Physiological and proteomic analyses of Fe( III )‐reducing co‐cultures of Desulfotomaculum reducens MI ‐1 and Geobacter sulfurreducens PCA
Abstract
Abstract We established Fe( III )‐reducing co‐cultures of two species of metal‐reducing bacteria, the Gram‐positive Desulfotomaculum reducens MI ‐1 and the Gram‐negative Geobacter sulfurreducens PCA . Co‐cultures were given pyruvate, a substrate that D. reducens can ferment and use as electron donor for Fe( III ) reduction. G. sulfurreducens relied upon products of pyruvate oxidation by D. reducens (acetate, hydrogen) for use as electron donor in the co‐culture. Co‐cultures reduced Fe( III ) to Fe( II ) robustly, and Fe( II ) was consistently detected earlier in co‐cultures than pure cultures. Notably, faster cell growth, and correspondingly faster pyruvate oxidation, was observed by D. reducens in co‐cultures. Global comparative proteomic analysis was performed to observe differential protein abundance during co‐culture vs. pure culture growth. Proteins previously associated with Fe( III ) reduction in G. sulfurreducens, namely c‐type cytochromes and type IV pili proteins, were significantly increased in abundance in co‐cultures relative to pure cultures. D. reducens ribosomal proteins were significantly increased in co‐cultures, likely a reflection of faster growth rates observed for D. reducens cells while in co‐culture. Furthermore, we developed multiple reaction monitoring ( MRM ) assays to quantitate specific biomarker peptides. The assays were validated in pure and co‐cultures, and protein abundance ratios from targetedmore »
- Authors:
-
[1];
- Department of Microbiology Cornell University Ithaca New York
- Pacific Northwest National Laboratory Richland Washington
- Proteomics and Mass Spectrometry Facility Cornell University Ithaca New York
- Department of Materials Science and Engineering Cornell University Ithaca New York
- Department of Civil and Environmental Engineering Cornell University Ithaca New York
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1454378
- Grant/Contract Number:
- DE‐AC05‐76RL01830
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Geobiology
- Additional Journal Information:
- Journal Name: Geobiology Journal Volume: 16 Journal Issue: 5; Journal ID: ISSN 1472-4677
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Otwell, Anne E., Callister, Stephen J., Sherwood, Robert W., Zhang, Sheng, Goldman, Abby R., Smith, Richard D., and Richardson, Ruth E. Physiological and proteomic analyses of Fe( III )‐reducing co‐cultures of Desulfotomaculum reducens MI ‐1 and Geobacter sulfurreducens PCA. United Kingdom: N. p., 2018.
Web. doi:10.1111/gbi.12295.
Otwell, Anne E., Callister, Stephen J., Sherwood, Robert W., Zhang, Sheng, Goldman, Abby R., Smith, Richard D., & Richardson, Ruth E. Physiological and proteomic analyses of Fe( III )‐reducing co‐cultures of Desulfotomaculum reducens MI ‐1 and Geobacter sulfurreducens PCA. United Kingdom. https://doi.org/10.1111/gbi.12295
Otwell, Anne E., Callister, Stephen J., Sherwood, Robert W., Zhang, Sheng, Goldman, Abby R., Smith, Richard D., and Richardson, Ruth E. Fri .
"Physiological and proteomic analyses of Fe( III )‐reducing co‐cultures of Desulfotomaculum reducens MI ‐1 and Geobacter sulfurreducens PCA". United Kingdom. https://doi.org/10.1111/gbi.12295.
