Abstract
Changes in gene regulatory circuits often give rise to phenotypic differences among closely related organisms. In bacteria, these changes can result from alterations in the ancestral genome and/or be brought about by genes acquired by horizontal transfer. Here, we identify an allele of the ancestral transcription factor PmrA that requires the horizontally acquired pmrD gene product to promote gene expression. We determined that a single amino acid difference between the PmrA proteins from the human adapted Salmonella enterica serovar Paratyphi B and the broad host range S. enterica serovar Typhimurium rendered transcription of PmrA-activated genes dependent on the PmrD protein in the former but not the latter serovar. Bacteria harboring the serovar Typhimurium allele exhibited polymyxin B resistance under PmrA- or under PmrA- and PmrD-inducing conditions. By contrast, isogenic strains with the serovar Paratyphi B allele displayed PmrA-regulated polymyxin B resistance only when experiencing activating conditions for both PmrA and PmrD. We establish that the two PmrA orthologs display quantitative differences in several biochemical properties. Strains harboring the serovar Paratyphi B allele showed enhanced biofilm formation, a property that might promote serovar Paratyphi B's chronic infection of the gallbladder. Our findings illustrate how subtle differences in ancestral genes can impact the ability of horizontally acquired genes to confer new properties.
Highlights
The phenotypic properties that distinguish closely related bacterial species are often ascribed to differences in gene content [1,2]
SARA46 is an S. enterica isolate belonging to the Paratyphi B serovar and is classified as a member of the systemic pathovar (SPV) that causes paratyphoid fever in humans [20,21]
This is in contrast to S. typhimurium, which grew on both media (Figure 2A)
Summary
The phenotypic properties that distinguish closely related bacterial species are often ascribed to differences in gene content [1,2]. Acquisition of the cholera toxin phage by Vibrio cholerae [4] or of the pathogenicity island LEE – for locus of enterocyte effacement – by enteropathogenic Escherichia coli (EPEC) [5] conferred virulence properties upon these bacteria. The recovery of the same antibiotic resistance genes in unrelated bacterial species [8] indicates that horizontally acquired genes are capable of conferring new properties to organisms with significantly different genomes. This situation might be different if a horizontally acquired gene product targets ancestral proteins because allelic differences among ancestral orthologs might impact the ability of a horizontally acquired gene to function.
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