Institute of Microbiology and College of Life Sciences, Zhejiang Universitygrid.13402.34, Hangzhou, Zhejiang, China.
Microbiol Spectr. 2021 Sep 3;9(1):e0069021. doi: 10.1128/Spectrum.00690-21. Epub 2021 Aug 18.
The bacterial cell envelope is not only a protective structure that surrounds the cytoplasm but also the place where a myriad of biological processes take place. This multilayered complex is particularly important for electroactive bacteria such as Shewanella oneidensis, as it generally hosts branched electron transport chains and numerous reductases for extracellular respiration. However, little is known about how the integrity of the cell envelope is established and maintained in these bacteria. By tracing the synthetic lethal effect of Arc two-component system and σ in S. oneidensis, in this study, we identified the lipopolysaccharide transport (Lpt) system as the determining factor. Both Arc and σ, by regulating transcription of and , respectively, are required for the Lpt system to function properly. The ArcA loss results in an LptFG shortage that triggers activation of σ and leads to LptD overproduction. LptFG and LptD at abnormal levels cause a defect in the lipopolysaccharide (LPS) transport, leading to cell death unless σ-dependent envelope stress response is in place. Overall, our report reveals for the first time that Arc works together with σ to maintain the integrity of the S. oneidensis cell envelope by participating in the regulation of the LPS transport system. Arc is a well-characterized global regulatory system that modulates cellular respiration by responding to changes in the redox status in bacterial cells. In addition to regulating expression of respiratory enzymes, Shewanella oneidensis Arc also plays a critical role in cell envelope integrity. The absence of Arc and master envelope stress response (ESR) regulator σ causes a synthetic lethal phenotype. Our research shows that the Arc loss downregulates expression, leading to cell envelope defects that require σ-mediated ESR for viability. The complex mechanisms revealed here underscore the importance of the interplay between global regulators in bacterial adaption to their natural inhabits.
细菌的细胞包膜不仅是包围细胞质的保护结构，也是许多生物过程发生的地方。这个多层次的复杂结构对电活性细菌（如希瓦氏菌属）尤为重要，因为它通常承载着分支的电子传递链和许多用于细胞外呼吸的还原酶。然而，对于这些细菌中细胞包膜的完整性是如何建立和维持的，人们知之甚少。通过追踪 Shewanella oneidensis 中Arc 双组分系统和σ的合成致死效应，本研究确定了脂多糖转运（Lpt）系统是决定因素。Arc 和 σ 分别通过调节 和 的转录，分别需要 Lpt 系统正常运作。ArcA 的缺失导致 LptFG 短缺，从而激活 σ，导致 LptD 过度产生。异常水平的 LptFG 和 LptD 导致脂多糖（LPS）转运缺陷，导致细胞死亡，除非存在 σ 依赖性包膜应激反应。总的来说，我们的报告首次揭示了 Arc 通过参与调节 LPS 转运系统与 σ 一起维持 Shewanella oneidensis 细胞包膜的完整性。Arc 是一个经过充分研究的全局调控系统，通过响应细菌细胞内氧化还原状态的变化来调节细胞呼吸。除了调节呼吸酶的表达外，Shewanella oneidensis Arc 还在细胞包膜完整性中发挥关键作用。Arc 和主包膜应激反应（ESR）调节因子 σ 的缺失会导致合成致死表型。我们的研究表明，Arc 的缺失下调了 表达，导致细胞包膜缺陷，需要 σ 介导的 ESR 才能存活。这里揭示的复杂机制强调了全局调节剂在细菌适应其自然栖息地中的相互作用的重要性。
