Succinyl-CoA:acetate CoA-transferase functioning in the oxidative tricarboxylic acid cycle in Desulfurella acetivorans

Desulfurella acetivorans is a strictly anaerobic sulfur-reducing deltaproteobacterium that possesses a very dynamic metabolism with the ability to revert the citrate synthase version of the tricarboxylic acid (TCA) cycle for autotrophic growth (reversed oxidative TCA cycle) or to use it for acetate...

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Main Authors: Eugenio Pettinato, Pauline Böhnert, Ivan A. Berg
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.1080142/full
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author Eugenio Pettinato
Pauline Böhnert
Ivan A. Berg
author_facet Eugenio Pettinato
Pauline Böhnert
Ivan A. Berg
author_sort Eugenio Pettinato
collection DOAJ
description Desulfurella acetivorans is a strictly anaerobic sulfur-reducing deltaproteobacterium that possesses a very dynamic metabolism with the ability to revert the citrate synthase version of the tricarboxylic acid (TCA) cycle for autotrophic growth (reversed oxidative TCA cycle) or to use it for acetate oxidation (oxidative TCA cycle). Here we show that for heterotrophic growth on acetate D. acetivorans uses a modified oxidative TCA cycle that was first discovered in acetate-oxidizing sulfate reducers in which a succinyl-CoA:acetate CoA-transferase catalyzes the conversion of succinyl-CoA to succinate, coupled with the activation of acetate to acetyl-CoA. We identified the corresponding enzyme in this bacterium as the AHF96498 gene product and characterized it biochemically. Our phylogenetic analysis of CoA-transferases revealed that the CoA-transferase variant of the oxidative TCA cycle has convergently evolved several times in different bacteria. Its functioning is especially important for anaerobes, as it helps to increase the energetic efficiency of the pathway by using one enzyme for two enzymatic reactions and by allowing to spend just one ATP equivalent for acetate activation.
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spelling doaj.art-3b22ff8f3d6344ab8ccec3507fa86baa2022-12-22T02:51:19ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-12-011310.3389/fmicb.2022.10801421080142Succinyl-CoA:acetate CoA-transferase functioning in the oxidative tricarboxylic acid cycle in Desulfurella acetivoransEugenio PettinatoPauline BöhnertIvan A. BergDesulfurella acetivorans is a strictly anaerobic sulfur-reducing deltaproteobacterium that possesses a very dynamic metabolism with the ability to revert the citrate synthase version of the tricarboxylic acid (TCA) cycle for autotrophic growth (reversed oxidative TCA cycle) or to use it for acetate oxidation (oxidative TCA cycle). Here we show that for heterotrophic growth on acetate D. acetivorans uses a modified oxidative TCA cycle that was first discovered in acetate-oxidizing sulfate reducers in which a succinyl-CoA:acetate CoA-transferase catalyzes the conversion of succinyl-CoA to succinate, coupled with the activation of acetate to acetyl-CoA. We identified the corresponding enzyme in this bacterium as the AHF96498 gene product and characterized it biochemically. Our phylogenetic analysis of CoA-transferases revealed that the CoA-transferase variant of the oxidative TCA cycle has convergently evolved several times in different bacteria. Its functioning is especially important for anaerobes, as it helps to increase the energetic efficiency of the pathway by using one enzyme for two enzymatic reactions and by allowing to spend just one ATP equivalent for acetate activation.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1080142/fullCoA-transferasestricarboxylic acid cycle (TCA cycle)acetate oxidationDesulfurellasuccinyl-CoA synthetaseacetyl-CoA synthetase
spellingShingle Eugenio Pettinato
Pauline Böhnert
Ivan A. Berg
Succinyl-CoA:acetate CoA-transferase functioning in the oxidative tricarboxylic acid cycle in Desulfurella acetivorans
Frontiers in Microbiology
CoA-transferases
tricarboxylic acid cycle (TCA cycle)
acetate oxidation
Desulfurella
succinyl-CoA synthetase
acetyl-CoA synthetase
title Succinyl-CoA:acetate CoA-transferase functioning in the oxidative tricarboxylic acid cycle in Desulfurella acetivorans
title_full Succinyl-CoA:acetate CoA-transferase functioning in the oxidative tricarboxylic acid cycle in Desulfurella acetivorans
title_fullStr Succinyl-CoA:acetate CoA-transferase functioning in the oxidative tricarboxylic acid cycle in Desulfurella acetivorans
title_full_unstemmed Succinyl-CoA:acetate CoA-transferase functioning in the oxidative tricarboxylic acid cycle in Desulfurella acetivorans
title_short Succinyl-CoA:acetate CoA-transferase functioning in the oxidative tricarboxylic acid cycle in Desulfurella acetivorans
title_sort succinyl coa acetate coa transferase functioning in the oxidative tricarboxylic acid cycle in desulfurella acetivorans
topic CoA-transferases
tricarboxylic acid cycle (TCA cycle)
acetate oxidation
Desulfurella
succinyl-CoA synthetase
acetyl-CoA synthetase
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.1080142/full
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