The unique Legionella longbeachae capsule favors intracellular replication and immune evasion

IF 6.7 1区 医学 Q1 Immunology and Microbiology PLoS Pathogens Pub Date : 2024-09-11 DOI:10.1371/journal.ppat.1012534
Silke Schmidt, Sonia Mondino, Laura Gomez-Valero, Pedro Escoll, Danielle P. A. Mascarenhas, Augusto Gonçalves, Pedro H. M. Camara, Francisco J. Garcia Rodriguez, Christophe Rusniok, Martin Sachse, Maryse Moya-Nilges, Thierry Fontaine, Dario S. Zamboni, Carmen Buchrieser
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Abstract

Legionella longbeachae and Legionella pneumophila are the most common causative agents of Legionnaires’ disease. While the clinical manifestations caused by both species are similar, species-specific differences exist in environmental niches, disease epidemiology, and genomic content. One such difference is the presence of a genomic locus predicted to encode a capsule. Here, we show that L. longbeachae indeed expresses a capsule in post-exponential growth phase as evidenced by electron microscopy analyses, and that capsule expression is abrogated when deleting a capsule transporter gene. Capsule purification and its analysis via HLPC revealed the presence of a highly anionic polysaccharide that is absent in the capsule mutant. The capsule is important for replication and virulence in vivo in a mouse model of infection and in the natural host Acanthamoeba castellanii. It has anti-phagocytic function when encountering innate immune cells such as human macrophages and it is involved in the low cytokine responses in mice and in human monocyte derived macrophages, thus dampening the innate immune response. Thus, the here characterized L. longbeachae capsule is a novel virulence factor, unique among the known Legionella species, which may aid L. longbeachae to survive in its specific niches and which partly confers L. longbeachae its unique infection characteristics.
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独特的长须鲸军团菌胶囊有利于细胞内复制和免疫逃避
长臂军团菌和嗜肺军团菌是军团病最常见的致病菌。虽然这两种病菌引起的临床表现相似,但在环境生态位、疾病流行病学和基因组内容方面存在物种特异性差异。其中一个差异是存在一个预测为胶囊编码的基因组位点。在这里,我们通过电子显微镜分析表明,L. longbeachae确实在后生长期表达胶囊,而且当删除胶囊转运体基因时,胶囊的表达也会减弱。通过 HLPC 对胶囊进行纯化和分析,发现胶囊突变体中不存在高阴离子多糖。这种胶囊对小鼠感染模型和自然宿主棘阿米巴的体内复制和毒力非常重要。当遇到先天性免疫细胞(如人类巨噬细胞)时,它具有抗吞噬功能,并参与小鼠和人类单核细胞衍生巨噬细胞的低细胞因子反应,从而抑制先天性免疫反应。因此,长须鲸军团菌胶囊是一种新的毒力因子,在已知的军团菌中是独一无二的,它可能有助于长须鲸军团菌在其特定的壁龛中生存,并在一定程度上赋予了长须鲸军团菌独特的感染特性。
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来源期刊
PLoS Pathogens
PLoS Pathogens 生物-病毒学
CiteScore
11.40
自引率
3.00%
发文量
598
审稿时长
2 months
期刊介绍: Bacteria, fungi, parasites, prions and viruses cause a plethora of diseases that have important medical, agricultural, and economic consequences. Moreover, the study of microbes continues to provide novel insights into such fundamental processes as the molecular basis of cellular and organismal function.
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