Bacterial Flagella: Twist and Stick, or Dodge across the Kingdoms

Rossez, Yannick; Wolfson, E; Holmes, Ashleigh; Gally, David L.; Holden, Nicola

doi:10.1371/journal.ppat.1004483

Cited by 157 publications

(133 citation statements)

References 108 publications

Supporting

Mentioning

129

Contrasting

Unclassified

Order By: Relevance

“…Flagellum-promoted swimming motility is often a hallmark characteristic of planktonic bacteria in their exponential growth phase [49, 50]. To study the role of the flagellum in NET formation we used flagellum-deficient PAO1 and PAK strains (PAO1 fliC and PAK flgC ).…”

Section: Resultsmentioning

confidence: 99%

Swimming Motility Mediates the Formation of Neutrophil Extracellular Traps Induced by Flagellated Pseudomonas aeruginosa

et al. 2016

View full text Add to dashboard Cite

Pseudomonas aeruginosa is an opportunistic pathogen causing severe infections often characterized by robust neutrophilic infiltration. Neutrophils provide the first line of defense against P. aeruginosa. Aside from their defense conferred by phagocytic activity, neutrophils also release neutrophil extracellular traps (NETs) to immobilize bacteria. Although NET formation is an important antimicrobial process, the details of its mechanism are largely unknown. The identity of the main components of P. aeruginosa responsible for triggering NET formation is unclear. In this study, our focus was to identify the main bacterial factors mediating NET formation and to gain insight into the underlying mechanism. We found that P. aeruginosa in its exponential growth phase promoted strong NET formation in human neutrophils while its NET-inducing ability dramatically decreased at later stages of bacterial growth. We identified the flagellum as the primary component of P. aeruginosa responsible for inducing NET extrusion as flagellum-deficient bacteria remained seriously impaired in triggering NET formation. Purified P. aeruginosa flagellin, the monomeric component of the flagellum, does not stimulate NET formation in human neutrophils. P. aeruginosa-induced NET formation is independent of the flagellum-sensing receptors TLR5 and NLRC4 in both human and mouse neutrophils. Interestingly, we found that flagellar motility, not flagellum binding to neutrophils per se, mediates NET release induced by flagellated bacteria. Immotile, flagellar motor-deficient bacterial strains producing paralyzed flagella did not induce NET formation. Forced contact between immotile P. aeruginosa and neutrophils restored their NET-inducing ability. Both the motAB and motCD genetic loci encoding flagellar motor genes contribute to maximal NET release; however the motCD genes play a more important role. Phagocytosis of P. aeruginosa and superoxide production by neutrophils were also largely dependent upon a functional flagellum. Taken together, the flagellum is herein presented for the first time as the main organelle of planktonic bacteria responsible for mediating NET release. Furthermore, flagellar motility, rather than binding of the flagellum to flagellum-sensing receptors on host cells, is required for P. aeruginosa to induce NET release.

show abstract

Section: Resultsmentioning

confidence: 99%

Swimming Motility Mediates the Formation of Neutrophil Extracellular Traps Induced by Flagellated Pseudomonas aeruginosa

et al. 2016

View full text Add to dashboard Cite

show abstract

“…Another motif of FliC, called flgII-28, is recognized independently of FLS2 by tomato and other solanaceous plants (but not by Arabidopsis), most likely via another pattern recognition receptor (24). Since these discoveries, it has been speculated that bacteria may escape recognition by variation or modification (decoration, e.g., glycosylation) of key flagellin residues, downregulation of flagellin expression, loss of the flagellum, or bacteria-driven enzymatic degradation of flagellin (111). Variations in Flg22 residues required for FLS2-mediated recognition are observed in xanthomonads, allowing evasion of FLS2-mediated immunity (128).…”

Section: Evasion Of Microbe-associated Molecular Pattern Recognition mentioning

confidence: 99%

Using Ecology, Physiology, and Genomics to Understand Host Specificity inXanthomonas

Jacques

Arlat

Boulanger

et al. 2016

Annu. Rev. Phytopathol.

