Skip to main content
OSTI.GOVU.S. Department of Energy Office of Scientific and Technical Information
U.S. Department of Energy
Office of Scientific and Technical Information
 

Syntrophus aciditrophicus uses the same enzymes in a reversible manner to degrade and synthesize aromatic and alicyclic acids

Journal Article · · Environmental Microbiology
 [1];  [2];  [2];  [2];  [2];  [3];  [3];  [3];  [3];  [2];  [4];  [3];  [3];  [3];  [2]
  1. Univ. of Oklahoma, Norman, OK (United States); University of Oklahoma
  2. Univ. of Oklahoma, Norman, OK (United States)
  3. Univ. of California, Los Angeles, CA (United States)
  4. Univ. of Oklahoma, Norman, OK (United States). Price Family Foundation Inst. of Structural Biology
+ Show Author Affiliations

We report that syntrophy is essential for the efficient conversion of organic carbon to methane in natural and constructed environments, but little is known about the enzymes involved in syntrophic carbon and electron flow. Syntrophus aciditrophicus strain SB syntrophically degrades benzoate and cyclohexane-1-carboxylate and catalyzes the novel synthesis of benzoate and cyclohexane-1-carboxylate from crotonate. We used proteomic, biochemical, and metabolomic approaches to determine what enzymes are used for fatty, aromatic, and alicyclic acid degradation versus for benzoate and cyclohexane-1-carboxylate synthesis. Enzymes involved in the metabolism of cyclohex-1,5-diene carboxyl-CoA to acetyl-CoA were in high abundance in S. aciditrophicus cells grown in pure culture on crotonate and in coculture with Methanospirillum hungatei on crotonate, benzoate or cyclohexane-1-carboxylate. Incorporation of 13C-atoms from 1-[13C]-acetate into crotonate, benzoate, and cyclohexane-1-carboxylate during growth on these different substrates showed that the pathways are reversible. A protein conduit for syntrophic reverse electron transfer from acyl-CoA intermediates to formate was detected. Ligases and membrane-bound pyrophosphatases make pyrophosphate needed for the synthesis of ATP by an acetyl-CoA synthetase. S. aciditrophicus, thus, uses a core set of enzymes that operates close to thermodynamic equilibrium to conserve energy in a novel and highly efficient manner.

Research Organization:
Univ. of Oklahoma, Norman, OK (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Institutes of Health (NIH)
Grant/Contract Number:
FG02-96ER20214; FC02-02ER63421
OSTI ID:
1604774
Alternate ID(s):
OSTI ID: 1510094
Journal Information:
Environmental Microbiology, Journal Name: Environmental Microbiology Journal Issue: 5 Vol. 21; ISSN 1462-2912
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (52)

