The PrpF protein of Shewanella oneidensis MR-1 catalyzes the isomerization of 2-methyl-cis-aconitate during the catabolism of propionate via the AcnD-dependent 2-methylcitric acid cycle

PLoS One. 2017 Nov 16;12(11):e0188130. doi: 10.1371/journal.pone.0188130. eCollection 2017.

Abstract

The 2-methylcitric acid cycle (2-MCC) is a common route of propionate catabolism in microorganisms. In Salmonella enterica, the prpBCDE operon encodes most of the 2-MCC enzymes. In other organisms, e.g., Shewanella oneidensis MR-1, two genes, acnD and prpF replace prpD, which encodes 2-methylcitrate dehydratase. We showed that together, S. oneidensis AcnD and PrpF (SoAcnD, SoPrpF) compensated for the absence of PrpD in a S. enterica prpD strain. We also showed that SoAcnD had 2-methylcitrate dehydratase activity and that PrpF has aconitate isomerase activity. Here we report in vitro evidence that the product of the SoAcnD reaction is an isomer of 2-methyl-cis-aconitate (2-MCA], the product of the SePrpD reaction. We show that the SoPrpF protein isomerizes the product of the AcnD reaction into the PrpD product (2-MCA], a known substrate of the housekeeping aconitase (AcnB]. Given that SoPrpF is an isomerase, that SoAcnD is a dehydratase, and the results from in vivo and in vitro experiments reported here, it is likely that 4-methylaconitate is the product of the AcnD enzyme. Results from in vivo studies using a S. enterica prpD strain show that SoPrpF variants with substitutions of residues K73 or C107 failed to support growth with propionate as the sole source of carbon and energy. High-resolution (1.22 Å) three-dimensional crystal structures of PrpFK73E in complex with trans-aconitate or malonate provide insights into the mechanism of catalysis of the wild-type protein.

MeSH terms

  • Aconitate Hydratase / chemistry
  • Aconitate Hydratase / metabolism*
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / classification
  • Bacterial Proteins / metabolism*
  • Catalysis
  • Citrates / metabolism*
  • Crystallography, X-Ray
  • Genes, Bacterial
  • Isomerism
  • Mutagenesis, Site-Directed
  • Phylogeny
  • Protein Conformation
  • Shewanella / genetics
  • Shewanella / metabolism*

Substances

  • Bacterial Proteins
  • Citrates
  • 2-methylcitric acid
  • Aconitate Hydratase