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Horizontally acquired genes typically function as autonomous units conferring new abilities when introduced into different species. However, we reasoned that proteins preexisting in an organism might constrain the functionality of a horizontally acquired gene product if it operates on an ancestral pathway. Here, we determine how the horizontally acquired  pmrD  gene product activates the ancestral PmrA/PmrB two-component system in  Salmonella enterica  but not in the closely related bacterium  Escherichia coli . The  Salmonella  PmrD protein binds to the phosphorylated PmrA protein (PmrA-P), protecting it from dephosphorylation by the PmrB protein. This results in transcription of PmrA-dependent genes, including those conferring polymyxin B resistance. We now report that the  E. coli  PmrD protein can activate the PmrA/PmrB system in  Salmonella  even though it cannot do it in  E. coli , suggesting that these two species differ in an additional component controlling PmrA-P levels. We establish that the  E. coli  PmrB displays higher phosphatase activity towards PmrA-P than the  Salmonella  PmrB, and we identified a PmrB subdomain responsible for this property. Replacement of the  E. coli pmrB  gene with the  Salmonella  homolog was sufficient to render  E. coli  resistant to polymyxin B under PmrD-inducing conditions. Our findings provide a singular example whereby quantitative differences in the biochemical activities of orthologous ancestral proteins dictate the ability of a horizontally acquired gene product to confer species-specific traits. And they suggest that horizontally acquired genes can potentiate selection at ancestral loci.

Ancestral Genes Can Control the Ability of Horizontally Acquired Loci to Confer New Traits