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Ancestral genes can control the ability of horizontally acquired loci to confer new traits.

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.

SUBMITTER: Chen HD

PROVIDER: S-EPMC3140997 | biostudies-literature | 2011 Jul

REPOSITORIES: biostudies-literature

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Ancestral genes can control the ability of horizontally acquired loci to confer new traits.

Chen H Deborah HD Jewett Mollie W MW Groisman Eduardo A EA

PLoS genetics 20110721 7

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 Escher ...[more]

PMID: 21811415

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Project description:SgrS RNA is a model for the large class of Hfq-associated small RNAs that act to post-transcriptionally regulate bacterial mRNAs. The function of SgrS is well-characterized in non-pathogenic Escherichia coli where it was originally shown to counteract glucose-phosphate stress by acting as a repressor of ptsG mRNA which encodes the major glucose transporter. We have discovered new SgrS targets in Salmonella Typhimurium, a pathogen related to E. coli, which recently acquired a quarter of all genes by horizontal gene transfer. We demonstrate that the conserved short seed region of SgrS that recognizes ptsG was recruited to target the Salmonella-specific sopD mRNA of a secreted virulence protein. The SgrS-sopD interaction is exceptionally selective; we find that sopD2 mRNA whose gene arose from sopD duplication during Salmonella evolution, is deaf to SgrS owing to a non-productive G:U pair in the potential SgrS-sopD2 RNA duplex versus G:C in SgrS-sopD. In other words, SgrS discriminates the two virulence factor mRNAs at the level of a single hydrogen bond. Our study suggests that bacterial pathogens employ their large suites of conserved Hfq-associated regulators to integrate horizontally acquired genes into existing post-transcriptional networks, just as conserved transcription factors are recruited to tame foreign genes at the DNA level. The results graphically illustrate the importance of the seed regions of bacterial small RNAs to select new targets with high fidelity, and argue that target predictions must consider all-or-none decisions by individual seed nucleotides. To determine the targets of the small regulatory RNA SgrS in S. Typhimurium, we looked at the effect of a short pulse of SgrS over-expression on the Salmonella transcriptome. To achieve over-expression, the sgrS gene was cloned in the pBAD plasmid and induced with 0.2% L-arabinose for 10 min. We then extracted the total RNA for transcriptional profiling. A strain carrying the pBAD plasmid w/o insert was used as negative control. 3 biological replicates were performed. This sRNA target identification strategy has been described in Papenfort et al; Molecular Microbiology (2006) 62(6), 1674–1688.

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Ancestral genes can control the ability of horizontally acquired loci to confer new traits.

Publications

Ancestral genes can control the ability of horizontally acquired loci to confer new traits.

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