Comparative analyses of how diverse pathogenic bacteria combat the potential for secretion-associated stress

Secretins are a family of outer membrane pore-forming proteins that are critical for virulence-related Type 2 and Type 3 secretion systems, as well as Type 4 pili biogenesis and filamentous phage export in Gram-negative bacteria. Although secretins normally localize in the outer membrane they can sometimes mislocalize and cause bacterial cell stress. This stress is specifically alleviated by the widely conserved phage-shock-protein (Psp) system. The Psp system is present in numerous bacterial species. However, some bacteria use secretins but do not have the Psp system. In order to provide a global understanding of how two different organisms Yersinia enterocolitica (Psp +) and Pseudomonas aeruginosa (Psp-) might deal with the potential for secretin-induced stress, random transposon mutagenesis and microarray studies were undertaken. This revealed that in the model Psp+ species Y. enterocolitica the Psp proteins were necessary and sufficient for tolerating secretin-induced stress. However, in the model Psp- species P. aeruginosa there was no transcriptional response to secretin-induced stress. Nevertheless, transposon insertion in four different loci rendered P. aeruginosa hypersensitive to secretin production. One of these loci (PA0943) encoded a protein that was shown to be important for localization of the XcpQ secretin, a component of a Type 2 secretion system, to the outer membrane. Therefore, deletion of PA0943 led to a defect in the export of several important Type 2 secretion substrates. Taken together, all of these data suggest that P. aeruginosa lacks an equivalent of the Psp stress-response system. Instead, P. aeruginosa may prevent secretin mislocalization stress from occurring. Mutations, such as a PA0943 disruption, may cause elevated secretin stress to which P. aeruginosa cannot respond. Consistent with this, providing the P. aeruginosa mutant with critical Psp components alleviated the secretin-sensitivity. In summary, with regard to secretin-induced stress, Y. enterocolitica employs a response strategy whereas P. aeruginosa may rely on prevention.