Abstract
Two closely related bacterial species, Segniliparus rotundus and Segniliparus rugosus, have emerged as important human pathogens, but little is known about the immune responses they elicit or their comparative pathophysiologies. To determine the virulence and immune responses of the two species, we compared their abilities to grow in phagocytic and non-phagocytic cells. Both species maintained non-replicating states within A549 epithelial cells. S. rugosus persisted longer and multiplied more rapidly inside murine bone marrow-derived macrophages (BMDMs), induced more pro-inflammatory cytokines, and induced higher levels of macrophage necrosis. Activation of BMDMs by both species was mediated by toll-like receptor 2 (TLR2), followed by mitogen-activated protein kinases (MAPK) and nuclear factor κB (NF-κB) signaling pathways, indicating a critical role for TLR2 in Segniliparus-induced macrophage activation. S. rugosus triggered faster and stronger activation of MAPK signaling and IκB degradation, indicating that S. rugosus induces more pro-inflammatory cytokines than S. rotundus. Multifocal granulomatous inflammations in the liver and lung were observed in mice infected with S. rugosus, but S. rotundus was rapidly cleared from all organs tested within 15 days post-infection. Furthermore, S. rugosus induced faster infiltration of innate immune cells such as neutrophils and macrophages to the lung than S. rotundus. Our results suggest that S. rugosus is more virulent and induces a stronger immune response than S. rotundus.
Highlights
Segniliparus rugosus and S. rotundus are the only two species belonging to the genus Segniliparus, first identified in 2005, which is the sole genus in the family Segniliparaceae [1]
We comparatively investigated the phenotypic differences in the pathogenesis and immune responses of S. rugosus and S. rotundus infections using murine bone marrow-derived macrophages and in vivo infection models
To examine whether S. rotundus and S. rugosus are selectively able to infect and replicate in phagocytic or nonphagocytic cells, bone marrow-derived macrophages (BMDMs) and A549 epithelial cells were infected with S. rotundus and S. rugosus marked with CFSE with a multiplicity of infection [16] of 1 bacterium per cell
Summary
Segniliparus rugosus and S. rotundus are the only two species belonging to the genus Segniliparus, first identified in 2005, which is the sole genus in the family Segniliparaceae [1] This family is of great interest because it has novel and extremely long carbonchain fatty acids (mycolic acids) embedded in the cell wall [1]. The type strains of S. rugosus and S. rotundus are CDC 945T (ATCC number: BAA-974T; CIP number: 108380T) and CDC 1076T (ATCC number: BAA-972T; CIP number: 108378T), respectively [1] Both type strains of the genus Segniliparus were isolated from human sputum originally suspected as containing nontuberculous mycobacteria because the cell walls contained mycolic acids and the rod-shaped bacilli had positive acid–alcohol-fast staining [2,3,4]. The Segniliparus spp. exhibited surprisingly intense acid-fast staining, and this suggested that the mycolate structures in these unusual bacteria may exhibit novel properties
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