Exploring the diversity of pathways of autotrophic carbon assimilation in thermophilic prokaryotes

• Applicant: Professor Dr. Ivan A. Berg
• Subject Area: Metabolism, Biochemistry and Genetics of Microorganisms ; Microbial Ecology and Applied Microbiology
• Term: from 2020 to 2023
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 429812134

• Final Report Year: 2025

Final Report Abstract

In this project, we screened different thermophilic autotrophs for the presence of novel autotrophic pathways or variants thereof. The strains studied, belonging to the Sulfolobales and Thermoproteales, used the 3-hydroxypropionate/4-hydroxybutyrate cycle and the dicarboxylate/4-hydroxybutyrate cycle, respectively, confirming previous experimental data. However, we found evidence for the functioning of the dicarboxylate/4-hydroxybutyrate cycle in a thermophilic sulfur-reducing bacterium Desulfurella propionica during autotrophic growth and during growth on propionate. Our data suggest that propionate assimilation in D. propionica starts with propionyl-CoA carboxylation and isomerisation to succinyl-CoA, which is further reduced via 4-hydroxybutyrate to two acetyl-CoA molecules. In contrast, propionate assimilation in a closely related species D. acetivorans (>99% of 16S rRNA gene identity) does not involve enzymes of the 4-hydroxybutyrate pathway, and succinyl-CoA formed in the initial phase of propionate metabolism is decarboxylated twice to acetyl-CoA. Interestingly, D. acetivorans possesses the methylcitrate cycle operon in its genome, but the corresponding genes are not expressed and do not participate in propionate utilisation. In this work, we have also identified and characterised the succinyl-CoA:acetate CoA transferase involved in the tricarboxylic acid cycle in D. acetivorans. Our study demonstrates the extreme plasticity of Desulfurella metabolism, with the possibility of substitution of even central metabolic processes in the closely related species.

Publications

• Succinyl-CoA:acetate CoA-transferase functioning in the oxidative tricarboxylic acid cycle in Desulfurella acetivorans. Frontiers in Microbiology, 13.
  Pettinato, Eugenio; Böhnert, Pauline & Berg, Ivan A.
  
• Propionate metabolism in Desulfurella acetivorans. Frontiers in Microbiology, 16.
  Pettinato, Eugenio; Steiner, Thomas M.; Cassens, Eric A.; Geisberger, Thomas; Seitz, Christian; König, Simone; Eisenreich, Wolfgang & Berg, Ivan A.