavy metal copper (Cu) export, leading to decreased Cu uptake in the ΔhgcAB mutant. This observation indicates possible linkages between this set of proteins and metal homeostasis in the cell. However, hgcAB gene expression is not induced by Hg, asmore » evidenced by similarly low abundance of HgcA and HgcB proteins in the absence or presence of Hg (500 nm). Altogether, these results suggest an apparent link between HgcAB, one-carbon metabolism, and metal homeostasis, thereby providing insights for further exploration of biochemical mechanisms and biological functions of microbial Hg methylation.« less

Authors:
 [1]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2];  [2]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [2]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
  2. 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 Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1468234
Alternate Identifier(s):
OSTI ID: 1464844
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Proteomics
Additional Journal Information:
Journal Volume: 18; Journal Issue: 17; Journal ID: ISSN 1615-9853
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; hgcAB genes; metabolic pathways; metal transporters; methylmercury; sulfate-reducing bacteria

Citation Formats

Qian, Chen, Chen, Hongmei, Johs, Alexander, Lu, Xia, An, Jing, Pierce, Eric M., Parks, Jerry M., Elias, Dwayne A., Hettich, Robert L., and Gu, Baohua. Quantitative Proteomic Analysis of Biological Processes and Responses of the Bacterium Desulfovibrio desulfuricans ND132 upon Deletion of Its Mercury Methylation Genes. United States: N. p., 2018. Web. doi:10.1002/pmic.201700479.
Qian, Chen, Chen, Hongmei, Johs, Alexander, Lu, Xia, An, Jing, Pierce, Eric M., Parks, Jerry M., Elias, Dwayne A., Hettich, Robert L., & Gu, Baohua. Quantitative Proteomic Analysis of Biological Processes and Responses of the Bacterium Desulfovibrio desulfuricans ND132 upon Deletion of Its Mercury Methylation Genes. United States. doi:10.1002/pmic.201700479.
Qian, Chen, Chen, Hongmei, Johs, Alexander, Lu, Xia, An, Jing, Pierce, Eric M., Parks, Jerry M., Elias, Dwayne A., Hettich, Robert L., and Gu, Baohua. Thu . "Quantitative Proteomic Analysis of Biological Processes and Responses of the Bacterium Desulfovibrio desulfuricans ND132 upon Deletion of Its Mercury Methylation Genes". United States. doi:10.1002/pmic.201700479. https://www.osti.gov/servlets/purl/1468234.
@article{osti_1468234,
title = {Quantitative Proteomic Analysis of Biological Processes and Responses of the Bacterium Desulfovibrio desulfuricans ND132 upon Deletion of Its Mercury Methylation Genes},
author = {Qian, Chen and Chen, Hongmei and Johs, Alexander and Lu, Xia and An, Jing and Pierce, Eric M. and Parks, Jerry M. and Elias, Dwayne A. and Hettich, Robert L. and Gu, Baohua},
abstractNote = {Recent studies of microbial mercury (Hg) methylation revealed a key gene pair, hgcAB, which is essential for methylmercury (MeHg) production in the environment. However, many aspects of the mechanism and biological processes underlying Hg methylation, as well as any additional physiological functions of the hgcAB genes, remain unknown. Here, quantitative proteomics are used to identify changes in potential functional processes related to hgcAB gene deletion in the Hg-methylating bacterium Desulfovibrio desulfuricans ND132. Global proteomics analyses indicate that the wild type and ΔhgcAB strains are similar with respect to the whole proteome and the identified number of proteins, but differ significantly in the abundance of specific proteins. The authors observe changes in the abundance of proteins related to the glycolysis pathway and one-carbon metabolism, suggesting that the hgcAB gene pair is linked to carbon metabolism. Unexpectedly, the authors find that the deletion of hgcAB significantly impacts a range of metal transport proteins, specifically membrane efflux pumps such as those associated with heavy metal copper (Cu) export, leading to decreased Cu uptake in the ΔhgcAB mutant. This observation indicates possible linkages between this set of proteins and metal homeostasis in the cell. However, hgcAB gene expression is not induced by Hg, as evidenced by similarly low abundance of HgcA and HgcB proteins in the absence or presence of Hg (500 nm). Altogether, these results suggest an apparent link between HgcAB, one-carbon metabolism, and metal homeostasis, thereby providing insights for further exploration of biochemical mechanisms and biological functions of microbial Hg methylation.},
doi = {10.1002/pmic.201700479},
journal = {Proteomics},
number = 17,
volume = 18,
place = {United States},
year = {2018},
month = {8}
}

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Works referenced in this record:

Effects of Cellular Sorption on Mercury Bioavailability and Methylmercury Production by Desulfovibrio desulfuricans ND132
journal, November 2016

  • Liu, Yu-Rong; Lu, Xia; Zhao, Linduo
  • Environmental Science & Technology, Vol. 50, Issue 24
  • DOI: 10.1021/acs.est.6b04041

Accurate Proteome-wide Label-free Quantification by Delayed Normalization and Maximal Peptide Ratio Extraction, Termed MaxLFQ
journal, June 2014