163

139

View full text Add to dashboard Cite

How pathogens coevolve with and adapt to their hosts are critical to understanding how host jumps and/or acquisition of novel traits can lead to new disease emergences. The Xanthomonas genus includes Gram-negative plant-pathogenic bacteria that collectively infect a broad range of crops and wild plant species. However, individual Xanthomonas strains usually cause disease on only a few plant species and are highly adapted to their hosts, making them pertinent models to study host specificity. This review summarizes our current understanding of the molecular basis of host specificity in the Xanthomonas genus, with a particular focus on the ecology, physiology, and pathogenicity of the bacterium. Despite our limited understanding of the basis of host specificity, type III effectors, microbe-associated molecular patterns, lipopolysaccharides, transcriptional regulators, and chemotactic sensors emerge as key determinants for shaping host specificity.

show abstract

“…Cultureindependent bioinformatic analysis could be used as a tool in finding candidate SFB functional genes. There are a large number of publications regarding flagellummediated adherence (15), and some studies demonstrated that flagellin has a role in regulating Th17 cell differentiation (16,17), IgA plasma cell generation, and Th1 functions (18). Comparative genomic analyses indicated that there is a set of genes that encode flagellin proteins within SFB genomes (19,20) and that the homology between SFB flagellin proteins is conserved in comparison to the most closely related Clostridium species (19).…”

mentioning

confidence: 99%

Host Specificity of Flagellins from Segmented Filamentous Bacteria Affects Their Patterns of Interaction with Mouse Ileal Mucosal Proteins

Chen

Yin

Wang

et al. 2017

Appl Environ Microbiol

View full text Add to dashboard Cite

Segmented filamentous bacteria (SFB) are known modulators of the mammalian immune system. Currently, the technology for investigating SFB culture in vitro is immature, and as a result, the mechanisms of SFB colonization and immune regulation are not yet fully elucidated. In this study, we investigated the gene diversity and host specificity of SFB flagellin genes. The fliC1 and fliC2 genes are relatively conserved, while the fliC3 and fliC4 genes are more variable, especially at the central and C-terminal regions. Host specificity analysis demonstrated that the fliC1 genes do not cluster together based on the host organism, whereas the fliC3 and fliC4 genes were host specific at the nucleotide and deduced amino acid levels. SFB flagellin protein expression in the ileum mucosa and cecal contents was detected by using fluorescence in situ hybridization (FISH) combined with immunohistochemical (IHC) analysis, immunoblotting, and liquid chromatography-tandem mass spectrometry (LC-MS/MS). Although the purified SFB FliC3 protein originating from both mouse and rat was able to activate Toll-like receptor 5 (TLR5)-linked NF-B signaling, no host specificity was observed. Interestingly, the patterns of interaction with mouse ileum mucosal proteins were different for mouse FliC3 (mFliC3) and rat FliC3 (rFliC3). Gene Ontology (GO) and KEGG analyses indicated that more adherence-related proteins interacted with mFliC3, while more lysosome-and proteolysis-related proteins interacted with rFliC3. In vitro degradation experiments indicated that the stability of rFliC3 was lower than that of mFliC3 when they were incubated with mouse ileum mucosal proteins. In summary, the gene diversity and host specificity of SFB flagellin genes were investigated, and SFB flagellin expression was detected in gut samples.IMPORTANCE Since SFB genomes contain only one copy of each FliC gene, the diversity of FliC is representative of SFB strain diversity. Currently, little is known regarding the diversity and specificity of members of the group of SFB. The work presented herein demonstrates that select SFB strains, exhibiting unique FliC patterns, are present in a variety of mammalian hosts. SFB fliC genes were found to interact with a number of unique targets, providing further evidence for SFB host selection. Together, this work represents a major advancement in identifying SFB and delineating how members of the group of SFB interact with the host. Future examination of FliC genes will likely enhance our knowledge of intestinal colonization by the gut microbiota.KEYWORDS segmented filamentous bacteria, flagellin, host specificity, gene diversity, ileum mucosal proteins

show abstract

Bacterial Flagella: Twist and Stick, or Dodge across the Kingdoms

Cited by 157 publications

References 108 publications

Swimming Motility Mediates the Formation of Neutrophil Extracellular Traps Induced by Flagellated Pseudomonas aeruginosa

Swimming Motility Mediates the Formation of Neutrophil Extracellular Traps Induced by Flagellated Pseudomonas aeruginosa

Using Ecology, Physiology, and Genomics to Understand Host Specificity inXanthomonas

Host Specificity of Flagellins from Segmented Filamentous Bacteria Affects Their Patterns of Interaction with Mouse Ileal Mucosal Proteins

Contact Info

Product

Resources

About