Environmental Constraints that Limit Methanogenesis book January 2018
Purification and characterization of benzoyl-CoA ligase from a syntrophic, benzoate-degrading, anaerobic mixed culture journal September 1992
The biotin-dependent sodium ion pump glutaconyl-CoA decarboxylase from Fusobacterium nucleatum (subsp. nucleatum): Comparison with the glutaconyl-CoA decarboxylases from gram-positive bacteria journal September 1990
Carbon monoxide pathway enzyme activities in a thermophilic anaerobic bacterium grown acetogenically and in a syntrophic acetate-oxidizing coculture journal October 1988
Syntrophus aciditrophicus sp. nov., a new anaerobic bacterium that degrades fatty acids and benzoate in syntrophic association with hydrogen-using microorganisms journal January 1999
Energetics and biochemistry of fermentative benzoate degradation by Syntrophus gentianae journal April 1999
Biochemical characterization of purified OmcS, a c-type cytochrome required for insoluble Fe(III) reduction in Geobacter sulfurreducens journal April 2011
Syntrophy in anaerobic global carbon cycles journal December 2009
Quantitative Proteomic Analysis by Accurate Mass Retention Time Pairs journal April 2005
Carboxylation of pyruvate and acetyl coenzyme A by reversal of the sodium pumps oxaloacetate decarboxylase and methylmalonyl-CoA decarboxylase journal October 1984
Metabolites Detected during Biodegradation of 13 C 6 -Benzene in Nitrate-Reducing and Methanogenic Enrichment Cultures journal September 2005
Quantitative Proteomic Analysis of Drug-Induced Changes in Mycobacteria journal January 2006
Enhanced FASP (eFASP) to Increase Proteome Coverage and Sample Recovery for Quantitative Proteomic Experiments journal March 2014
Anaerobic microbial metabolism can proceed close to thermodynamic limits journal January 2002
Membrane-bound proton-translocating pyrophosphatase of Syntrophus gentianae, a syntrophically benzoate-degrading fermenting bacterium journal September 1998
6-Hydroxycyclohex-1-ene-1-carbonyl-CoA dehydrogenase and 6-oxocyclohex-1-ene-1-carbonyl-CoA hydrolase, enzymes of the benzoyl-CoA pathway of anaerobic aromatic metabolism in the denitrifying bacterium Thauera aromatica journal July 1999
Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms journal July 2006
The genome of Syntrophus aciditrophicus: Life at the thermodynamic limit of microbial growth journal April 2007
Identification and characterization of the tungsten-containing class of benzoyl-coenzyme A reductases journal October 2009
Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1 journal October 2010
Bacterial Na+-translocating ferredoxin:NAD+ oxidoreductase journal October 2010
Microbial interspecies electron transfer via electric currents through conductive minerals journal June 2012
A Na + -translocating Pyrophosphatase in the Acetogenic Bacterium Acetobacterium woodii journal December 2010
Absolute Quantification of Proteins by LCMS E : A Virtue of Parallel ms Acquisition journal October 2005
The importance of hydrogen and formate transfer for syntrophic fatty, aromatic and alicyclic metabolism: Importance of interspecies hydrogen and formate transfer journal October 2013
Gene clusters involved in anaerobic benzoate degradation of Geobacter metallireducens: Benzoate metabolism in G. metallireducens journal October 2005
6-Oxocyclohex-1-ene-1-carbonyl-coenzyme A hydrolases from obligately anaerobic bacteria: characterization and identification of its gene as a functional marker for aromatic compounds degrading anaerobes: Gene probe for ring-opening hydrolases journal February 2008
Use of benzoate as an electron acceptor by Syntrophus aciditrophicus grown in pure culture with crotonate journal December 2008
Occurrence, genes and expression of the W/Se-containing class II benzoyl-coenzyme A reductases in anaerobic bacteria: Distribution of class II benzoyl-CoA reductases journal November 2010
The Plate Debate: Cultivable communities have no utility in contemporary environmental microbial ecology: The plate debate journal June 2007
Energetics of syntrophic fatty acid oxidation journal October 1994
Anaerobic metabolism of aromatic compounds via the benzoyl-CoA pathway journal December 1998
Direct Exchange of Electrons Within Aggregates of an Evolved Syntrophic Coculture of Anaerobic Bacteria journal December 2010
Alignment of the c-Type Cytochrome OmcS along Pili of Geobacter sulfurreducens journal April 2010
Metabolism of Hydroxylated and Fluorinated Benzoates by Syntrophus aciditrophicus and Detection of a Fluorodiene Metabolite journal December 2008
Production of Glutaconic Acid in a Recombinant Escherichia coli Strain journal October 2010
Cyclohexane Carboxylate and Benzoate Formation from Crotonate in Syntrophus aciditrophicus journal December 2006
Benzoate Fermentation by the Anaerobic Bacterium Syntrophus aciditrophicus in the Absence of Hydrogen-Using Microorganisms journal December 2001
Metabolism of Benzoate, Cyclohex-1-ene Carboxylate, and Cyclohexane Carboxylate by "Syntrophus aciditrophicus" Strain SB in Syntrophic Association with H2-Using Microorganisms journal April 2001
Cyclohexanecarboxyl-Coenzyme A (CoA) and Cyclohex-1-ene-1-Carboxyl-CoA Dehydrogenases, Two Enzymes Involved in the Fermentation of Benzoate and Crotonate in Syntrophus aciditrophicus journal May 2013
Cyclohexa-1,5-Diene-1-Carbonyl-Coenzyme A (CoA) Hydratases of Geobacter metallireducens and Syntrophus aciditrophicus: Evidence for a Common Benzoyl-CoA Degradation Pathway in Facultative and Strict Anaerobes journal November 2006
Enzymes Involved in a Novel Anaerobic Cyclohexane Carboxylic Acid Degradation Pathway journal August 2014
2-Hydroxycyclohexanecarboxyl Coenzyme A Dehydrogenase, an Enzyme Characteristic of the Anaerobic Benzoate Degradation Pathway Used by Rhodopseudomonas palustris journal May 2000
Benzoate-Coenzyme A Ligase from Thauera aromatica: an Enzyme Acting in Anaerobic and Aerobic Pathways journal August 2003
Operation of the CO Dehydrogenase/Acetyl Coenzyme A Pathway in both Acetate Oxidation and Acetate Formation by the Syntrophically Acetate-Oxidizing Bacterium Thermacetogenium phaeum journal May 2005
Pyrophosphate-Dependent ATP Formation from Acetyl Coenzyme A in Syntrophus aciditrophicus , a New Twist on ATP Formation journal August 2016
Genomic Insights into Syntrophy: The Paradigm for Anaerobic Metabolic Cooperation journal October 2012
Physiology, Ecology, Phylogeny, and Genomics of Microorganisms Capable of Syntrophic Metabolism journal March 2008
Anaerobic Metabolism of Aromatic Compounds journal March 2008
A Proteomic View at the Biochemistry of Syntrophic Butyrate Oxidation in Syntrophomonas wolfei journal February 2013
Proteomic analysis reveals metabolic and regulatory systems involved in the syntrophic and axenic lifestyle of Syntrophomonas wolfei journal February 2015
Membrane Complexes of Syntrophomonas wolfei Involved in Syntrophic Butyrate Degradation and Hydrogen Formation journal November 2016

Similar Records

Two Pathways for Glutamate Biosynthesis in the Syntrophic Bacterium Syntrophus aciditrophicus
Journal Article · Fri Oct 02 00:00:00 EDT 2015 · Applied and Environmental Microbiology · OSTI ID:1470219

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
bioenergy
methanogenesis
syntrophy