@article{osti_1454378,
title = {Physiological and proteomic analyses of Fe( III )‐reducing co‐cultures of Desulfotomaculum reducens MI ‐1 and Geobacter sulfurreducens PCA},
author = {Otwell, Anne E. and Callister, Stephen J. and Sherwood, Robert W. and Zhang, Sheng and Goldman, Abby R. and Smith, Richard D. and Richardson, Ruth E.},
abstractNote = {Abstract We established Fe( III )‐reducing co‐cultures of two species of metal‐reducing bacteria, the Gram‐positive Desulfotomaculum reducens MI ‐1 and the Gram‐negative Geobacter sulfurreducens PCA . Co‐cultures were given pyruvate, a substrate that D. reducens can ferment and use as electron donor for Fe( III ) reduction. G. sulfurreducens relied upon products of pyruvate oxidation by D. reducens (acetate, hydrogen) for use as electron donor in the co‐culture. Co‐cultures reduced Fe( III ) to Fe( II ) robustly, and Fe( II ) was consistently detected earlier in co‐cultures than pure cultures. Notably, faster cell growth, and correspondingly faster pyruvate oxidation, was observed by D. reducens in co‐cultures. Global comparative proteomic analysis was performed to observe differential protein abundance during co‐culture vs. pure culture growth. Proteins previously associated with Fe( III ) reduction in G. sulfurreducens, namely c‐type cytochromes and type IV pili proteins, were significantly increased in abundance in co‐cultures relative to pure cultures. D. reducens ribosomal proteins were significantly increased in co‐cultures, likely a reflection of faster growth rates observed for D. reducens cells while in co‐culture. Furthermore, we developed multiple reaction monitoring ( MRM ) assays to quantitate specific biomarker peptides. The assays were validated in pure and co‐cultures, and protein abundance ratios from targeted MRM and global proteomic analysis correlate significantly.},
doi = {10.1111/gbi.12295},
journal = {Geobiology},
number = 5,
volume = 16,
place = {United Kingdom},
year = {Fri Jun 15 00:00:00 EDT 2018},
month = {Fri Jun 15 00:00:00 EDT 2018}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/gbi.12295
https://doi.org/10.1111/gbi.12295
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 3 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
OmcB, a c-Type Polyheme Cytochrome, Involved in Fe(III) Reduction in Geobacter sulfurreducens
journal, April 2003
- Leang, C.; Coppi, M. V.; Lovley, D. R.
- Journal of Bacteriology, Vol. 185, Issue 7
Direct Interspecies Electron Transfer between Geobacter metallireducens and Methanosarcina barkeri
journal, May 2014
- Rotaru, Amelia-Elena; Shrestha, Pravin Malla; Liu, Fanghua
- Applied and Environmental Microbiology, Vol. 80, Issue 15
The biogeochemistry and bioremediation of uranium and other priority radionuclides
journal, January 2014
- Newsome, Laura; Morris, Katherine; Lloyd, Jonathan R.
- Chemical Geology, Vol. 363
Computational and Experimental Analysis of Redundancy in the Central Metabolism of Geobacter sulfurreducens
journal, January 2008
- Segura, Daniel; Mahadevan, Radhakrishnan; Juárez, Katy
- PLoS Computational Biology, Vol. 4, Issue 2
DAnTE: a statistical tool for quantitative analysis of -omics data
journal, May 2008
- Polpitiya, A. D.; Qian, W. -J.; Jaitly, N.
- Bioinformatics, Vol. 24, Issue 13
A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by G eobacter sulfurreducens PCA : A trans-outer membrane electron transfer complex
journal, September 2014
- Liu, Yimo; Wang, Zheming; Liu, Juan
- Environmental Microbiology Reports, Vol. 6, Issue 6
Stepping stones in the electron transport from cells to electrodes in Geobacter sulfurreducens biofilms
journal, January 2013
- Bonanni, Pablo Sebastián; Massazza, Diego; Busalmen, Juan Pablo
- Physical Chemistry Chemical Physics, Vol. 15, Issue 25
Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange: Growth with electrons supplied solely by DIET
journal, September 2013
- Shrestha, Pravin Malla; Rotaru, Amelia-Elena; Aklujkar, Muktak
- Environmental Microbiology Reports, Vol. 5, Issue 6
Genome Sequence of the Sulfate-Reducing Bacterium Desulfotomaculum hydrothermale Lam5T
journal, January 2013
- Amin, O.; Fardeau, M. -L.; Valette, O.
- Genome Announcements, Vol. 1, Issue 1
Characterization of the surfaceome of the metal-reducing bacterium Desulfotomaculum reducens
journal, August 2014
- Dalla Vecchia, Elena; Shao, Paul P.; Suvorova, Elena
- Frontiers in Microbiology, Vol. 5
Syntrophic growth via quinone-mediated interspecies electron transfer
journal, February 2015
- Smith, Jessica A.; Nevin, Kelly P.; Lovley, Derek R.
- Frontiers in Microbiology, Vol. 6
Genome sequence of Desulfitobacterium hafniense DCB-2, a Gram-positive anaerobe capable of dehalogenation and metal reduction
journal, January 2012
- Kim, Sang-Hoon; Harzman, Christina; Davis, John K.
