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

Abstract

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.

Authors:
 [1];  [1];  [1];  [1];  [1];  [2];  [2];  [2];  [2];  [1];  [3];  [2];  [2];  [2];  [1]
  1. Univ. of Oklahoma, Norman, OK (United States)
  2. Univ. of California, Los Angeles, CA (United States)
  3. Univ. of Oklahoma, Norman, OK (United States). Price Family Foundation Inst. of Structural Biology
Publication Date:
Research Org.:
Univ. of Oklahoma, Norman, OK (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH)
OSTI Identifier:
1604774
Alternate Identifier(s):
OSTI ID: 1510094
Grant/Contract Number:  
FG02-96ER20214; FC02‐02ER63421; R01GM085402; R01GM104610; FG02‐96ER20214
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Volume: 21; Journal Issue: 5; Journal ID: ISSN 1462-2912
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; syntrophy; methanogenesis; bioenergy

Citation Formats

James, Kimberly L., Kung, Johannes W., Crable, Bryan R., Mouttaki, Housna, Sieber, Jessica R., Nguyen, Hong H., Yang, Yanan, Xie, Yongming, Erde, Jonathan, Wofford, Neil Q., Karr, Elizabeth A., Loo, Joseph A., Ogorzalek Loo, Rachel R., Gunsalus, Robert P., and McInerney, Michael J. Syntrophus aciditrophicus uses the same enzymes in a reversible manner to degrade and synthesize aromatic and alicyclic acids. United States: N. p., 2019. Web. doi:10.1111/1462-2920.14601.
James, Kimberly L., Kung, Johannes W., Crable, Bryan R., Mouttaki, Housna, Sieber, Jessica R., Nguyen, Hong H., Yang, Yanan, Xie, Yongming, Erde, Jonathan, Wofford, Neil Q., Karr, Elizabeth A., Loo, Joseph A., Ogorzalek Loo, Rachel R., Gunsalus, Robert P., & McInerney, Michael J. Syntrophus aciditrophicus uses the same enzymes in a reversible manner to degrade and synthesize aromatic and alicyclic acids. United States. https://doi.org/10.1111/1462-2920.14601
James, Kimberly L., Kung, Johannes W., Crable, Bryan R., Mouttaki, Housna, Sieber, Jessica R., Nguyen, Hong H., Yang, Yanan, Xie, Yongming, Erde, Jonathan, Wofford, Neil Q., Karr, Elizabeth A., Loo, Joseph A., Ogorzalek Loo, Rachel R., Gunsalus, Robert P., and McInerney, Michael J. Wed . "Syntrophus aciditrophicus uses the same enzymes in a reversible manner to degrade and synthesize aromatic and alicyclic acids". United States. https://doi.org/10.1111/1462-2920.14601. https://www.osti.gov/servlets/purl/1604774.
@article{osti_1604774,
title = {Syntrophus aciditrophicus uses the same enzymes in a reversible manner to degrade and synthesize aromatic and alicyclic acids},
author = {James, Kimberly L. and Kung, Johannes W. and Crable, Bryan R. and Mouttaki, Housna and Sieber, Jessica R. and Nguyen, Hong H. and Yang, Yanan and Xie, Yongming and Erde, Jonathan and Wofford, Neil Q. and Karr, Elizabeth A. and Loo, Joseph A. and Ogorzalek Loo, Rachel R. and Gunsalus, Robert P. and McInerney, Michael J.},
abstractNote = {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.},
doi = {10.1111/1462-2920.14601},
url = {https://www.osti.gov/biblio/1604774}, journal = {Environmental Microbiology},
issn = {1462-2912},
number = 5,
volume = 21,
place = {United States},
year = {2019},
month = {3}
}

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