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Abstract
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.
Highlights
Related bacterial species often exhibit significant differences in gene content [1]
A search of the completed genomes in the NCBI microbial genomes database for the presence of sequences homologous to the S. enterica 14028s or E. coli K12 MG1655 PmrD protein showed that pmrD is limited to enteric bacteria of the Klebsiella, Citrobacter, Salmonella and Escherichia lineages (Figure S1A)
Unlike self-contained horizontally acquired gene clusters that readily confer a new trait upon introgression [1,8,9], the functionality of a horizontally acquired gene product operating on ancestral pathways depends largely upon the biochemical properties of existing ancestral proteins, which can act in a variety of ways [33,34,35]
Summary
Related bacterial species often exhibit significant differences in gene content [1]. Other horizontally acquired genes operate on ancestral cellular pathways [10,11], raising questions as to the changes experienced both by the horizontally acquired DNA and the host bacterial genome that enable an organism to realize the fitness gains mediated by the acquired sequences. This question can be addressed by first identifying a horizontally acquired gene product that behaves differently in present-day bacterial species, and by subsequently determining the changes in the horizontally acquired locus and/or associated ancestral genes that are responsible for a change in function. We provide a singular example of how an ancestral locus controls the ability of a horizontally acquired gene to confer a new ability
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