Miller Halie K, Kwuan Laura, Schwiesow Leah, Bernick David L, Mettert Erin, Ramirez Hector A, Ragle James M, Chan Patricia P, Kiley Patricia J, Lowe Todd M, Auerbuch Victoria
Department of Microbiology and Environmental Toxicology, University of California Santa Cruz, Santa Cruz, California, United States of America.
Biomolecular Engineering, University of California Santa Cruz, Santa Cruz, California, United States of America.
PLoS Pathog. 2014 Jun 12;10(6):e1004194. doi: 10.1371/journal.ppat.1004194. eCollection 2014 Jun.
Type III secretion systems (T3SS) are essential for virulence in dozens of pathogens, but are not required for growth outside the host. Therefore, the T3SS of many bacterial species are under tight regulatory control. To increase our understanding of the molecular mechanisms behind T3SS regulation, we performed a transposon screen to identify genes important for T3SS function in the food-borne pathogen Yersinia pseudotuberculosis. We identified two unique transposon insertions in YPTB2860, a gene that displays 79% identity with the E. coli iron-sulfur cluster regulator, IscR. A Y. pseudotuberculosis iscR in-frame deletion mutant (ΔiscR) was deficient in secretion of Ysc T3SS effector proteins and in targeting macrophages through the T3SS. To determine the mechanism behind IscR control of the Ysc T3SS, we carried out transcriptome and bioinformatic analysis to identify Y. pseudotuberculosis genes regulated by IscR. We discovered a putative IscR binding motif upstream of the Y. pseudotuberculosis yscW-lcrF operon. As LcrF controls transcription of a number of critical T3SS genes in Yersinia, we hypothesized that Yersinia IscR may control the Ysc T3SS through LcrF. Indeed, purified IscR bound to the identified yscW-lcrF promoter motif and mRNA levels of lcrF and 24 other T3SS genes were reduced in Y. pseudotuberculosis in the absence of IscR. Importantly, mice orally infected with the Y. pseudotuberculosis ΔiscR mutant displayed decreased bacterial burden in Peyer's patches, mesenteric lymph nodes, spleens, and livers, indicating an essential role for IscR in Y. pseudotuberculosis virulence. This study presents the first characterization of Yersinia IscR and provides evidence that IscR is critical for virulence and type III secretion through direct regulation of the T3SS master regulator, LcrF.
III型分泌系统(T3SS)对于几十种病原体的毒力至关重要,但在宿主外生长时并非必需。因此,许多细菌物种的T3SS受到严格的调控。为了增进我们对T3SS调控背后分子机制的了解,我们进行了转座子筛选,以鉴定食源性病原体假结核耶尔森菌中对T3SS功能重要的基因。我们在YPTB2860中鉴定出两个独特的转座子插入,该基因与大肠杆菌铁硫簇调节因子IscR有79%的同源性。假结核耶尔森菌iscR框内缺失突变体(ΔiscR)在分泌Ysc T3SS效应蛋白以及通过T3SS靶向巨噬细胞方面存在缺陷。为了确定IscR控制Ysc T3SS的机制,我们进行了转录组和生物信息学分析,以鉴定受IscR调控的假结核耶尔森菌基因。我们在假结核耶尔森菌yscW - lcrF操纵子上游发现了一个假定的IscR结合基序。由于LcrF控制耶尔森菌中许多关键T3SS基因的转录,我们推测假结核耶尔森菌IscR可能通过LcrF控制Ysc T3SS。事实上,纯化的IscR与鉴定出的yscW - lcrF启动子基序结合,并且在没有IscR的情况下,假结核耶尔森菌中lcrF和其他24个T3SS基因的mRNA水平降低。重要的是,口服感染假结核耶尔森菌ΔiscR突变体的小鼠在派尔集合淋巴结、肠系膜淋巴结、脾脏和肝脏中的细菌载量降低,表明IscR在假结核耶尔森菌毒力中起重要作用。这项研究首次对假结核耶尔森菌IscR进行了表征,并提供证据表明IscR通过直接调控T3SS主调节因子LcrF对毒力和III型分泌至关重要。