- BMC Microbiology, Vol. 12, Issue 1
Diving into the redox properties of Geobacter sulfurreducens cytochromes: a model for extracellular electron transfer
journal, January 2015
- Santos, Telma C.; Silva, Marta A.; Morgado, Leonor
- Dalton Transactions, Vol. 44, Issue 20
Identification of proteins capable of metal reduction from the proteome of the Gram-positive bacterium D esulfotomaculum reducens MI-1 using an NADH-based activity assay : Metal reductases from Gram-positive metal reducer
journal, January 2015
- Otwell, Anne Elyse; Sherwood, Robert W.; Zhang, Sheng
- Environmental Microbiology, Vol. 17, Issue 6
Normalization Approaches for Removing Systematic Biases Associated with Mass Spectrometry and Label-Free Proteomics
journal, February 2006
- Callister, Stephen J.; Barry, Richard C.; Adkins, Joshua N.
- Journal of Proteome Research, Vol. 5, Issue 2
A systematic investigation of multiheme c-type cytochromes in prokaryotes
journal, January 2010
- Sharma, Shailesh; Cavallaro, Gabriele; Rosato, Antonio
- JBIC Journal of Biological Inorganic Chemistry, Vol. 15, Issue 4
Advancing the High Throughput Identification of Liver Fibrosis Protein Signatures Using Multiplexed Ion Mobility Spectrometry
journal, January 2014
- Baker, Erin Shammel; Burnum-Johnson, Kristin E.; Jacobs, Jon M.
- Molecular & Cellular Proteomics, Vol. 13, Issue 4, p. 1119-1127
Proteomic Analysis of Stationary Phase in the Marine Bacterium "Candidatus Pelagibacter ubique"
journal, May 2008
- Sowell, S. M.; Norbeck, A. D.; Lipton, M. S.
- Applied and Environmental Microbiology, Vol. 74, Issue 13
Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens
journal, January 2007
- Shelobolina, Evgenya S.; Coppi, Maddalena V.; Korenevsky, Anton A.
- BMC Microbiology, Vol. 7, Issue 1
Absolute quantification of Dehalococcoides proteins: enzyme bioindicators of chlorinated ethene dehalorespiration
journal, October 2009
- Werner, Jeffrey J.; Ptak, A. Celeste; Rahm, Brian G.
- Environmental Microbiology, Vol. 11, Issue 10
Geobacter sulfurreducens sp. nov., a hydrogen- and acetate-oxidizing dissimilatory metal-reducing microorganism.
journal, January 1994
- Caccavo, F.; Lonergan, D. J.; Lovley, D. R.
- Applied and Environmental Microbiology, Vol. 60, Issue 10
Global analysis of the Deinococcus radiodurans proteome by using accurate mass tags
journal, August 2002
- Lipton, M. S.; Pasa-Tolic, L.; Anderson, G. A.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 17
Transcriptomic and Genetic Analysis of Direct Interspecies Electron Transfer
journal, February 2013
- Shrestha, Pravin Malla; Rotaru, Amelia-Elena; Summers, Zarath M.
- Applied and Environmental Microbiology, Vol. 79, Issue 7
Relating Chloroethene Respiration Rates in Dehalococcoides to Protein and mRNA Biomarkers
journal, August 2012
- Rowe, Annette R.; Heavner, Gretchen L.; Mansfeldt, Cresten B.
- Environmental Science & Technology, Vol. 46, Issue 17
IMG 4 version of the integrated microbial genomes comparative analysis system
journal, October 2013
- Markowitz, Victor M.; Chen, I-Min A.; Palaniappan, Krishna
- Nucleic Acids Research, Vol. 42, Issue D1
Proteome of Geobacter sulfurreducens in the presence of U(VI)
journal, October 2014
- Orellana, R.; Hixson, K. K.; Murphy, S.
- Microbiology, Vol. 160, Issue Pt_12
DOOR 2.0: presenting operons and their functions through dynamic and integrated views
journal, November 2013
- Mao, Xizeng; Ma, Qin; Zhou, Chuan
- Nucleic Acids Research, Vol. 42, Issue D1
Comparative genomic analysis of Geobacter sulfurreducens KN400, a strain with enhanced capacity for extracellular electron transfer and electricity production
journal, January 2012
- Butler, Jessica E.; Young, Nelson D.; Aklujkar, Muktak
- BMC Genomics, Vol. 13, Issue 1
Electromicrobiology
journal, October 2012
- Lovley, Derek R.
