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To establish a successful infection within the host, a pathogen must closely regulate multiple virulence traits to ensure their accurate temporal and spatial expression. As a highly adapted intracellular pathogen,  Salmonella enterica  has acquired during its evolution various virulence genes via numerous lateral transfer events, including the acquisition of the  Salmonella  Pathogenicity Island 2 (SPI-2) and its associated effectors. Beneficial use of horizontally acquired genes requires that their expression is effectively coordinated with the already existing virulence programs and the regulatory set-up in the bacterium. As an example for such a mechanism, we show here that the ancestral PhoPQ system of  Salmonella enterica  is able to regulate directly the SPI-2 effector gene  sseL  (encoding a secreted deubiquitinase) in an SsrB-independent manner and that PhoP plays a part in a feed-forward regulatory loop, which fine-tunes the cellular level of SseL. Additionally, we demonstrate the presence of conserved  cis  regulatory elements in the promoter region of  sseL  and show direct binding of purified PhoP to this region. Interestingly, in contrast to the  S. enterica  PhoP, an ortholog regulator from a  S. bongori  SARC 12 strain was found to be impaired in promoting transcription of  sseL  and other genes from the PhoP regulon. These findings have led to the identification of a previously uncharacterized residue in the DNA-binding domain of PhoP, which is required for the transcriptional activation of PhoP regulated genes in  Salmonella  spp. Collectively our data demonstrate an interesting interface between the acquired SsrB regulon and the ancestral PhoPQ regulatory circuit, provide novel insights into the function of PhoP, and highlight a mechanism of regulatory integration of horizontally acquired genes into the virulence network of  Salmonella enterica .

The Salmonella enterica PhoP Directly Activates the Horizontally Acquired SPI-2 Gene sseL and Is Functionally Different from a S. bongori Ortholog