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Membrane Complexes of Syntrophomonas wolfei Involved in Syntrophic Butyrate Degradation and Hydrogen Formation

Journal Article · · Frontiers in Microbiology
 [1];  [1];  [2];  [2];  [3];  [4];  [4];  [1]
  1. Univ. of Oklahoma, Norman, OK (United States). Dept. of Microbiology and Plant Biology
  2. Univ. of California, Berkeley, CA (United States). Dept. of Civil and Environmental Engineering
  3. Univ. of California, Los Angeles, CA (United States). Dept. of Microbiology, Immunology, and Molecular Genetics
  4. Univ. of California, Los Angeles, CA (United States). Dept. of Biological Chemistry
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Syntrophic butyrate metabolism involves the thermodynamically unfavorable production of hydrogen and/or formate from the high potential electron donor, butyryl-CoA. Such redox reactions can occur only with energy input by a process called reverse electron transfer. Previous studies have demonstrated that hydrogen production from butyrate requires the presence of a proton gradient, but the biochemical machinery involved has not been clearly elucidated. In this study, the gene and enzyme systems involved in reverse electron transfer by Syntrophomonas wolfei were investigated using proteomic and gene expression approaches. S. wolfei was grown in co-culture with Methanospirillum hungatei or Dehalococcoides mccartyi under conditions requiring reverse electron transfer and compared to both axenic S. wolfei cultures and co-cultures grown in conditions that do not require reverse electron transfer. Blue native gel analysis of membranes solubilized from syntrophically grown cells revealed the presence of a membrane-bound hydrogenase, Hyd2, which exhibited hydrogenase activity during in gel assays. Bands containing a putative iron-sulfur (FeS) oxidoreductase were detected in membranes of crotonate-grown and butyrate grown S. wolfei cells. The genes for the corresponding hydrogenase subunits, hyd2ABC, were differentially expressed at higher levels during syntrophic butyrate growth when compared to growth on crotonate. The expression of the FeS oxidoreductase gene increased when S. wolfei was grown with M. hungatei. Additional membrane-associated proteins detected included FoF1 ATP synthase subunits and several membrane transporters that may aid syntrophic growth. Furthermore, syntrophic butyrate metabolism can proceed exclusively by interspecies hydrogen transfer, as demonstrated by growth with D. mccartyi, which is unable to use formate. These results argue for the importance of Hyd2 and FeS oxidoreductase in reverse electron transfer during syntrophic butyrate degradation.
Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of Oklahoma, Norman, OK (United States)
Sponsoring Organization:
National Inst. of Health (NIH) (United States); National Science Foundation (NSF) (United States); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division; USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Grant/Contract Number:
AC02-05CH11231; FC02-02ER63421; FG02-96ER20214; FG03-86ER13498
OSTI ID:
1480747
Alternate ID(s):
OSTI ID: 1604789
Journal Information:
Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 7; ISSN 1664-302X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English

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Cited By (5)

Complete Genome Sequence of “Candidatus Syntrophocurvum alkaliphilum” Strain B(2M), Obtained from the Metagenome of a Salt-Tolerant Alkaliphilic Anaerobic Syntrophic Butyrate-Degrading Consortium journal February 2020
Elucidating Syntrophic Butyrate-Degrading Populations in Anaerobic Digesters Using Stable-Isotope-Informed Genome-Resolved Metagenomics journal August 2019
Novel syntrophic bacteria in full-scale anaerobic digesters revealed by genome-centric metatranscriptomics journal January 2020
Hydrogen or formate: Alternative key players in methanogenic degradation: Hydrogen/formate as interspecies electron carriers journal March 2017
Syntrophic acetate oxidation replaces acetoclastic methanogenesis during thermophilic digestion of biowaste journal July 2020

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
biohydrogen
fatty acids
hydrogenase
methanogenesis
syntrophy
syntrophy
methanogenesis
biohydrogen
hydrogenase
fatty acids