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Title: Proteomic analysis reveals metabolic and regulatory systems involved in the syntrophic and axenic lifestyle of Syntrophomonas wolfei

Abstract

Microbial syntrophy is a vital metabolic interaction necessary for the complete oxidation of organic biomass to methane in all-anaerobic ecosystems. However, this process is thermodynamically constrained and represents an ecosystem-level metabolic bottleneck. To gain insight into the physiology of this process, a shotgun proteomics approach was used to quantify the protein landscape of the model syntrophic metabolizer, Syntrophomonas wolfei, grown axenically and syntrophically with Methanospirillum hungatei. Remarkably, the abundance of most proteins as represented by normalized spectral abundance factor (NSAF) value changed very little between the pure and coculture growth conditions. Among the most abundant proteins detected were GroEL and GroES chaperonins, a small heat shock protein, and proteins involved in electron transfer, beta-oxidation, and ATP synthesis. Several putative energy conservation enzyme systems that utilize NADH and ferredoxin were present. The abundance of an EtfAB2 and the membrane-bound iron-sulfur oxidoreductase (Swol_0698 gene product) delineated a potential conduit for electron transfer between acyl-CoA dehydrogenases and membrane redox carriers. Proteins detected only when S. wolfei was grown with M. hungatei included a zinc-dependent dehydrogenase with a GroES domain, whose gene is present in genomes in many organisms capable of syntrophy, and transcriptional regulators responsive to environmental stimuli or the physiological status ofmore » the cell. The proteomic analysis revealed an emphasis on macromolecular stability and energy metabolism by S. wolfei and presence of regulatory mechanisms responsive to external stimuli and cellular physiological status.« less

Authors:
 [1];  [1];  [2];  [3];  [4];  [4];  [1]
  1. Univ. of Oklahoma, Norman, OK (United States). Dept. of Botany and Microbiology
  2. Univ. of Michigan, Ann Arbor, MI (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
  4. Univ. of California, Los Angeles, CA (United States)
Publication Date:
Research Org.:
Univ. of California, Los Angeles, CA (United States); Univ. of Oklahoma, Norman, OK (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; USDOE Office of Science (SC), Biological and Environmental Research (BER)
Contributing Org.:
Univ. of Oklahoma, Norman, OK (United States); Univ. of California, Los Angeles, CA (United States)
OSTI Identifier:
1254004
Alternate Identifier(s):
OSTI ID: 1286726
Grant/Contract Number:  
FC02-02ER63421; FG03-86ER13498; FG02-96ER20214; AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; syntrophy; Syntrophomonas wolfei; interspecies electron transfer; reverse electron transfer; hydrogen; methanogenesis

Citation Formats

Sieber, Jessica R., Crable, Bryan R., Sheik, Cody S., Hurst, Gregory B., Rohlin, Lars, Gunsalus, Robert P., and McInerney, Michael J. Proteomic analysis reveals metabolic and regulatory systems involved in the syntrophic and axenic lifestyle of Syntrophomonas wolfei. United States: N. p., 2015. Web. doi:10.3389/fmicb.2015.00115.
Sieber, Jessica R., Crable, Bryan R., Sheik, Cody S., Hurst, Gregory B., Rohlin, Lars, Gunsalus, Robert P., & McInerney, Michael J. Proteomic analysis reveals metabolic and regulatory systems involved in the syntrophic and axenic lifestyle of Syntrophomonas wolfei. United States. https://doi.org/10.3389/fmicb.2015.00115
Sieber, Jessica R., Crable, Bryan R., Sheik, Cody S., Hurst, Gregory B., Rohlin, Lars, Gunsalus, Robert P., and McInerney, Michael J. Wed . "Proteomic analysis reveals metabolic and regulatory systems involved in the syntrophic and axenic lifestyle of Syntrophomonas wolfei". United States. https://doi.org/10.3389/fmicb.2015.00115. https://www.osti.gov/servlets/purl/1254004.
@article{osti_1254004,
title = {Proteomic analysis reveals metabolic and regulatory systems involved in the syntrophic and axenic lifestyle of Syntrophomonas wolfei},
author = {Sieber, Jessica R. and Crable, Bryan R. and Sheik, Cody S. and Hurst, Gregory B. and Rohlin, Lars and Gunsalus, Robert P. and McInerney, Michael J.},
abstractNote = {Microbial syntrophy is a vital metabolic interaction necessary for the complete oxidation of organic biomass to methane in all-anaerobic ecosystems. However, this process is thermodynamically constrained and represents an ecosystem-level metabolic bottleneck. To gain insight into the physiology of this process, a shotgun proteomics approach was used to quantify the protein landscape of the model syntrophic metabolizer, Syntrophomonas wolfei, grown axenically and syntrophically with Methanospirillum hungatei. Remarkably, the abundance of most proteins as represented by normalized spectral abundance factor (NSAF) value changed very little between the pure and coculture growth conditions. Among the most abundant proteins detected were GroEL and GroES chaperonins, a small heat shock protein, and proteins involved in electron transfer, beta-oxidation, and ATP synthesis. Several putative energy conservation enzyme systems that utilize NADH and ferredoxin were present. The abundance of an EtfAB2 and the membrane-bound iron-sulfur oxidoreductase (Swol_0698 gene product) delineated a potential conduit for electron transfer between acyl-CoA dehydrogenases and membrane redox carriers. Proteins detected only when S. wolfei was grown with M. hungatei included a zinc-dependent dehydrogenase with a GroES domain, whose gene is present in genomes in many organisms capable of syntrophy, and transcriptional regulators responsive to environmental stimuli or the physiological status of the cell. The proteomic analysis revealed an emphasis on macromolecular stability and energy metabolism by S. wolfei and presence of regulatory mechanisms responsive to external stimuli and cellular physiological status.},
doi = {10.3389/fmicb.2015.00115},
journal = {Frontiers in Microbiology},
number = ,
volume = 6,
place = {United States},
year = {Wed Feb 11 00:00:00 EST 2015},
month = {Wed Feb 11 00:00:00 EST 2015}
}

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Cited by: 37 works
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Figures / Tables:

FIGURE 1 FIGURE 1: Non-metric multidimensional scaling of the S. wolfei protein profiles obtained from each technical replicate for each duplicate culture grown under the three conditions. Symbols: green circle, S. wolfei pure culture on crotonate; pink circles, S. wolfei-M. hungatei coculture on crotonate; blue circles, S. wolfei-M. hungatei coculture on butyrate.

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Works referencing / citing this record:

Novel syntrophic bacteria in full-scale anaerobic digesters revealed by genome-centric metatranscriptomics
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