  • Cox, Jürgen; Hein, Marco Y.; Luber, Christian A.
  • Molecular & Cellular Proteomics, Vol. 13, Issue 9
  • DOI: 10.1074/mcp.M113.031591

PSORTdb: a protein subcellular localization database for bacteria
journal, December 2004


Acetogenesis and the Wood–Ljungdahl pathway of CO2 fixation
journal, December 2008

  • Ragsdale, Stephen W.; Pierce, Elizabeth
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1784, Issue 12, p. 1873-1898
  • DOI: 10.1016/j.bbapap.2008.08.012

Nickel-based Enzyme Systems
journal, April 2009


Intracellular Hg(0) Oxidation in Desulfovibrio desulfuricans ND132
journal, October 2016

  • Wang, Yuwei; Schaefer, Jeffra K.; Mishra, Bhoopesh
  • Environmental Science & Technology, Vol. 50, Issue 20
  • DOI: 10.1021/acs.est.6b03299

Andromeda: A Peptide Search Engine Integrated into the MaxQuant Environment
journal, April 2011

  • Cox, Jürgen; Neuhauser, Nadin; Michalski, Annette
  • Journal of Proteome Research, Vol. 10, Issue 4
  • DOI: 10.1021/pr101065j

Mechanisms of copper homeostasis in bacteria
journal, January 2013

  • Argüello, José M.; Raimunda, Daniel; Padilla-Benavides, Teresita
  • Frontiers in Cellular and Infection Microbiology, Vol. 3
  • DOI: 10.3389/fcimb.2013.00073

Thiol-Facilitated Cell Export and Desorption of Methylmercury by Anaerobic Bacteria
journal, September 2015


KAAS: an automatic genome annotation and pathway reconstruction server
journal, May 2007

  • Moriya, Y.; Itoh, M.; Okuda, S.
  • Nucleic Acids Research, Vol. 35, Issue S2, p. W182-W185
  • DOI: 10.1093/nar/gkm321

Mercury Methylation by the Methanogen Methanospirillum hungatei
journal, August 2013

  • Yu, Ri-Qing; Reinfelder, John R.; Hines, Mark E.
  • Applied and Environmental Microbiology, Vol. 79, Issue 20
  • DOI: 10.1128/AEM.01556-13

Recent advances toward a molecular mechanism of efflux pump inhibition
journal, May 2015


Unexpected Effects of Gene Deletion on Interactions of Mercury with the Methylation-Deficient Mutant Δ hgcAB
journal, April 2014

  • Lin, Hui; Hurt, Richard A.; Johs, Alexander
  • Environmental Science & Technology Letters, Vol. 1, Issue 5
  • DOI: 10.1021/ez500107r

KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 2000

  • Kanehisa, Minoru; Goto, Susumu
  • Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30
  • DOI: 10.1093/nar/28.1.27

Deep Proteomics of Mouse Skeletal Muscle Enables Quantitation of Protein Isoforms, Metabolic Pathways, and Transcription Factors
journal, January 2015

  • Deshmukh, Atul S.; Murgia, Marta; Nagaraj, Nagarjuna
  • Molecular & Cellular Proteomics, Vol. 14, Issue 4
  • DOI: 10.1074/mcp.M114.044222

The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases
journal, November 2015

  • Caspi, Ron; Billington, Richard; Ferrer, Luciana
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1164

Mercury Methylation by Novel Microorganisms from New Environments
journal, September 2013

  • Gilmour, Cynthia C.; Podar, Mircea; Bullock, Allyson L.
  • Environmental Science & Technology, Vol. 47, Issue 20
  • DOI: 10.1021/es403075t

Large-scale analysis of the yeast proteome by multidimensional protein identification technology
journal, March 2001

  • Washburn, Michael P.; Wolters, Dirk; Yates, John R.
  • Nature Biotechnology, Vol. 19, Issue 3
  • DOI: 10.1038/85686

Mercury Methylation Independent of the Acetyl-Coenzyme A Pathway in Sulfate-Reducing Bacteria
journal, September 2003

  • Ekstrom, E. B.; Morel, F. M. M.; Benoit, J. M.
  • Applied and Environmental Microbiology, Vol. 69, Issue 9, p. 5414-5422
  • DOI: 10.1128/AEM.69.9.5414-5422.2003

Oxidation and methylation of dissolved elemental mercury by anaerobic bacteria
journal, August 2013

  • Hu, Haiyan; Lin, Hui; Zheng, Wang
  • Nature Geoscience, Vol. 6, Issue 9
  • DOI: 10.1038/ngeo1894

The Perseus computational platform for comprehensive analysis of (prote)omics data
journal, June 2016

  • Tyanova, Stefka; Temu, Tikira; Sinitcyn, Pavel
  • Nature Methods, Vol. 13, Issue 9
  • DOI: 10.1038/nmeth.3901

Molybdenum cofactors, enzymes and pathways
journal, August 2009

  • Schwarz, Günter; Mendel, Ralf R.; Ribbe, Markus W.
  • Nature, Vol. 460, Issue 7257
  • DOI: 10.1038/nature08302

