Flagellin phase-dependent swimming on epithelial cell surfaces contributes to productive<i>Salmonella</i>gut colonisation

Horstmann, Julia; Zschieschang, Erik; Truschel, Theresa; Diego, Juana de; Lunelli, Michele; Rohde, Manfred; May, Tobias; Strowig, Till; Stradal, Theresia E. B.; Kolbe, Michael; Erhardt, Marc

doi:10.1111/cmi.12739

Cited by 47 publications

(44 citation statements)

References 59 publications

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“…Typhimurium has been established (22,28,43,49), and this study highlights another potential reason for this. Flagella interactions with actin were undertaken with isolated components in physiological conditions, confirming direct binding.…”

Section: Discussionmentioning

confidence: 83%

“…This is also true in near surface swimming, a biophysical process dependent on rotating flagella, which has been shown to aid cooperative colonisation by probing and facilitating docking at membrane protrusions (41,42). Additionally, the structural properties of different flagellin phase types have been shown to alter S. Typhimurium flagella rotation and near-surface swimming behaviour, with downstream effects on colonisation (43).…”

Section: Discussionmentioning

confidence: 97%

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Bacterial flagella disrupt host cell membranes and interact with cytoskeletal components

Wolfson

Elvidge

Tahoun

et al. 2020

Preprint

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Bacterial flagella have many established roles beyond swimming motility. Despite clear evidence of flagella-dependent adherence, the specificity of ligands and mechanisms of binding are still debated. In this study, the molecular basis of E. coli O157:H7 and S. Typhimurium flagella binding to epithelial cell cultures was investigated. Flagella interactions with host cell surfaces were intimate and crossed cellular boundaries as demarcated by actin and membrane labelling. SEM revealed flagella disappearing into cellular surfaces and TEM of S. Typhiumurium indicated host membrane deformation and disruption in proximity to flagella. Motor mutants of E. coli O157:H7 and S. Typhimurium caused reduced haemolysis compared to wild-type, indicating that membrane disruption was in part due to flagella rotation. Flagella from E. coli O157 (H7), EPEC O127 (H6), and S. Typhimurium (P1 & P2 flagella) were shown to bind to purified intracellular components of the actin cytoskeleton and directly increase in vitro actin polymerisation rates.

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Section: Discussionmentioning

confidence: 83%

Section: Discussionmentioning

confidence: 97%

Bacterial flagella disrupt host cell membranes and interact with cytoskeletal components

Wolfson

Elvidge

Tahoun

et al. 2020

Preprint

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“…Protein secretion into the culture supernatant was analyzed as described before 16 . Samples were fractionated under denaturizing conditions on SDS-gels (200 OD units) and immunoblotting was performed using primary a-FliC/FljB and secondary a-rabbit antibodies.…”

Section: Methodsmentioning

confidence: 99%

“…Many S. enterica serovars express either of two distinct flagellins, FliC or FljB, in a process called flagellar phase variation 14,15 . FliC-expressing bacteria display a distinct motility behavior on host cell surfaces and a competitive advantage in colonization of the intestinal epithelia compared to FljB-expressing bacteria 16 . However, while the structure of FliC has been determined previously 17 , the structure of FljB remained unknown.…”

