Cobamides (Cbas) are cobalt-containing tetrapyrroles that are synthesized only by some bacteria and archaea. Cbas are distinguished from each other by the chemical identity of the lower ligand base. The lower ligand must be activated to a unique nucleotide before its attachment to the central ring of the cobamide precursor cobinamide-GDP. This nucleotide exhibits an alpha N-glycosidic linkage between the base and the C1 of the ribosyl moiety. Classically, this activation proceeds directly via a single enzyme, the phosphoribosyltransferase CobT. However, some Firmicutes utilize an alternative route to synthesize the ribotide: a transporter, CblT, to scavenge the -N-link riboside (i.e., -Ribazole, -R) from the environment; and a kinase, CblS, to phosphorylate the riboside to the ribotide upon transport. Here, we report that expression of CblS and CblT from G. kaustophilus restores growth in an S. enterica strain lacking CobT under conditions where Cba synthesis is required, even in the absence of the -riboside. This unexpected finding suggests that S. enterica synthesizes -R endogenously. A continuous spectrophotometric assay revealed that CblS is specific for -N-linked ribosides. Feeding experiments reveal that while most -ribosides are utilized directly by S. enterica when it depends on the kinase for the synthesis of -ribotides, the -riboside -adenosine is neither synthesized nor transported by S. enterica. Site-directed mutagenesis of conserved residues generated variants of the CblS kinase which could be used to probe for -R synthesis in S. enterica.Attempts to understand how S. enterica synthesizes DMB and activates the base to -R revealed a complex interplay between purine metabolism and DMB scavenging as the loss of genes involved in nucleoside salvaging and purine biosynthesis resulted in strains unable to scavenge DMB. We report that the uptake of the bases 5-hydroxybenzimidazole or 5-methoxybenzimidazole lead to the synthesis of the 5,6-dimethybenzimidazole (DMB)-containing Cba, indicating that the purine synthesis intermediate aminoimidazole-ribotide (AIR) may be the origin of DMB instead of reduced FMN, as has been proposed.