- Annual Review of Microbiology, Vol. 66, Issue 1
Biochemical characterization of purified OmcS, a c-type cytochrome required for insoluble Fe(III) reduction in Geobacter sulfurreducens
journal, April 2011
- Qian, Xinlei; Mester, Tünde; Morgado, Leonor
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 4
Direct Exchange of Electrons Within Aggregates of an Evolved Syntrophic Coculture of Anaerobic Bacteria
journal, December 2010
- Summers, Z. M.; Fogarty, H. E.; Leang, C.
- Science, Vol. 330, Issue 6009, p. 1413-1415
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
journal, December 2008
- Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A.
- Nature Protocols, Vol. 4, Issue 1
Extracellular electron transfer via microbial nanowires
journal, June 2005
- Reguera, Gemma; McCarthy, Kevin D.; Mehta, Teena
- Nature, Vol. 435, Issue 7045, p. 1098-1101
Characterizing Microbial Community and Geochemical Dynamics at Hydrothermal Vents Using Osmotically Driven Continuous Fluid Samplers
journal, April 2013
- Robidart, Julie; Callister, Stephen J.; Song, Pengfei
- Environmental Science & Technology, Vol. 47, Issue 9
Enzymatic U(VI) reduction by Desulfosporosinus species
journal, January 2004
- Suzuki, Yohey; Kelly, Shelly D.; Kemner, Ken M.
- Radiochimica Acta, Vol. 92, Issue 1
Growth with hydrogen, and further physiological characteristics of Desulfotomaculum species
journal, November 1985
- Klemps, Robert; Cypionka, Heribert; Widdel, Friedrich
- Archives of Microbiology, Vol. 143, Issue 2
A Statistical Method for Assessing Peptide Identification Confidence in Accurate Mass and Time Tag Proteomics
journal, August 2011
- Stanley, Jeffrey R.; Adkins, Joshua N.; Slysz, Gordon W.
- Analytical Chemistry, Vol. 83, Issue 16
Fe(III) reduction during pyruvate fermentation by Desulfotomaculum reducens strain MI-1
journal, November 2013
- Dalla Vecchia, E.; Suvorova, E. I.; Maillard, J.
- Geobiology, Vol. 12, Issue 1
The genome of the Gram-positive metal- and sulfate-reducing bacterium Desulfotomaculum reducens strain MI-1: The genome of Desulfotomaculum reducens
journal, June 2010
- Junier, Pilar; Junier, Thomas; Podell, Sheila
- Environmental Microbiology
A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane
journal, January 2014
- Rotaru, Amelia-Elena; Shrestha, Pravin Malla; Liu, Fanghua
- Energy Environ. Sci., Vol. 7, Issue 1
Development of a biomarker for Geobacter activity and strain composition; Proteogenomic analysis of the citrate synthase protein during bioremediation of U(VI): Geobacter citrate synthase biomarker
journal, December 2010
- Wilkins, Michael J.; Callister, Stephen J.; Miletto, Marzia
- Microbial Biotechnology, Vol. 4, Issue 1
Dynamic Succession of Groundwater Functional Microbial Communities in Response to Emulsified Vegetable Oil Amendment during Sustained In Situ U(VI) Reduction
journal, April 2015
- Zhang, Ping; Wu, Wei-Min; Van Nostrand, Joy D.
- Applied and Environmental Microbiology, Vol. 81, Issue 12
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
Cysteine-mediated electron transfer in syntrophic acetate oxidation by cocultures of Geobacter sulfurreducens and Wolinella succinogenes
journal, July 2002
- Kaden, Jan; S. Galushko, Alexander; Schink, Bernhard
- Archives of Microbiology, Vol. 178, Issue 1
Direct involvement of ombB, omaB, and omcB genes in extracellular reduction of Fe(III) by Geobacter sulfurreducens PCA
journal, October 2015
- Liu, Yimo; Fredrickson, James K.; Zachara, John M.
- Frontiers in Microbiology, Vol. 6
Microbial interspecies electron transfer via electric currents through conductive minerals
journal, June 2012
- Kato, S.; Hashimoto, K.; Watanabe, K.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 25
Significant Association between Sulfate-Reducing Bacteria and Uranium-Reducing Microbial Communities as Revealed by a Combined Massively Parallel Sequencing-Indicator Species Approach
journal, August 2010
- Cardenas, E.; Wu, W. -M.; Leigh, M. B.
- Applied and Environmental Microbiology, Vol. 76, Issue 20
Extracellular electron transfer
journal, October 2001
- Hernandez, M. E.; Newman, D. K.
