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

Journal Article · · Frontiers in Microbiology
 [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)

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.

Research Organization:
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 Organization:
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 Organization:
Univ. of Oklahoma, Norman, OK (United States); Univ. of California, Los Angeles, CA (United States)
Grant/Contract Number:
FC02-02ER63421; FG03-86ER13498; FG02-96ER20214; AC05-00OR22725
OSTI ID:
1254004
Alternate ID(s):
OSTI ID: 1286726
Journal Information:
Frontiers in Microbiology, Vol. 6; ISSN 1664-302X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 37 works
Citation information provided by
Web of Science

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Cited By (12)

Label-Free Proteomics of a Defined, Binary Co-culture Reveals Diversity of Competitive Responses Between Members of a Model Soil Microbial System journal October 2017
Novel syntrophic bacteria in full-scale anaerobic digesters revealed by genome-centric metatranscriptomics journal January 2020
Methanogenic paraffin degradation proceeds via alkane addition to fumarate by ‘Smithella’ spp. mediated by a syntrophic coupling with hydrogenotrophic methanogens : Methanogenic paraffin-utilizing consortium journal June 2016
Comparative proteome analysis of propionate degradation by Syntrophobacter fumaroxidans in pure culture and in coculture with methanogens: Proteome analysis of Syntrophobacter fumaroxidans journal April 2018
Hydrogen or formate: Alternative key players in methanogenic degradation: Hydrogen/formate as interspecies electron carriers journal March 2017
Elucidating Syntrophic Butyrate-Degrading Populations in Anaerobic Digesters Using Stable-Isotope-Informed Genome-Resolved Metagenomics journal August 2019
Syntrophic acetate oxidation replaces acetoclastic methanogenesis during thermophilic digestion of biowaste journal July 2020
Membrane Complexes of Syntrophomonas wolfei Involved in Syntrophic Butyrate Degradation and Hydrogen Formation journal November 2016
Flavin-Based Electron Bifurcation, Ferredoxin, Flavodoxin, and Anaerobic Respiration With Protons (Ech) or NAD+ (Rnf) as Electron Acceptors: A Historical Review journal March 2018
Concerted Metabolic Shifts Give New Insights Into the Syntrophic Mechanism Between Propionate-Fermenting Pelotomaculum thermopropionicum and Hydrogenotrophic Methanocella conradii journal July 2018
Comparative Genomics of Syntrophic Branched-Chain Fatty Acid Degrading Bacteria journal January 2016
Metagenomic Characterization of Candidatus Smithella cisternae Strain M82_1, a Syntrophic Alkane-Degrading Bacteria, Enriched from the Shengli Oil Field journal January 2017

Figures / Tables (4)