School of Infection and Immunity, University of Glasgow, Glasgow, United Kingdom.
School of Microbiology, University College Cork, Cork, Ireland.
PLoS Pathog. 2024 Oct 15;20(10):e1012451. doi: 10.1371/journal.ppat.1012451. eCollection 2024 Oct.
The ability of the attaching and effacing pathogens enterohaemorrhagic Escherichia coli (EHEC) and Citrobacter rodentium to overcome colonisation resistance is reliant on a type 3 secretion system used to intimately attach to the colonic epithelium. This crucial virulence factor is encoded on a pathogenicity island known as the Locus of Enterocyte Effacement (LEE) but its expression is regulated by several core-genome encoded transcription factors. Here, we unveil that the core transcription factor PdhR, traditionally known as a regulator of central metabolism in response to cellular pyruvate levels, is a key activator of the LEE. Through genetic and molecular analyses, we demonstrate that PdhR directly binds to a specific motif within the LEE master regulatory region, thus activating type 3 secretion directly and enhancing host cell adhesion. Deletion of pdhR in EHEC significantly impacted the transcription of hundreds of genes, with pathogenesis and protein secretion emerging as the most affected functional categories. Furthermore, in vivo studies using C. rodentium, a murine model for EHEC infection, revealed that PdhR is essential for effective host colonization and maximal LEE expression within the host. Our findings provide new insights into the complex regulatory networks governing bacterial pathogenesis. This research highlights the intricate relationship between virulence and metabolic processes in attaching and effacing pathogens, demonstrating how core transcriptional regulators can be co-opted to control virulence factor expression in tandem with the cell's essential metabolic circuitry.
黏附侵袭性肠出血性大肠杆菌(EHEC)和鼠柠檬酸杆菌克服定植抗性的能力依赖于一种用于紧密黏附结肠上皮的 III 型分泌系统。这种关键毒力因子编码在一个被称为肠上皮细胞消失(LEE)的致病性岛,但它的表达受几个核心基因组编码的转录因子调控。在这里,我们揭示了核心转录因子 PdhR,传统上被认为是响应细胞内丙酮酸水平的中央代谢调节剂,是 LEE 的关键激活剂。通过遗传和分子分析,我们证明 PdhR 直接结合到 LEE 主调控区的特定模体上,从而直接激活 III 型分泌并增强宿主细胞黏附。EHEC 中 pdhR 的缺失显著影响了数百个基因的转录,其中发病机制和蛋白质分泌是受影响最大的功能类别。此外,使用鼠柠檬酸杆菌(EHEC 的一种小鼠感染模型)进行的体内研究表明,PdhR 对于有效的宿主定植和宿主内 LEE 的最大表达是必不可少的。我们的发现为调控细菌发病机制的复杂调控网络提供了新的见解。这项研究强调了黏附侵袭性病原体中毒力和代谢过程之间的复杂关系,展示了核心转录调节剂如何与细胞的基本代谢电路协同作用来控制毒力因子的表达。