Abstract
BackgroundPost-translational glycosylation of the flagellin protein is relatively common among Gram-negative bacteria, and has been linked to several phenotypes, including flagellar biosynthesis and motility, biofilm formation, host immune evasion and manipulation and virulence. However to date, despite extensive physiological and genetic characterization, it has never been reported for the peritrichously flagellate Enterobacteriaceae.ResultsUsing comparative genomic approaches we analyzed 2,000 representative genomes of Enterobacteriaceae, and show that flagellin glycosylation islands are relatively common and extremely versatile among members of this family. Differences in the G + C content of the FGIs and the rest of the genome and the presence of mobile genetic elements provide evidence of horizontal gene transfer occurring within the FGI loci. These loci therefore encode highly variable flagellin glycan structures, with distinct sugar backbones, heavily substituted with formyl, methyl, acetyl, lipoyl and amino groups. Additionally, an N-lysine methylase, FliB, previously identified only in the enterobacterial pathogen Salmonella enterica, is relatively common among several distinct taxa within the family. These flagellin methylase island loci (FMIs), in contrast to the FGI loci, appear to be stably maintained within these diverse lineages.ConclusionsThe prevalence and versatility of flagellin modification loci, both glycosylation and methylation loci, suggests they play important biological roles among the Enterobacteriaceae.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2735-x) contains supplementary material, which is available to authorized users.
Highlights
Post-translational glycosylation of the flagellin protein is relatively common among Gram-negative bacteria, and has been linked to several phenotypes, including flagellar biosynthesis and motility, biofilm formation, host immune evasion and manipulation and virulence
Flagellin ornamentation loci are widespread among the Enterobacteriaceae The complete and draft genomes of 2,000 strains belonging to the family Enterobacteriaceae, encompassing 50 distinct genera, were screened for the presence of inserts within their flagellin loci (Additional file 1: Table S1)
307 (15.4 %) contained hallmarks of flagellin glycosylation islands (FGIs), including genes coding for glycosyltransferases and sugar biosynthetic enzymes (Additional file 1: Table S2)
Summary
Post-translational glycosylation of the flagellin protein is relatively common among Gram-negative bacteria, and has been linked to several phenotypes, including flagellar biosynthesis and motility, biofilm formation, host immune evasion and manipulation and virulence. Other pathogens attach sugar chains to the flagellin protein, resulting in a flagellin with distinct antigenic properties, in a process termed posttranslational flagellin glycosylation [13]. This phenomenon has been observed in a number of Gram-negative bacteria, including the human and animal pathogens Campylobacter, Aeromonas and Pseudomonas aeruginosa, as well as the phytopathogen Pseudomonas syringae [13,14,15,16]. A number of additional functions have been ascribed to flagellin glycosylation, in pathogenic microorganisms, including surface recognition, adhesion, biofilm formation, mimicry of host cell surface glycans and virulence [13, 17, 18]
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