Structure and function of stator units of the bacterial flagellar motor

Santiveri, Mònica; Roa-Eguiara, Aritz; Kühne, Caroline; Wadhwa, Navish; Berg, Howard C.; Erhardt, Marc; Taylor, Nicholas M. I.

doi:10.1101/2020.05.15.096610

Cited by 8 publications

(8 citation statements)

References 62 publications

(42 reference statements)

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“…The torque that drives the BFM is supplied by motor-associated transmembrane protein complexes known as stators. The stator complex, an asymmetric heteroheptamer (in Escherichia coli: MotA 5 MotA 2 ) most likely acts itself as a miniature rotating nanomachine coupling ion transit to rotation ( 10 , 11 ). The stators are essential for motility, as they drive rotation, and are accessible for studies in experimental evolution due to their unambiguous role in connecting a specific environmental cue (the presence of the coupling ion) to an easily discernible phenotype (cell swimming).…”

Section: Introductionmentioning

confidence: 99%

The rapid evolution of flagellar ion selectivity in experimental populations of E. coli

et al. 2022

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Determining which cellular processes facilitate adaptation requires a tractable experimental model where an environmental cue can generate variants that rescue function. The bacterial flagellar motor (BFM) is an excellent candidate—an ancient and highly conserved molecular complex for bacterial propulsion toward favorable environments. Motor rotation is often powered by H + or Na + ion transit through the torque-generating stator subunit of the motor complex, and ion selectivity has adapted over evolutionary time scales. Here, we used CRISPR engineering to replace the native Escherichia coli H + -powered stator with Na + -powered stator genes and report the spontaneous reversion of our edit in a low-sodium environment. We followed the evolution of the stators during their reversion to H + -powered motility and used both whole-genome and RNA sequencing to identify genes involved in the cell’s adaptation. Our transplant of an unfit protein and the cells’ rapid response to this edit demonstrate the adaptability of the stator subunit and highlight the hierarchical modularity of the flagellar motor.

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Section: Introductionmentioning

confidence: 99%

The rapid evolution of flagellar ion selectivity in experimental populations of E. coli

et al. 2022

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“…However, an oddly multimeric structure of Mot-A 5 -B 2 was also recently reported in which the pioneer Berg suggested that it is the B 2 dimer that initiated and drives the rotation of A 5 , which in turn rotated the C-ring (Santiveri et al, 2020)! Even the numbers of these Mot-AB proteins vary among organisms: 11 in E.coli to 18 in H. pylori.…”

Section: A Structure-function-evolution Correlations and Quantitative...mentioning

confidence: 96%

“…Rev. Biochem., as depicted in Figures 6 & 7 ofSantiveri et al, 2020 and Figure1ofWadhwa et al., 2022, respectively): The 360 degree rotation of MotA5 is achieved in five steps of 72 degrees each. In the first half of the angular step of 72 degrees, the binding of a proton to one of the two MotB proteins (say, MotB1) at the periplasmic side induces an angular/rotary movement of 36 degrees in the earlier cycle protonated MotB2 associated-MotA pentamer, thereafter enabling the MotB2 to lose the proton to the cytoplasm.…”

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confidence: 97%

Questioning physiological rotary functionality in the bacterial flagellar system and proposing a murburn model for motility

Manoj¹,

Jacob²,

Kavdia³

et al. 2022

Preprint

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Bacterial flagellar system (BFS) was the first perceived example of a ‘natural rotary-motor” functionality, mandating the translation of a circular motion of components inside into a linear displacement of the cell body outside. This outcome is supposedly orchestrated with the following features of the BFS: (i) A chemical/electrical differential generates proton motive force (pmf, including a trans-membrane potential, TMP), which is electro-mechanically transduced by inward movement of protons via BFS. (ii) Membrane-bound roteins of BFS serve as stators and the slender filament acts as an external propeller, culminating into a hook-rod that pierces the membrane to connect to a ‘broader assembly of deterministically movable rotor’. We had disclaimed the purported pmf/TMP-based respiratory/photosynthetic physiology involving Complex V, which was also perceived as a “rotary machine” earlier. We pointed out that the murburn redox logic was operative therein. In the context of BFS, we pursue the following similar perspectives: (i) Low probability for the evolutionary attainment of an ordered/synchronized teaming of about two dozen types of proteins (assembled across five-seven distinct phases) towards the singular agendum of rotary motility. (ii) Vital redox activity (not the gambit of pmf/TMP!) powers the molecular and macroscopic activities of cells, including flagella. (iii) Flagellar movement is noted even in ambiances lacking/countering the directionality mandates sought by pmf/TMP. (iv) Structural features of BFS lack component(s) capable of harnessing/achieving pmf/TMP and functional rotation. Falling short of disproving rotability, a viable murburn model for conversion of molecular/biochemical activity into macroscopic/mechanical outcomes is proposed herein for understanding BFS-assisted motility.

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“…The torque that drives the BFM is supplied by motor-associated transmembrane protein-complexes known as stators. The stator complex, an asymmetric heteroheptamer (in E. coli: MotA 5 MotA 2 ) most likely acts itself as a miniature rotating nanomachine coupling ion transit to rotation (Deme, Johnson et al 2020, Santiveri, Roa-Eguiara et al 2020). The stators are essential for motility, as they drive rotation, and are accessible for studies in experimental evolution due to their unambiguous role in connecting a specific environmental cue (presence of the coupling ion) to an easily discernible phenotype (cell swimming).…”

Section: Introductionmentioning

confidence: 99%

The rapid evolution of flagellar ion-selectivity in experimental populations ofE. coli

Ridone

Sowa

Baker

2021

Preprint

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Motility provides a selective advantage to many bacterial species and is often achieved by rotation of flagella that propel the cell towards more favourable conditions. In most species, the rotation of the flagellum, driven by the Bacterial Flagellar Motor (BFM), is powered by H+ or Na+ ion transit through the torque-generating stator subunit of the motor complex. The ionic requirements for motility appear to have adapted to environmental changes throughout history but the molecular basis of this adaptation, and the constraints which govern the evolution of the stator proteins are unknown. Here we use CRISPR-mediated genome engineering to replace the native H+-powered stator genes of E. coli with a compatible sodium-powered stator set from V. alginolyticus and subsequently direct the evolution of the stators to revert to H+-powered motility. Evidence from whole genome sequencing indicates both flagellar- and non-flagellar-associated genes that are involved in longer-term adaptation to new power sources. Overall, transplanted Na+-powered stator genes can spontaneously incorporate novel mutations that allow H+-motility when environmental Na+ is lacking.

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Structure and function of stator units of the bacterial flagellar motor

Cited by 8 publications

References 62 publications

The rapid evolution of flagellar ion selectivity in experimental populations of E. coli

The rapid evolution of flagellar ion selectivity in experimental populations of E. coli

Questioning physiological rotary functionality in the bacterial flagellar system and proposing a murburn model for motility

The rapid evolution of flagellar ion-selectivity in experimental populations ofE. coli

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