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Salmonella enterica  serovar Typhimurium ( S . Typhimurium) is a major intestinal pathogen of both humans and animals.  Salmonella  pathogenicity island 1 (SPI-1)-encoded virulence genes are required for  S . Typhimurium invasion. While oxygen (O 2 ) limitation is an important signal for SPI-1 induction under host conditions, how the signal is received and integrated to the central SPI-1 regulatory system in  S . Typhimurium is not clear. Here, we report a signal transduction pathway that activates SPI-1 expression in response to low O 2 . A novel regulator encoded within SPI-14 (STM14_1008), named LoiA ( l ow  o xygen  i nduced factor  A ), directly binds to the promoter and activates transcription of  hilD , leading to the activation of  hilA  (the master activator of SPI-1). Deletion of  loiA  significantly decreased the transcription of  hilA ,  hilD  and other representative SPI-1 genes ( sipB ,  spaO ,  invH ,  prgH  and  invF ) under low O 2  conditions. The response of LoiA to the low O 2  signal is mediated by the ArcB/ArcA two-component system. Deletion of either  arcA  or  arcB  significantly decreased transcription of  loiA  under low O 2  conditions. We also confirmed that SPI-14 contributes to  S . Typhimurium virulence by affecting invasion, and that  loiA  is the virulence determinant of SPI-14. Mice infection assays showed that  S . Typhimurium virulence was severely attenuated by deletion of either the entire SPI-14 region or the single  loiA  gene after oral infection, while the virulence was not affected by either deletion after intraperitoneal infection. The signal transduction pathway described represents an important mechanism for  S . Typhimurium to sense and respond to low O 2  conditions of the host intestinal tract for invasion. SPI-14-encoded  loiA  is an essential element of this pathway that integrates the low O 2  signal into the SPI-1 regulatory system. Acquisition of SPI-14 is therefore crucial for the evolution of  S . Typhimurium as an intestinal pathogen.

Signal transduction pathway mediated by the novel regulator LoiA for low oxygen tension induced Salmonella Typhimurium invasion