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Title: Global Proteome Response to Deletion of Genes Related to Mercury Methylation and Dissimilatory Metal Reduction Reveals Changes in Respiratory Metabolism in Geobacter sulfurreducens PCA

Abstract

Geobacter sulfurreducens PCA can reduce, sorb, and methylate mercury (Hg); however, the underlying biochemical mechanisms of these processes and interdependent metabolic pathways remain unknown. In this study, shotgun proteomics was used to compare global proteome profiles between wild-type G. sulfurreducens PCA and two mutant strains: a ΔhgcAB mutant, which is deficient in two genes known to be essential for Hg methylation and a ΔomcBESTZ mutant, which is deficient in five outer membrane c-type cytochromes and thus impaired in its ability for dissimilatory metal ion reduction. We were able to delineate the global response of G. sulfurreducens PCA in both mutants and identify cellular networks and metabolic pathways that were affected by the loss of these genes. Deletion of hgcAB increased the relative abundances of proteins implicated in extracellular electron transfer, including most of the c-type cytochromes, PilA-C, and OmpB, and is consistent with a previously observed increase in Hg reduction in the hgcAB mutant. Deletion of omcBESTZ was found to significantly increase relative abundances of various methyltransferases, suggesting that a loss of dissimilatory reduction capacity results in elevated activity among one-carbon metabolic pathways and thus increased methylation. We show that G. sulfurreducens PCA encodes only the folate branch of themore » Wood Ljungdahl pathway, and proteins associated with the folate branch were found at lower abundance in the ΔhgcAB mutant strain than the wild type. In conclusion, this observation supports the hypothesis that the function of HgcA and HgcB may be linked to one carbon metabolism through the folate branch of the Wood-Ljungdahl pathway by providing methyl groups required for Hg methylation.« less

Authors:
 [1];  [2];  [2];  [2];  [2];  [3];  [1];  [2]
  1. Chemical Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, United States, Graduate School of Genome Science and Technology, University of Tennessee, Knoxville, Tennessee 37996, United States
  2. Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, United States
  3. Chemical Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, United States
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1315838
Alternate Identifier(s):
OSTI ID: 1319186
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Published Article
Journal Name:
Journal of Proteome Research
Additional Journal Information:
Journal Name: Journal of Proteome Research Journal Volume: 15 Journal Issue: 10; Journal ID: ISSN 1535-3893
Publisher:
American Chemical Society
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; Comparative proteomics; gene deletion; acetyl-CoA pathway; mercury reduction; methylation; metabolic processes; ΔomcBESTZ; ΔhgcAB

