Gradients in mechanotransduction of force and body weight in insects

Harris, Christian M.; Dinges, Gesa F.; Haberkorn, Anna; Gebehart, Corinna; Büschges, Ansgar; Zill, Sasha N.

doi:10.1016/j.asd.2020.100970

“…There are several similarities between the phenomena discussed in this work and proprioception in neuromuscular systems, which enables an organism to detect its velocity and position in space 32 , 33 . For example, proprioceptive feedback in the motor neurons that enervate the leg muscles in an insect maintains maximal sensitivity to different mechanical loads, allowing the insect to maintain its posture and grip when walking on the floor or the ceiling 34 .…”

Section: Discussionmentioning

confidence: 77%

Mechanosensitive recruitment of stator units promotes binding of the response regulator CheY-P to the flagellar motor

Antani

¹

,

Gupta

²

,

Lee

³

et al. 2021

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Reversible switching of the bacterial flagellar motor between clockwise (CW) and counterclockwise (CCW) rotation is necessary for chemotaxis, which enables cells to swim towards favorable chemical habitats. Increase in the viscous resistance to the rotation of the motor (mechanical load) inhibits switching. However, cells must maintain homeostasis in switching to navigate within environments of different viscosities. The mechanism by which the cell maintains optimal chemotactic function under varying loads is not understood. Here, we show that the flagellar motor allosterically controls the binding affinity of the chemotaxis response regulator, CheY-P, to the flagellar switch complex by modulating the mechanical forces acting on the rotor. Mechanosensitive CheY-P binding compensates for the load-induced loss of switching by precisely adapting the switch response to a mechanical stimulus. The interplay between mechanical forces and CheY-P binding tunes the chemotactic function to match the load. This adaptive response of the chemotaxis output to mechanical stimuli resembles the proprioceptive feedback in the neuromuscular systems of insects and vertebrates.

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“…Grouping CS based on the orientation of their long axes is suggested to unitize their functionality as they will respond to similar forces [ 1 , 25 , 31 ]. All eight elliptical CS in the femoral field are orientated at roughly 45° to the long axis of the limb (figures 1 f and 2 c ).…”

Section: Discussionmentioning

confidence: 99%

“…In addition to orientation variability, differences in CS cap sizes are present ([ 25 ], figure 2 c ). In our study, we found a size gradient in each column, with the smallest CS in the most proximal positions and the largest in the most distal positions (figures 1 f and 2 c ).…”

Section: Discussionmentioning

confidence: 99%

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Ultra high-resolution biomechanics suggest that substructures within insect mechanosensors decisively affect their sensitivity

Dinges

¹

,

Bockemühl

²

,

Iacoviello

³

et al. 2022

J. R. Soc. Interface.

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Insect load sensors, called campaniform sensilla (CS), measure strain changes within the cuticle of appendages. This mechanotransduction provides the neuromuscular system with feedback for posture and locomotion. Owing to their diverse morphology and arrangement, CS can encode different strain directions. We used nano-computed tomography and finite-element analysis to investigate how different CS morphologies within one location—the femoral CS field of the leg in the fruit fly Drosophila —interact under load. By investigating the influence of CS substructures' material properties during simulated limb displacement with naturalistic forces, we could show that CS substructures (i.e. socket and collar) influence strain distribution throughout the whole CS field. Altered socket and collar elastic moduli resulted in 5% relative differences in displacement, and the artificial removal of all sockets caused differences greater than 20% in cap displacement. Apparently, CS sockets support the distribution of distal strain to more proximal CS, while collars alter CS displacement more locally. Harder sockets can increase or decrease CS displacement depending on sensor location. Furthermore, high-resolution imaging revealed that sockets are interconnected in subcuticular rows. In summary, the sensitivity of individual CS is dependent on the configuration of other CS and their substructures.

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“…There are several similarities between the phenomena discussed in this work and proprioception in neuromuscular systems, which enables an organism to detect its velocity and position in space 31,32 . For example, proprioceptive feedback in the motor neurons that enervate the leg muscles in an insect maintains maximal sensitivity to different mechanical loads, allowing the insect to maintain its posture and grip when walking on the oor or the ceiling 33 .…”

Section: Discussionmentioning

confidence: 78%

Mechanosensitive recruitment of stator units promotes binding of the response regulator CheY-P to the flagellar motor

Antani

¹

,

Gupta

²

,

Lee

³

et al. 2021

Preprint

0

View full text Add to dashboard Cite

Reversible switching of the bacterial flagellar motor between clockwise (CW) and counterclockwise (CCW) rotation is necessary for chemotaxis, which enables cells to swim towards favorable chemical habitats. Increase in the viscous resistance to the rotation of the motor (mechanical load) inhibits switching. However, cells must maintain homeostasis in switching to navigate within environments of different viscosities. The mechanism by which the cell maintains optimal chemotactic function under varying loads is not understood. Here, we show that the flagellar motor allosterically controls the binding affinity of the chemotaxis response regulator, CheY-P, to the flagellar switch complex by modulating the mechanical forces acting on the rotor. Mechanosensitive CheY-P binding compensates for the load-induced loss of switching by precisely adapting the switch response to a mechanical stimulus. The interplay between mechanical forces and CheY-P binding tunes the chemotactic function to match the load. This adaptive response of the chemotaxis output to mechanical stimuli resembles the proprioceptive feedback in the neuromuscular systems of insects and vertebrates.

show abstract

Gradients in mechanotransduction of force and body weight in insects

Cited by 16 publications

References 73 publications

Mechanosensitive recruitment of stator units promotes binding of the response regulator CheY-P to the flagellar motor

Mechanosensitive recruitment of stator units promotes binding of the response regulator CheY-P to the flagellar motor

Ultra high-resolution biomechanics suggest that substructures within insect mechanosensors decisively affect their sensitivity

Mechanosensitive recruitment of stator units promotes binding of the response regulator CheY-P to the flagellar motor

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