Alkaline shock protein 23 (Asp23)-controlled cell wall imbalance promotes membrane vesicle biogenesis in Staphylococcus aureus

IF 15.5 1区 医学 Q1 CELL BIOLOGY Journal of Extracellular Vesicles Pub Date : 2024-08-28 DOI:10.1002/jev2.12501
Jia Li, Keting Zhu, Chao Li, Wei Huang, Xing Tian, He Yan, Yan Zhao, Jing Zhou, Xindi Gao, Xiancai Rao, Gang Li, Renjie Zhou, Ming Li
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Abstract

Membrane vesicles (MVs) are produced by species across all domains of life and have diverse physiological functions as well as promising applications. While the mechanisms for vesiculation in Gram-negative bacteria are well-established, the genetic determinants and regulatory factors responsible for MV biogenesis in Gram-positive bacteria remain largely unknown. Here, we demonstrate that a Q225P substitution in the alternative sigma factor B (SigB) triggers MV production in Staphylococcus aureus strain Newman by hindering the specific binding of SigB to the asp23 promoter, thereby repressing expression of alkaline shock protein 23 (Asp23). Isogenic deletion of asp23 also promotes MV formation in Newman, confirming the critical roles played by sigB and asp23 in modulating S. aureus vesiculation. While bacterial growth and cytoplasmic membrane fluidity are not impaired, mutation of asp23 weakens the cell wall and enhances autolysis, consistent with decreased expression of alpha-type psm and lrgAB that modulate murein hydrolase activity. TEM and proteomic analysis show that Newman and asp23 deletion mutant generate MVs with nearly identical morphology and composition, but virulence-associated factors are significantly enriched in MVs from the asp23 mutant. Overall, this study reveals novel genetic determinants underlying S. aureus vesiculation and advances the understanding of the physiology of MV biogenesis in S. aureus.

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碱性休克蛋白 23(Asp23)控制的细胞壁失衡促进了金黄色葡萄球菌膜囊泡的生物生成。
生命各领域的物种都会产生膜囊泡,膜囊泡具有多种生理功能,应用前景广阔。虽然革兰氏阴性细菌的囊泡形成机制已经确立,但负责革兰氏阳性细菌中膜泡生物生成的遗传决定因素和调控因子在很大程度上仍然未知。在这里,我们证明了替代σ因子 B(SigB)中的 Q225P 取代会阻碍 SigB 与 asp23 启动子的特异性结合,从而抑制碱性休克蛋白 23(Asp23)的表达,从而引发金黄色葡萄球菌纽曼菌株中 MV 的产生。在纽曼菌株中,asp23的同源缺失也会促进MV的形成,这证实了sigB和asp23在调节金黄色葡萄球菌泡状化过程中所起的关键作用。虽然细菌生长和细胞质膜流动性并未受损,但突变 asp23 会削弱细胞壁并促进自溶,这与调节金黄色葡萄球菌水解酶活性的 alpha 型 psm 和 lrgAB 表达量减少是一致的。TEM和蛋白质组分析表明,纽曼和asp23缺失突变体产生的MV具有几乎相同的形态和组成,但asp23突变体的MV中显著富集了毒力相关因子。总之,这项研究揭示了金黄色葡萄球菌输精管形成的新的遗传决定因素,加深了人们对金黄色葡萄球菌输精管生物发生生理学的理解。
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来源期刊
Journal of Extracellular Vesicles
Journal of Extracellular Vesicles Biochemistry, Genetics and Molecular Biology-Cell Biology
CiteScore
27.30
自引率
4.40%
发文量
115
审稿时长
12 weeks
期刊介绍: The Journal of Extracellular Vesicles is an open access research publication that focuses on extracellular vesicles, including microvesicles, exosomes, ectosomes, and apoptotic bodies. It serves as the official journal of the International Society for Extracellular Vesicles and aims to facilitate the exchange of data, ideas, and information pertaining to the chemistry, biology, and applications of extracellular vesicles. The journal covers various aspects such as the cellular and molecular mechanisms of extracellular vesicles biogenesis, technological advancements in their isolation, quantification, and characterization, the role and function of extracellular vesicles in biology, stem cell-derived extracellular vesicles and their biology, as well as the application of extracellular vesicles for pharmacological, immunological, or genetic therapies. The Journal of Extracellular Vesicles is widely recognized and indexed by numerous services, including Biological Abstracts, BIOSIS Previews, Chemical Abstracts Service (CAS), Current Contents/Life Sciences, Directory of Open Access Journals (DOAJ), Journal Citation Reports/Science Edition, Google Scholar, ProQuest Natural Science Collection, ProQuest SciTech Collection, SciTech Premium Collection, PubMed Central/PubMed, Science Citation Index Expanded, ScienceOpen, and Scopus.
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