Citation Formats

Qian, Chen, Johs, Alexander, Chen, Hongmei, Mann, Benjamin F., Lu, Xia, Abraham, Paul E., Hettich, Robert L., and Gu, Baohua. Global Proteome Response to Deletion of Genes Related to Mercury Methylation and Dissimilatory Metal Reduction Reveals Changes in Respiratory Metabolism in Geobacter sulfurreducens PCA. United States: N. p., 2016. Web. doi:10.1021/acs.jproteome.6b00263.
Qian, Chen, Johs, Alexander, Chen, Hongmei, Mann, Benjamin F., Lu, Xia, Abraham, Paul E., Hettich, Robert L., & Gu, Baohua. Global Proteome Response to Deletion of Genes Related to Mercury Methylation and Dissimilatory Metal Reduction Reveals Changes in Respiratory Metabolism in Geobacter sulfurreducens PCA. United States. https://doi.org/10.1021/acs.jproteome.6b00263
Qian, Chen, Johs, Alexander, Chen, Hongmei, Mann, Benjamin F., Lu, Xia, Abraham, Paul E., Hettich, Robert L., and Gu, Baohua. Fri . "Global Proteome Response to Deletion of Genes Related to Mercury Methylation and Dissimilatory Metal Reduction Reveals Changes in Respiratory Metabolism in Geobacter sulfurreducens PCA". United States. https://doi.org/10.1021/acs.jproteome.6b00263.
@article{osti_1315838,
title = {Global Proteome Response to Deletion of Genes Related to Mercury Methylation and Dissimilatory Metal Reduction Reveals Changes in Respiratory Metabolism in Geobacter sulfurreducens PCA},
author = {Qian, Chen and Johs, Alexander and Chen, Hongmei and Mann, Benjamin F. and Lu, Xia and Abraham, Paul E. and Hettich, Robert L. and Gu, Baohua},
abstractNote = {Geobacter sulfurreducens PCA can reduce, sorb, and methylate mercury (Hg); however, the underlying biochemical mechanisms of these processes and interdependent metabolic pathways remain unknown. In this study, shotgun proteomics was used to compare global proteome profiles between wild-type G. sulfurreducens PCA and two mutant strains: a ΔhgcAB mutant, which is deficient in two genes known to be essential for Hg methylation and a ΔomcBESTZ mutant, which is deficient in five outer membrane c-type cytochromes and thus impaired in its ability for dissimilatory metal ion reduction. We were able to delineate the global response of G. sulfurreducens PCA in both mutants and identify cellular networks and metabolic pathways that were affected by the loss of these genes. Deletion of hgcAB increased the relative abundances of proteins implicated in extracellular electron transfer, including most of the c-type cytochromes, PilA-C, and OmpB, and is consistent with a previously observed increase in Hg reduction in the hgcAB mutant. Deletion of omcBESTZ was found to significantly increase relative abundances of various methyltransferases, suggesting that a loss of dissimilatory reduction capacity results in elevated activity among one-carbon metabolic pathways and thus increased methylation. We show that G. sulfurreducens PCA encodes only the folate branch of the Wood Ljungdahl pathway, and proteins associated with the folate branch were found at lower abundance in the ΔhgcAB mutant strain than the wild type. In conclusion, this observation supports the hypothesis that the function of HgcA and HgcB may be linked to one carbon metabolism through the folate branch of the Wood-Ljungdahl pathway by providing methyl groups required for Hg methylation.},
doi = {10.1021/acs.jproteome.6b00263},
journal = {Journal of Proteome Research},
number = 10,
volume = 15,
place = {United States},
year = {Fri Sep 02 00:00:00 EDT 2016},
month = {Fri Sep 02 00:00:00 EDT 2016}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1021/acs.jproteome.6b00263

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Cited by: 21 works
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Works referenced in this record:

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

The Eastern and Western branches of the Wood/Ljungdahl pathway: how the East and West were won
journal, January 1997


Bioinformatics Study on Relationship of Hyperlipidemia and Phospholipids Based on Cytoscape Software
conference, January 2014

  • Shi, Zhongfeng; Feng, Yifan; Rui, Wen
  • 2014 International Conference on Mechatronics, Electronic, Industrial and Control Engineering (MEIC-14), Advances in Engineering Research
  • DOI: 10.2991/meic-14.2014.80

Alignment of the c-Type Cytochrome OmcS along Pili of Geobacter sulfurreducens
journal, April 2010

  • Leang, C.; Qian, X.; Mester, T.
  • Applied and Environmental Microbiology, Vol. 76, Issue 12, p. 4080-4084
  • DOI: 10.1128/AEM.00023-10

Global Change and Mercury
journal, September 2013


Moving Away from the Reference Genome: Evaluating a Peptide Sequencing Tagging Approach for Single Amino Acid Polymorphism Identifications in the Genus Populus
journal, July 2013

  • Abraham, Paul; Adams, Rachel M.; Tuskan, Gerald A.
  • Journal of Proteome Research, Vol. 12, Issue 8
  • DOI: 10.1021/pr400192r

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

Cysteine Inhibits Mercury Methylation by Geobacter sulfurreducens PCA Mutant Δ omcBESTZ
journal, April 2015


Crystal structures of the CusA efflux pump suggest methionine-mediated metal transport
journal, September 2010

  • Long, Feng; Su, Chih-Chia; Zimmermann, Michael T.
  • Nature, Vol. 467, Issue 7314
  • DOI: 10.1038/nature09395

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

Enzymology of the Wood-Ljungdahl Pathway of Acetogenesis
journal, March 2008


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

Two RND proteins involved in heavy metal efflux in Caulobacter crescentus belong to separate clusters within proteobacteria
journal, January 2013

