title: Evolutionary expansion of a regulatory network by counter-silencing.
abstract: Horizontal gene transfer plays a major role in bacterial evolution. Successful acquisition of new genes requires their incorporation into existing regulatory networks. This study compares the regulation of conserved genes in the PhoPQ regulon of Salmonella enterica serovar Typhimurium with that of PhoPQ-regulated horizontally acquired genes, which are silenced by the histone-like protein H-NS. We demonstrate that PhoP upregulates conserved and horizontally acquired genes by distinct mechanisms. Conserved genes are regulated by classical PhoP-mediated activation and are invariant in promoter architecture, whereas horizontally acquired genes exhibit variable promoter architecture and are regulated by PhoP-mediated counter-silencing. Biochemical analyses show that a horizontally acquired promoter adopts different structures in the silenced and counter-silenced states, implicating the remodelling of the H-NS nucleoprotein filament and the subsequent restoration of open-complex formation as the central mechanism of counter-silencing. Our results indicate that counter-silencing is favoured in the regulatory integration of newly acquired genes because it is able to accommodate multiple promoter architectures.
authors.affiliation: Department of Laboratory Medicine, University of Washington School of Medicine, Seattle, Washington 98195, USA.
authors.forename: W Ryan
authors.initials: WR
authors.lastname: Will
authors.affiliation: Department of Chemistry, University of Washington, Seattle, Washington 98195, USA.
authors.forename: Denise H
authors.initials: DH
authors.lastname: Bale
authors.affiliation: Department of Chemistry, University of Washington, Seattle, Washington 98195, USA.
authors.forename: Philip J
authors.initials: PJ
authors.lastname: Reid
authors.affiliation: Department of Laboratory Medicine, University of Washington School of Medicine, Seattle, Washington 98195, USA.
authors.forename: Stephen J
authors.initials: SJ
authors.lastname: Libby
authors.affiliation: 1] Department of Laboratory Medicine, University of Washington School of Medicine, Seattle, Washington 98195, USA [2] Department of Microbiology, University of Washington School of Medicine, Seattle, Washington 98195, USA.
authors.forename: Ferric C
authors.initials: FC
authors.lastname: Fang
mesh_terms: D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D005075:Biological Evolution; D004268:DNA-Binding Proteins / Q000378:metabolism; D003850:Deoxyribonuclease I / Q000378:metabolism; D015964:Gene Expression Regulation, Bacterial; D053263:Gene Regulatory Networks; D020868:Gene Silencing; D011401:Promoter Regions, Genetic; D018085:Regulon / Q000235:genetics; D012486:Salmonella typhimurium / Q000235:genetics*; D014466:Ultraviolet Rays
chemical_list: D001426:Bacterial Proteins; D004268:DNA-Binding Proteins; C031908:H-NS protein, bacteria; C061064:PhoP protein, Bacteria; D003850:Deoxyribonuclease I