Force per cross-sectional area from molecules to muscles: a general property of biological motors

Jean-Pierre Rospars,Nicole Meyer-Vernet

doi:10.1098/rsos.160313

Abstract

We propose to formally extend the notion of specific tension, i.e. force per cross-sectional area—classically used for muscles, to quantify forces in molecular motors exerting various biological functions. In doing so, we review and compare the maximum tensions exerted by about 265 biological motors operated by about 150 species of different taxonomic groups. The motors considered range from single molecules and motile appendages of microorganisms to whole muscles of large animals. We show that specific tensions exerted by molecular and non-molecular motors follow similar statistical distributions, with in particular, similar medians and (logarithmic) means. Over the 1019 mass (M) range of the cell or body from which the motors are extracted, their specific tensions vary as Mα with α not significantly different from zero. The typical specific tension found in most motors is about 200 kPa, which generalizes to individual molecular motors and microorganisms a classical property of macroscopic muscles. We propose a basic order-of-magnitude interpretation of this result.

Highlights

Living organisms use biological motors for various functions, which range from internal transport of ions and molecules in cells to motion of microorganisms and animals, the latter being driven by muscles
It has been known for a long time that the vertebrate striated muscles can exert maximum tensions at constant length of about 200–300 kPa which are on first
A review of the literature based on muscles of 72 species of different taxonomic groups, including mammals, birds, reptiles, amphibians, molluscs, insects and crustaceans [4] concluded that there was no significant relationship between body mass and isometric tension, isometric tension was found to be significantly higher in molluscs, crustaceans and amphibians than in other groups

Summary

Introduction

Living organisms use biological motors for various functions, which range from internal transport of ions and molecules in cells to motion of microorganisms and animals, the latter being driven by muscles. The forces developed by muscles are generally expressed as force per cross-sectional area, called specific tension or stress. It has been known for a long time that the vertebrate striated muscles can exert maximum tensions at constant length (isometric tension) of about 200–300 kPa which are on first. Approximation independent of the muscle and the body mass [1] This rule was extended to arthropod 2 muscles with values in the range 300–700 kPa [2], in some mollusc muscles stresses up to 1400 kPa were reported [3]. A review of the literature based on muscles of 72 species of different taxonomic groups, including mammals, birds, reptiles, amphibians, molluscs, insects and crustaceans [4] concluded that there was no significant relationship between body mass and isometric tension, isometric tension was found to be significantly higher in molluscs, crustaceans and amphibians than in other groups

Results

Discussion

Conclusion