Efflux-mediated heavy metal resistance in prokaryotes
journal, June 2003


Sulfate-Reducing Bacterium Desulfovibrio desulfuricans ND132 as a Model for Understanding Bacterial Mercury Methylation
journal, April 2011

  • Gilmour, Cynthia C.; Elias, Dwayne A.; Kucken, Amy M.
  • Applied and Environmental Microbiology, Vol. 77, Issue 12, p. 3938-3951
  • DOI: 10.1128/AEM.02993-10

Effects of warming on the degradation and production of low-molecular-weight labile organic carbon in an Arctic tundra soil
journal, April 2016


Coordination Chemistry of Bacterial Metal Transport and Sensing
journal, October 2009

  • Ma, Zhen; Jacobsen, Faith E.; Giedroc, David P.
  • Chemical Reviews, Vol. 109, Issue 10
  • DOI: 10.1021/cr900077w

R Factors Mediate Resistance to Mercury, Nickel, and Cobalt
journal, May 1967


KEGG for integration and interpretation of large-scale molecular data sets
journal, November 2011

  • Kanehisa, M.; Goto, S.; Sato, Y.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr988

Site-Directed Mutagenesis of HgcA and HgcB Reveals Amino Acid Residues Important for Mercury Methylation
journal, February 2015

  • Smith, Steven D.; Bridou, Romain; Johs, Alexander
  • Applied and Environmental Microbiology, Vol. 81, Issue 9
  • DOI: 10.1128/AEM.00217-15

BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks
journal, June 2005


Active transport, substrate specificity, and methylation of Hg(II) in anaerobic bacteria
journal, May 2011

  • Schaefer, J. K.; Rocks, S. S.; Zheng, W.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 21
  • DOI: 10.1073/pnas.1105781108

The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases
journal, November 2013

  • Caspi, Ron; Altman, Tomer; Billington, Richard
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1103

Effect of the Deletion of qmoABC and the Promoter-Distal Gene Encoding a Hypothetical Protein on Sulfate Reduction in Desulfovibrio vulgaris Hildenborough
journal, June 2010

  • Zane, G. M.; Yen, H. -c. B.; Wall, J. D.
  • Applied and Environmental Microbiology, Vol. 76, Issue 16
  • DOI: 10.1128/AEM.00691-10

Relationships between bacterial energetic metabolism, mercury methylation potential, and hgcA/hgcB gene expression in Desulfovibrio dechloroacetivorans BerOc1
journal, March 2015

  • Goñi-Urriza, Marisol; Corsellis, Yannick; Lanceleur, Laurent
  • Environmental Science and Pollution Research, Vol. 22, Issue 18
  • DOI: 10.1007/s11356-015-4273-5

The superfamily of heme-copper respiratory oxidases.
journal, September 1994


The Genetic Basis for Bacterial Mercury Methylation
journal, February 2013


Biological Cycles for Toxic Elements in the Environment
journal, March 1974


Coupled Mercury–Cell Sorption, Reduction, and Oxidation on Methylmercury Production by Geobacter sulfurreducens PCA
journal, October 2014

  • Lin, Hui; Morrell-Falvey, Jennifer L.; Rao, Balaji
  • Environmental Science & Technology, Vol. 48, Issue 20
  • DOI: 10.1021/es502537a

Global prevalence and distribution of genes and microorganisms involved in mercury methylation
journal, October 2015

  • Podar, Mircea; Gilmour, Cynthia C.; Brandt, Craig C.
  • Science Advances, Vol. 1, Issue 9
  • DOI: 10.1126/sciadv.1500675

Pathways of anaerobic organic matter decomposition in tundra soils from Barrow, Alaska: BIOGEOCHEMISTRY OF ANOXIC ARCTIC TUNDRA
journal, November 2015

  • Herndon, Elizabeth M.; Mann, Benjamin F.; Roy Chowdhury, Taniya
  • Journal of Geophysical Research: Biogeosciences, Vol. 120, Issue 11
  • DOI: 10.1002/2015JG003147

Organization, Expression, and Evolution of Genes for Mercury Resistance
journal, October 1986


Enzymatic catalysis of mercury methylation by Desulfovibrio desulfuricans LS.
journal, January 1994


Metabolic Pathways Leading to Mercury Methylation in Desulfovibrio desulfuricans LS †
journal, January 1994


    Works referencing / citing this record:

    Shotgun proteomic analysis of nanoparticle-synthesizing Desulfovibrio alaskensis in response to platinum and palladium
    journal, December 2019

    • Capeness, Michael J.; Imrie, Lisa; Mühlbauer, Lukas F.
    • Microbiology, Vol. 165, Issue 12
    • DOI: 10.1099/mic.0.000840

    Kinetics of Enzymatic Mercury Methylation at Nanomolar Concentrations Catalyzed by HgcAB
    journal, April 2019

    • Date, Swapneeta S.; Parks, Jerry M.; Rush, Katherine W.
    • Applied and Environmental Microbiology, Vol. 85, Issue 13
    • DOI: 10.1128/aem.00438-19