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
{"title":"The unique Legionella longbeachae capsule favors intracellular replication and immune evasion","authors":"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","doi":"10.1371/journal.ppat.1012534","DOIUrl":null,"url":null,"abstract":"<jats:italic>Legionella longbeachae</jats:italic> and <jats:italic>Legionella pneumophila</jats:italic> 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 <jats:italic>L</jats:italic>. <jats:italic>longbeachae</jats:italic> 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 <jats:italic>via</jats:italic> HLPC revealed the presence of a highly anionic polysaccharide that is absent in the capsule mutant. The capsule is important for replication and virulence <jats:italic>in vivo</jats:italic> in a mouse model of infection and in the natural host <jats:italic>Acanthamoeba castellanii</jats:italic>. 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 <jats:italic>L</jats:italic>. <jats:italic>longbeachae</jats:italic> capsule is a novel virulence factor, unique among the known <jats:italic>Legionella</jats:italic> species, which may aid <jats:italic>L</jats:italic>. <jats:italic>longbeachae</jats:italic> to survive in its specific niches and which partly confers <jats:italic>L</jats:italic>. <jats:italic>longbeachae</jats:italic> its unique infection characteristics.","PeriodicalId":20178,"journal":{"name":"PLoS Pathogens","volume":null,"pages":null},"PeriodicalIF":6.7000,"publicationDate":"2024-09-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"PLoS Pathogens","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1371/journal.ppat.1012534","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"Immunology and Microbiology","Score":null,"Total":0}
引用次数: 0
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.
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.