AbstractPhosphoenolpyruvate carboxykinases (PEPCK) are a well‐studied family of enzymes responsible for the regulation of TCA cycle flux, where they catalyze the interconversion of oxaloacetic acid (OAA) and phosphoenolpyruvate (PEP) using a phosphoryl donor/acceptor. These enzymes have typically been divided into two nucleotide‐dependent classes, those that use ATP and those that use GTP. In the 1960's and early 1970's, a group of papers detailed biochemical properties of an enzyme named phosphoenolpyruvate carboxytransphosphorylase (later identified as a third PEPCK) from Propionibacterium freudenreichii (PP_i‐PfPEPCK), which instead of using a nucleotide, utilized PP_i to catalyze the same interconversion of OAA and PEP. The presented work expands upon the initial biochemical experiments for PP_i‐PfPEPCK and interprets these data considering both the current understanding of nucleotide‐dependent PEPCKs and is supplemented with a new crystal structure of PP_i‐PfPEPCK in complex with malate at a putative allosteric site. Most interesting, the data are consistent with PP_i‐PfPEPCK being a Fe²⁺ activated enzyme in contrast with the Mn²⁺ activated nucleotide‐dependent enzymes which in part results in some unique kinetic properties for the enzyme when compared to the more widely distributed GTP‐ and ATP‐dependent enzymes.