Propionate metabolism in Desulfurella acetivorans
Desulfurella acetivorans is a strictly anaerobic sulfur-reducing deltaproteobacterium that can grow heterotrophically by oxidation of acetate or autotrophically with molecular hydrogen. Here we show that D. acetivorans possesses a putative operon encoding enzymes of the methylcitrate cycle of propio...
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Frontiers Media S.A.
2025-02-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1545849/full |
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| author | Eugenio Pettinato Thomas M. Steiner Eric A. Cassens Thomas Geisberger Christian Seitz Simone König Wolfgang Eisenreich Ivan A. Berg |
| author_facet | Eugenio Pettinato Thomas M. Steiner Eric A. Cassens Thomas Geisberger Christian Seitz Simone König Wolfgang Eisenreich Ivan A. Berg |
| author_sort | Eugenio Pettinato |
| collection | DOAJ |
| description | Desulfurella acetivorans is a strictly anaerobic sulfur-reducing deltaproteobacterium that can grow heterotrophically by oxidation of acetate or autotrophically with molecular hydrogen. Here we show that D. acetivorans possesses a putative operon encoding enzymes of the methylcitrate cycle of propionate oxidation and demonstrate that this bacterium is capable of propionate growth. However, activities of the methylcitrate cycle enzymes could not be detected in extracts of propionate-grown cells, and experiments with [U-13C3]propionate and comparative proteomic analysis of acetate- and propionate-grown cells suggested that the methylcitrate cycle is not active during propionate growth. Instead, propionyl-CoA assimilation proceeds via its carboxylation to methylmalonyl-CoA, which is further converted to succinyl-CoA. The latter is directed to the tricarboxylic acid (TCA) cycle, where it is converted to oxaloacetate and condenses with acetyl-CoA (produced by decarboxylation of another oxaloacetate molecule) to form citrate, which is oxidized in the TCA cycle. These results highlight the uncertainty of genomic predictions in the analysis of microbial metabolic pathways and the need for their experimental confirmation. |
| format | Article |
| id | doaj-art-1d54145cda244836baaff45fc2ac9820 |
| institution | Kabale University |
| issn | 1664-302X |
| language | English |
| publishDate | 2025-02-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj-art-1d54145cda244836baaff45fc2ac98202025-02-12T07:26:21ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-02-011610.3389/fmicb.2025.15458491545849Propionate metabolism in Desulfurella acetivoransEugenio Pettinato0Thomas M. Steiner1Eric A. Cassens2Thomas Geisberger3Christian Seitz4Simone König5Wolfgang Eisenreich6Ivan A. Berg7Institute for Molecular Microbiology and Biotechnology, University of Münster, Münster, GermanyBavarian NMR Center–Structural Membrane Biochemistry, Department of Chemistry, Technische Universität München, Garching, GermanyInstitute for Molecular Microbiology and Biotechnology, University of Münster, Münster, GermanyBavarian NMR Center–Structural Membrane Biochemistry, Department of Chemistry, Technische Universität München, Garching, GermanyBavarian NMR Center–Structural Membrane Biochemistry, Department of Chemistry, Technische Universität München, Garching, GermanyCore Unit Proteomics, Interdisciplinary Center for Clinical Research, Faculty of Medical, University of Münster, Münster, GermanyBavarian NMR Center–Structural Membrane Biochemistry, Department of Chemistry, Technische Universität München, Garching, GermanyInstitute for Molecular Microbiology and Biotechnology, University of Münster, Münster, GermanyDesulfurella acetivorans is a strictly anaerobic sulfur-reducing deltaproteobacterium that can grow heterotrophically by oxidation of acetate or autotrophically with molecular hydrogen. Here we show that D. acetivorans possesses a putative operon encoding enzymes of the methylcitrate cycle of propionate oxidation and demonstrate that this bacterium is capable of propionate growth. However, activities of the methylcitrate cycle enzymes could not be detected in extracts of propionate-grown cells, and experiments with [U-13C3]propionate and comparative proteomic analysis of acetate- and propionate-grown cells suggested that the methylcitrate cycle is not active during propionate growth. Instead, propionyl-CoA assimilation proceeds via its carboxylation to methylmalonyl-CoA, which is further converted to succinyl-CoA. The latter is directed to the tricarboxylic acid (TCA) cycle, where it is converted to oxaloacetate and condenses with acetyl-CoA (produced by decarboxylation of another oxaloacetate molecule) to form citrate, which is oxidized in the TCA cycle. These results highlight the uncertainty of genomic predictions in the analysis of microbial metabolic pathways and the need for their experimental confirmation.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1545849/fullpropionate assimilationtricarboxylic acid cycleDesulfurella acetivoransmethylcitrate cyclemethylmalonyl-CoA pathway |
| spellingShingle | Eugenio Pettinato Thomas M. Steiner Eric A. Cassens Thomas Geisberger Christian Seitz Simone König Wolfgang Eisenreich Ivan A. Berg Propionate metabolism in Desulfurella acetivorans Frontiers in Microbiology propionate assimilation tricarboxylic acid cycle Desulfurella acetivorans methylcitrate cycle methylmalonyl-CoA pathway |
| title | Propionate metabolism in Desulfurella acetivorans |
| title_full | Propionate metabolism in Desulfurella acetivorans |
| title_fullStr | Propionate metabolism in Desulfurella acetivorans |
| title_full_unstemmed | Propionate metabolism in Desulfurella acetivorans |
| title_short | Propionate metabolism in Desulfurella acetivorans |
| title_sort | propionate metabolism in desulfurella acetivorans |
| topic | propionate assimilation tricarboxylic acid cycle Desulfurella acetivorans methylcitrate cycle methylmalonyl-CoA pathway |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1545849/full |
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