Section: Introductionmentioning

confidence: 99%

Flagella methylation promotes bacterial adhesion and host cell invasion

Horstmann

Lunelli

Cazzola

et al. 2019

Preprint

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35The flagellum is the motility device of many bacteria and the long external filament is 36 made of several thousand copies of a single protein, flagellin. While posttranslational 37 modifications of flagellin are common among bacterial pathogens, the role of lysine 38 methylation remained unknown. Here, we show that both flagellins of Salmonella 39 enterica, FliC and FljB, are methylated at surface-exposed lysine residues. A 40 Salmonella mutant deficient in flagellin methylation was outcompeted for gut 41 colonization in a gastroenteritis mouse model. In support, methylation of flagellin 42 promoted invasion of epithelial cells in vitro. Lysine methylation increased the surface 43 hydrophobicity of flagellin and enhanced flagella-dependent adhesion of Salmonella to 44 phosphatidylcholine vesicles and epithelial cells. In summary, posttranslational flagellin 45 methylation constitutes a novel mechanism how flagellated bacteria facilitate adhesion 46 to hydrophobic host cell surfaces and thereby contributes to efficient gut colonization 47 and successful infection of the host. 48 49 50 51 52 53 54 Introduction: 57 The Gram-negative enteropathogen Salmonella enterica uses a variety of strategies to 58 successfully enter and replicate within a host. In this respect, bacterial motility enables 59 the directed movement of the bacteria towards nutrients or the target site of infection. A 60 rotary nanomachine, the flagellum, mediates motility of many bacteria, including 61 Salmonella enterica 1 . Flagella also play a central role in other infection processes, 62 involving biofilm formation, immune system modulation and adhesion 2-4 . 63 The eukaryotic plasma membrane plays an important role in the interaction of 64 flagellated bacteria with host cells during the early stages of infection 5 . The flagella of S. 65 enterica, Escherichia coli and Pseudomonas aeruginosa can function as adhesion 66 molecules 6-8 mediating the contact to various lipidic plasma membrane components, 67 including cholesterol, phospholipids, sulfolipids and the gangliosides GM1 and aGM1 9-68 12 . 69 Structurally, the flagellum consists out of three main parts: the basal body embedded 70 within the inner and outer membranes of the bacterium, a flexible linking structure -the 71 hook, and the long, external filament, which functions as the propeller of the motility 72 device 13 . The filament is formed by more than 20,000 subunits of a single protein, 73 flagellin. Many S. enterica serovars express either of two distinct flagellins, FliC or FljB, 74 in a process called flagellar phase variation 14,15 . FliC-expressing bacteria display a 75 distinct motility behavior on host cell surfaces and a competitive advantage in 76 colonization of the intestinal epithelia compared to FljB-expressing bacteria 16 . However, 77while the structure of FliC has been determined previously 17 , the structure of FljB 78 remained unknown. 130We next aligned the amino acid sequences of FljB and FliC up-and downstream of the 131 identified ɛ-N-methyl-lysine residues (...

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“…Since they utilize the propulsive force of the rotating flagella, the motility regulation is basically equivalent to the torque regulation of the flagellar motor. The bacterial flagellar motor (BFM) [1][2][3][4][5] (Fig. 1A) is a large protein complex and can rotate at up to 1,700 Hz 6 , reverse the rotation, and vary the torque depending on the load on the motor.…”

mentioning

confidence: 99%

Cooperative stator assembly of bacterial flagellar motor mediated by rotation

Ito

Nakamura²,

Toyabe³

2020

Preprint

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Cooperativity has a central place in biological regulation, providing robust and highly-sensitive regulation. The bacterial flagellar motor (BFM) implements autonomous torque regulation by the nonequilibrium structure of the stators; the stators assemble at high load and disperse at low load. It would be natural to suppose that the stator packing is affected by stator-stator interaction. However, the cooperativity among the stators has rarely been explored. Here, we evaluated the energetics and kinetics of the stator assembly by combining dynamic load control of a single motor and the trajectory analysis based on statistical mechanics. We demonstrate that the BFM exploits the dynamic cooperativity of the stator binding for the autonomous torque regulation. The cooperative assembly leads to a discontinuous phase transition and hysteresis, which may implement torque regulation with high sensitivity and robustness.

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Flagellin phase-dependent swimming on epithelial cell surfaces contributes to productiveSalmonellagut colonisation

Cited by 47 publications

References 59 publications

Bacterial flagella disrupt host cell membranes and interact with cytoskeletal components

Bacterial flagella disrupt host cell membranes and interact with cytoskeletal components

Flagella methylation promotes bacterial adhesion and host cell invasion

Cooperative stator assembly of bacterial flagellar motor mediated by rotation

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