Abstract
Lactobacillus ruminis is one of at least twelve motile but poorly characterized species found in the genus Lactobacillus. Of these, only L. ruminis has been isolated from mammals, and this species may be considered as an autochthonous member of the gastrointestinal microbiota of humans, pigs and cows. Nine L. ruminis strains were investigated here to elucidate the biochemistry and genetics of Lactobacillus motility. Six strains isolated from humans were non-motile while three bovine isolates were motile. A complete set of flagellum biogenesis genes was annotated in the sequenced genomes of two strains, ATCC25644 (human isolate) and ATCC27782 (bovine isolate), but only the latter strain produced flagella. Comparison of the L. ruminis and L. mali DSM20444T motility loci showed that their genetic content and gene-order were broadly similar, although the L. mali motility locus was interrupted by an 11.8 Kb region encoding rhamnose utilization genes that is absent from the L. ruminis motility locus. Phylogenetic analysis of 39 motile bacteria indicated that Lactobacillus motility genes were most closely related to those of motile carnobacteria and enterococci. Transcriptome analysis revealed that motility genes were transcribed at a significantly higher level in motile L. ruminis ATCC27782 than in non-motile ATCC25644. Flagellin proteins were isolated from L. ruminis ATCC27782 and from three other Lactobacillus species, while recombinant flagellin of aflagellate L. ruminis ATCC25644 was expressed and purified from E. coli. These native and recombinant Lactobacillus flagellins, and also flagellate L. ruminis cells, triggered interleukin-8 production in cultured human intestinal epithelial cells in a manner suppressed by short interfering RNA directed against Toll-Like Receptor 5. This study provides genetic, transcriptomic, phylogenetic and immunological insights into the trait of flagellum-mediated motility in the lactobacilli.
Highlights
Bacterial flagella are long, thin, proteinaceous structures that form rigid helices which rotate in a counterclockwise direction to propel the cell forward [1,2]
The filament of the bacterial flagellum is composed of polymers of a protein called flagellin, a microbe associated molecular pattern (MAMP) that is recognized by toll-like receptor 5 (TLR5) of the host [3], and which activates the nuclear factor-kb (NFkb) signaling-pathway in epithelial and innate immune cells [4,5,6]
Among the accepted motile species found in the L. salivarius clade, most have been isolated from environmental sources (Table S1), where the advantages of motility for nutrient acquisition and niche colonisation justify the associated metabolic costs of flagellum production and energization
Summary
Thin, proteinaceous structures that form rigid helices which rotate in a counterclockwise direction to propel the cell forward [1,2]. The filament of the bacterial flagellum is composed of polymers of a protein called flagellin, a microbe associated molecular pattern (MAMP) that is recognized by toll-like receptor 5 (TLR5) of the host [3], and which activates the nuclear factor-kb (NFkb) signaling-pathway in epithelial and innate immune cells [4,5,6]. The production of flagella requires a substantial investment of resources by the bacterium, with ,0.1% and ,2% of the cell’s energy devoted to flagellum rotation and biosynthesis respectively [12]. For this reason, and presumably to avoid stimulating immune responses, some species, such as Listeria monocytogenes suppress motility gene expression in vivo [13,14]
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