Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, Michigan, USA.
mBio. 2012 Oct 9;3(5):e00307-12. doi: 10.1128/mBio.00307-12.
Intracellular concentration of cyclic diguanylate monophosphate (c-di-GMP), a second messenger molecule, is regulated in bacteria by diguanylate cyclases (DGCs) (synthesizing c-di-GMP) and phosphodiesterases (PDEs) (degrading c-di-GMP). c-di-GMP concentration ([c-di-GMP]) affects motility and sessility in a reciprocal fashion; high [c-di-GMP] typically inhibits motility and promotes sessility. A c-di-GMP sensor domain, PilZ, also regulates motility and sessility. Uropathogenic Escherichia coli regulates these processes during infection; motility is necessary for ascending the urinary tract, while sessility is essential for colonization of anatomical sites. Here, we constructed and screened 32 mutants containing deletions of genes encoding each PDE (n = 11), DGC (n = 13), PilZ (n = 2), and both PDE and DGC (n = 6) domains for defects in motility, biofilm formation, and adherence for the prototypical pyelonephritis isolate E. coli CFT073. Three of 32 mutations affected motility, all of which were in genes encoding enzymatically inactive PDEs. Four PDEs, eight DGCs, four PDE/DGCs, and one PilZ regulated biofilm formation in a medium-specific manner. Adherence to bladder epithelial cells was regulated by [c-di-GMP]. Four PDEs, one DGC, and three PDE/DGCs repress adherence and four DGCs and one PDE/DGC stimulate adherence. Thus, specific effectors of [c-di-GMP] and catalytically inactive DGCs and PDEs regulate adherence and motility in uropathogenic E. coli. IMPORTANCE Uropathogenic Escherichia coli (UPEC) contains several genes annotated as encoding enzymes that increase or decrease the abundance of the second messenger molecule, c-di-GMP. While this class of enzymes has been studied in an E. coli K-12 lab strain, these proteins have not been comprehensively examined in UPEC. UPEC utilizes both swimming motility and adherence to colonize and ascend the urinary tract; both of these processes are hypothesized to be regulated by the concentration of c-di-GMP. Here, for the first time, in a uropathogenic strain, E. coli CFT073, we have characterized mutants lacking each protein and demonstrated that the uropathogen has diverged from E. coli K-12 to utilize these enzymes to regulate adherence and motility by distinct mechanisms.
细胞内环二鸟苷酸(c-di-GMP)的浓度是由细菌中的双鸟苷酸环化酶(DGCs)(合成 c-di-GMP)和磷酸二酯酶(PDEs)(降解 c-di-GMP)调节的。c-di-GMP 浓度([c-di-GMP])以相互相反的方式影响运动性和固着性;高 [c-di-GMP] 通常抑制运动性并促进固着性。c-di-GMP 传感器结构域 PilZ 也调节运动性和固着性。尿路致病性大肠杆菌(uropathogenic Escherichia coli)在感染过程中调节这些过程;运动性对于上尿路感染是必要的,而固着性对于解剖部位的定植是必不可少的。在这里,我们构建并筛选了 32 个突变体,这些突变体缺失了编码每个 PDE(n = 11)、DGC(n = 13)、PilZ(n = 2)和 PDE 和 DGC (n = 6)结构域的基因,以研究其在运动性、生物膜形成和粘附方面的缺陷,用于研究原型肾盂肾炎分离株大肠杆菌 CFT073。在 32 个突变体中,有 3 个突变体影响运动性,它们都存在于编码无酶活性 PDE 的基因中。四个 PDE、八个 DGC、四个 PDE/DGC 和一个 PilZ 以特定培养基的方式调节生物膜形成。对膀胱上皮细胞的粘附受到 [c-di-GMP] 的调节。四个 PDE、一个 DGC 和三个 PDE/DGC 抑制粘附,而四个 DGC 和一个 PDE/DGC 刺激粘附。因此,[c-di-GMP]的特定效应物和无酶活性的 DGC 和 PDE 调节尿路致病性大肠杆菌的粘附和运动性。重要性尿路致病性大肠杆菌(UPEC)包含几个被注释为编码酶的基因,这些酶可以增加或减少第二信使分子 c-di-GMP 的丰度。虽然这类酶已经在大肠杆菌 K-12 实验室菌株中进行了研究,但这些蛋白质尚未在 UPEC 中进行全面研究。UPEC 利用游泳运动性和粘附性来定植和上尿路感染;这两个过程都被假设受 c-di-GMP 浓度的调节。在这里,我们首次在尿路致病性菌株大肠杆菌 CFT073 中对缺失每种蛋白的突变体进行了特征描述,并证明了尿路病原体已经从大肠杆菌 K-12 分化出来,利用这些酶通过不同的机制来调节粘附性和运动性。