- Cellular and Molecular Life Sciences, Vol. 58, Issue 11
Rapid Assay for Microbially Reducible Ferric Iron in Aquatic Sediments
journal, January 1987
- Lovley, Derek R.; Phillips, Elizabeth J. P.
- Applied and Environmental Microbiology, Vol. 53, Issue 7
Comparative Proteomic Analysis of Desulfotomaculum reducens MI-1: Insights into the Metabolic Versatility of a Gram-Positive Sulfate- and Metal-Reducing Bacterium
journal, February 2016
- Otwell, Anne E.; Callister, Stephen J.; Zink, Erika M.
- Frontiers in Microbiology, Vol. 7
Interspecies Electron Transfer via Hydrogen and Formate Rather than Direct Electrical Connections in Cocultures of Pelobacter carbinolicus and Geobacter sulfurreducens
journal, August 2012
- Rotaru, Amelia-Elena; Shrestha, Pravin M.; Liu, Fanghua
- Applied and Environmental Microbiology, Vol. 78, Issue 21
Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists
journal, November 2008
- Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A.
- Nucleic Acids Research, Vol. 37, Issue 1
Suspension Array Analysis of 16S rRNA from Fe- and SO42-Reducing Bacteria in Uranium-Contaminated Sediments Undergoing Bioremediation
journal, July 2006
- Chandler, D. P.; Jarrell, A. E.; Roden, E. R.
- Applied and Environmental Microbiology, Vol. 72, Issue 7
Sulfate-reducing bacterium grows with Cr(VI), U(VI), Mn(IV), and Fe(III) as electron acceptors
journal, May 1998
- Tebo, Bradley M.; Obraztsova, Anna Ya
- FEMS Microbiology Letters, Vol. 162, Issue 1
Selected reaction monitoring for quantitative proteomics: a tutorial
journal, January 2008
- Lange, Vinzenz; Picotti, Paola; Domon, Bruno
- Molecular Systems Biology, Vol. 4, Issue 1
Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction
journal, October 2006
- Weber, Karrie A.; Achenbach, Laurie A.; Coates, John D.
- Nature Reviews Microbiology, Vol. 4, Issue 10, p. 752-764
Proteins involved in electron transfer to Fe(III) and Mn(IV) oxides by Geobacter sulfurreducens and Geobacter uraniireducens
journal, January 2013
- Aklujkar, M.; Coppi, M. V.; Leang, C.
- Microbiology, Vol. 159, Issue Pt_3
Bioenergetic challenges of microbial iron metabolisms
journal, July 2011
- Bird, Lina J.; Bonnefoy, Violaine; Newman, Dianne K.
- Trends in Microbiology, Vol. 19, Issue 7
Spectral Probabilities and Generating Functions of Tandem Mass Spectra: A Strike against Decoy Databases
journal, August 2008
- Kim, Sangtae; Gupta, Nitin; Pevzner, Pavel A.
- Journal of Proteome Research, Vol. 7, Issue 8
PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes
journal, May 2010
- Yu, Nancy Y.; Wagner, James R.; Laird, Matthew R.
- Bioinformatics, Vol. 26, Issue 13
Proteomic tools to decipher microbial community structure and functioning
journal, December 2014
- Arsène-Ploetze, Florence; Bertin, Philippe N.; Carapito, Christine
- Environmental Science and Pollution Research, Vol. 22, Issue 18
Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens
journal, January 2003
- Lloyd, Jon R.; Leang, Ching; Myerson, Allison L. HODGES
- Biochemical Journal, Vol. 369, Issue 1
Dissimilatory Fe(III) and Mn(IV) Reduction
book, January 2004
- Lovley, Derek R.; Holmes, Dawn E.; Nevin, Kelly P.
- Advances in Microbial Physiology
Surface multiheme c-type cytochromes from Thermincola potens and implications for respiratory metal reduction by Gram-positive bacteria
journal, January 2012
- Carlson, H. K.; Iavarone, A. T.; Gorur, A.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 5
Reversed-phase chromatography with multiple fraction concatenation strategy for proteome profiling of human MCF10A cells
journal, April 2011
- Wang, Yuexi; Yang, Feng; Gritsenko, Marina A.
- PROTEOMICS, Vol. 11, Issue 10
Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens
journal, October 2006
- Holmes, Dawn E.; Chaudhuri, Swades K.; Nevin, Kelly P.
- Environmental Microbiology, Vol. 8, Issue 10