  • Valencia, Estela Y.; Braz, Vânia S.; Guzzo, Cristiane
  • BMC Microbiology, Vol. 13, Issue 1
  • DOI: 10.1186/1471-2180-13-79

IDPicker 2.0: Improved Protein Assembly with High Discrimination Peptide Identification Filtering
journal, August 2009

  • Ma, Ze-Qiang; Dasari, Surendra; Chambers, Matthew C.
  • Journal of Proteome Research, Vol. 8, Issue 8
  • DOI: 10.1021/pr900360j

Genome of Geobacter sulfurreducens: Metal Reduction in Subsurface Environments
journal, December 2003

  • Methe, B. A.; Nelson, K. E.; Eisen, J. A.
  • Science, Vol. 302, Issue 5652, p. 1967-1969
  • DOI: 10.1126/science.1088727

The Chemical Cycle and Bioaccumulation of Mercury
journal, November 1998


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

Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
journal, September 1997

  • Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A.
  • Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402
  • DOI: 10.1093/nar/25.17.3389

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


A Ni-Fe-Cu Center in a Bifunctional Carbon Monoxide Dehydrogenase/ Acetyl-CoA Synthase
journal, October 2002


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


Proteins involved in electron transfer to Fe(III) and Mn(IV) oxides by Geobacter sulfurreducens and Geobacter uraniireducens
journal, January 2013


MyriMatch:  Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis
journal, February 2007

  • Tabb, David L.; Fernando, Christopher G.; Chambers, Matthew C.
  • Journal of Proteome Research, Vol. 6, Issue 2
  • DOI: 10.1021/pr0604054

Development of an Enhanced Metaproteomic Approach for Deepening the Microbiome Characterization of the Human Infant Gut
journal, October 2014

  • Xiong, Weili; Giannone, Richard J.; Morowitz, Michael J.
  • Journal of Proteome Research, Vol. 14, Issue 1
  • DOI: 10.1021/pr500936p

Detecting Differential and Correlated Protein Expression in Label-Free Shotgun Proteomics
journal, November 2006

  • Zhang, Bing; VerBerkmoes, Nathan C.; Langston, Michael A.
  • Journal of Proteome Research, Vol. 5, Issue 11
  • DOI: 10.1021/pr0600273

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

The Genetic Basis for Bacterial Mercury Methylation
journal, February 2013


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

Catalysis of Methyl Group Transfers Involving Tetrahydrofolate and B12
book, January 2008


Influence of External Resistance on Electrogenesis, Methanogenesis, and Anode Prokaryotic Communities in Microbial Fuel Cells
journal, November 2010

  • Jung, Sokhee; Regan, John M.
  • Applied and Environmental Microbiology, Vol. 77, Issue 2
  • DOI: 10.1128/AEM.01392-10

Proteomic Characterization of Cellular and Molecular Processes that Enable the Nanoarchaeum equitans-Ignicoccus hospitalis Relationship
journal, August 2011


Mercury Reduction and Cell-Surface Adsorption by Geobacter sulfurreducens PCA
journal, September 2013

  • Hu, Haiyan; Lin, Hui; Zheng, Wang
  • Environmental Science & Technology, Vol. 47, Issue 19
  • DOI: 10.1021/es400527m

Systematic Comparison of Label-Free, Metabolic Labeling, and Isobaric Chemical Labeling for Quantitative Proteomics on LTQ Orbitrap Velos
journal, January 2012

  • Li, Zhou; Adams, Rachel M.; Chourey, Karuna
  • Journal of Proteome Research, Vol. 11, Issue 3
  • DOI: 10.1021/pr200748h

Role of Geobacter sulfurreducens Outer Surface c-Type Cytochromes in Reduction of Soil Humic Acid and Anthraquinone-2,6-Disulfonate
journal, February 2010

  • Voordeckers, J. W.; Kim, B. -C.; Izallalen, M.
  • Applied and Environmental Microbiology, Vol. 76, Issue 7
  • DOI: 10.1128/AEM.02250-09

Structure and mechanism of the tripartite CusCBA heavy-metal efflux complex
journal, April 2012

  • Long, Feng; Su, Chih-Chia; Lei, Hsiang-Ting
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1592
  • DOI: 10.1098/rstb.2011.0203