Outer Membrane Protein STM3031 (Ail/OmpX-Like Protein) Plays a Key Role in the Ceftriaxone Resistance of Salmonella enterica Serovar Typhimurium

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Abstract
Previously, the putative outer membrane protein STM3031 has been correlated with ceftriaxone resistance in Salmonella enterica serovar Typhimurium. In this study, this protein was almost undetectable in the ceftriaxone-susceptible strain 01-4, but its levels were increased in 01-4 isogenic strains for which MICs were higher. The stm3031 gene deletion mutant, R200(Δ stm3031 ), was generated and showed >64-fold lower ceftriaxone resistance than R200, supporting a key role for STM3031 in ceftriaxone resistance. To investigate which outer membrane protein(s) was associated with resistance, the outer membrane protein profiles of 01-4, R200, and R200(Δ stm3031 ) were compared proteomically. Nine proteins were identified as altered. The expression levels of AcrA, TolC, STM3031, STM1530, VacJ, and Psd in R200 were increased; those of OmpC, OmpD, and OmpW were decreased. The expression levels of OmpD, OmpW, STM1530, VacJ, and Psd, but not those of OmpC, AcrA, and TolC, in R200(Δ stm3031 ) were returned to the levels in strain 01-4. Furthermore, the genes' mRNA levels correlated with their protein levels when the three strains were compared. The detection of higher AcrB levels, linked to higher acrB , acrD , and acrF mRNA levels, in strain R200 than in strains 01-4 and R200(Δ stm3031 ) suggests that AcrB, AcrD, and AcrF participate in ceftriaxone resistance. Taken together with the location of STM3031 in the outer membrane, these results suggest that STM3031 plays a key role in ceftriaxone resistance, probably by reducing permeability via a decreased porin OmpD level and enhancing export via increased AcrD efflux pump activity.

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