The CpxAR signaling system confers a fitness advantage for flea gut colonization by the plague bacillus.

IF 2.7 3区 生物学 Q3 MICROBIOLOGY
Journal of Bacteriology Pub Date : 2024-09-19 Epub Date: 2024-08-19 DOI:10.1128/jb.00173-24
Brandon Robin, Amélie Dewitte, Véronique Alaimo, Cecile Lecoeur, François Pierre, Gabriel Billon, Florent Sebbane, Sébastien Bontemps-Gallo
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Abstract

The adaptation of Yersinia pestis, the flea-borne plague agent, to fluctuating environmental conditions is essential for the successful colonization of the flea vector. A previous comparative transcriptomic analysis showed that the Cpx pathway of Y. pestis is up-regulated in infected fleas. The CpxAR two-component system is a component of the envelope stress response and is critical for maintaining the integrity of the cell. Here, a phenotypic screening revealed a survival defect of the cpxAR mutant to oxidative stress and copper. The measured copper concentration in the digestive tract contents of fed fleas increased fourfold during the digestive process. By direct analysis of phosphorylation of CpxR by a Phos-Tag gel approach, we demonstrated that biologically relevant concentrations of copper triggered the system. Then, a competitive challenge highlighted the role of the CpxAR system in bacterial fitness during flea infection. Lastly, an in vitro sequential exposure to copper and then H2O2 to mimic the flea suggests a model in which, within the insect digestive tract, the CpxAR system would be triggered by copper, establishing an oxidative stress response.

Importance: The bacterium Yersinia pestis is the agent of flea-borne plague. Our knowledge of the mechanisms used by the plague bacillus to infect the flea vector is limited. The up-regulation of the envelope stress response under the control of the Cpx signaling pathway was previously shown in a transcriptomic study. Here, our in vivo and in vitro approaches suggest a model in which Y. pestis uses the CpxAR phosphorelay system to sense and respond to the copper present in the flea gut, thereby optimizing the flea gut colonization. In other words, the system is essential for bacterial fitness in the flea.

CpxAR 信号系统为鼠疫杆菌在跳蚤肠道定殖提供了适应优势。
鼠疫耶尔森氏菌是由跳蚤传播的鼠疫病原体,它对波动的环境条件的适应对于跳蚤载体的成功定殖至关重要。之前的一项比较转录组分析表明,鼠疫耶尔森菌的 Cpx 通路在受感染的跳蚤体内上调。CpxAR 双组分系统是包膜应激反应的一个组成部分,对维持细胞的完整性至关重要。这里,表型筛选发现了 cpxAR 突变体对氧化应激和铜的生存缺陷。在消化过程中,喂食跳蚤消化道内容物中的铜浓度增加了四倍。通过 Phos-Tag 凝胶法对 CpxR 磷酸化的直接分析,我们证明了生物相关浓度的铜触发了该系统。然后,通过竞争挑战突出了 CpxAR 系统在跳蚤感染过程中对细菌适应性的作用。最后,通过体外连续暴露于铜和 H2O2 以模拟跳蚤,我们提出了一个模型,在该模型中,CpxAR 系统将在昆虫消化道内被铜触发,从而建立一种氧化应激反应:重要意义:鼠疫耶尔森菌是跳蚤传播鼠疫的病原体。我们对鼠疫杆菌感染跳蚤载体的机制了解有限。之前的一项转录组研究显示,包膜应激反应在 Cpx 信号通路的控制下上调。在这里,我们的体内和体外方法提出了一个模型,在该模型中,鼠疫酵母菌利用 CpxAR 磷酸循环系统来感知和响应跳蚤肠道中存在的铜,从而优化跳蚤肠道定植。换句话说,该系统对细菌在跳蚤体内的生存至关重要。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
Journal of Bacteriology
Journal of Bacteriology 生物-微生物学
CiteScore
6.10
自引率
9.40%
发文量
324
审稿时长
1.3 months
期刊介绍: The Journal of Bacteriology (JB) publishes research articles that probe fundamental processes in bacteria, archaea and their viruses, and the molecular mechanisms by which they interact with each other and with their hosts and their environments.
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