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SmeYZ efflux pump is a critical pump responsible for aminoglycosides resistance, virulence-related characteristics (oxidative stress susceptibility, motility, and secreted protease activity), and virulence in  Stenotrophomonas maltophilia . However, the regulatory circuit involved in SmeYZ expression is little known. A two-component regulatory system (TCS),  smeRySy , transcribed divergently from the  smeYZ  operon is the first candidate to be considered. To assess the role of SmeRySy in  smeYZ  expression, the  smeRySy  isogenic deletion mutant, KJΔRSy, was constructed by gene replacement strategy. Inactivation of  smeSyRy  correlated with a higher susceptibility to aminoglycosides concomitant with an increased resistance to chloramphenicol, ciprofloxacin, tetracycline, and macrolides. To elucidate the underlying mechanism responsible for the antimicrobials susceptibility profiles, the SmeRySy regulon was firstly revealed by transcriptome analysis and further confirmed by quantitative real-time polymerase chain reaction (qRT-PCR) and promoter transcription fusion constructs assay. The results demonstrate that inactivation of  smeRySy  decreased the expression of SmeYZ pump and increased the expression of SmeDEF pump, which underlies the  ΔsmeSyRy -mediated antimicrobials susceptibility profile. To elucidate the cognate relationship between SmeSy and SmeRy, a single mutant, KJΔRy, was constructed and the complementation assay of KJΔRSy with  smeRy  were performed. The results support that SmeSy-SmeRy TCS is responsible for the regulation of  smeYZ  operon; whereas SmeSy may be cognate with another unidentified response regulator for the regulation of  smeDEF  operon. The impact of inverse expression of SmeYZ and SmeDEF pumps on physiological functions was evaluated by mutants construction, H 2 O 2  susceptibility test, swimming, and secreted protease activity assay. The increased expression of SmeDEF pump in KJΔRSy may compensate, to some extents, the SmeYZ downexpression-mediated compromise with respect to its role in secreted protease activity.

plos one

Inactivation of SmeSyRy Two-Component Regulatory System Inversely Regulates the Expression of SmeYZ and SmeDEF Efflux Pumps in Stenotrophomonas maltophilia