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

Kimberly L. James, Johannes W. Kung, Bryan R. Crable, Housna Mouttaki, Jessica R. Sieber, Hong H. Nguyen, Yanan Yang, Yongming Xie, Jonathan Erde, Neil Q. Wofford, Elizabeth A. Karr, Joseph A. Loo, Rachel R. Ogorzalek Loo, Robert P. Gunsalus, Michael J. McInerney

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Abstract

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 catalyses 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 13 C-atoms from 1-[ 13 C]-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. Syntrophus aciditrophicus, thus, uses a core set of enzymes that operates close to thermodynamic equilibrium to conserve energy in a novel and highly efficient manner.

Original languageEnglish (US)
Pages (from-to)1833-1846
Number of pages14
JournalEnvironmental microbiology
Volume21
Issue number5
DOIs
StatePublished - May 2019

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James, K. L., Kung, J. W., Crable, B. R., Mouttaki, H., Sieber, J. R., Nguyen, H. H., Yang, Y., Xie, Y., Erde, J., Wofford, N. Q., Karr, E. A., Loo, J. A., Ogorzalek Loo, R. R., Gunsalus, R. P., & McInerney, M. J. (2019). Syntrophus aciditrophicus uses the same enzymes in a reversible manner to degrade and synthesize aromatic and alicyclic acids. Environmental microbiology, 21(5), 1833-1846. https://doi.org/10.1111/1462-2920.14601