Abstract

In the past few decades, studies on translation have converged towards the metaphor of a “ribosome nanomachine”; they also revealed intriguing ribosome properties challenging this view. Many studies have shown that to perform an accurate protein synthesis in a fluctuating cellular environment, ribosomes sense, transfer information and even make decisions. This complex “behaviour” that goes far beyond the skills of a simple mechanical machine has suggested that the ribosomal protein networks could play a role equivalent to nervous circuits at a molecular scale to enable information transfer and processing during translation. We analyse here the significance of this analogy and establish a preliminary link between two fields: ribosome structure-function studies and the analysis of information processing systems. This cross-disciplinary analysis opens new perspectives about the mechanisms of information transfer and processing in ribosomes and may provide new conceptual frameworks for the understanding of the behaviours of unicellular organisms.

Highlights

  • More than twenty years ago, Dennis Bray proposed, on the basis of his analysis of bacterial chemotaxis, the idea that proteins may constitute computational elements in cells [1]. This seminal work suggested that “in unicellular organisms, protein-based circuits act in place of a nervous system to control the behaviour” and that “because of the high degree of interconnection, systems of interacting proteins act as neural networks trained by the evolution to respond appropriately to patterns of extracellular stimuli” [1]

  • He noticed that an important difference with true neural networks is “the wiring of these networks depends on diffusion-limited encounters between molecules and for this and other reasons, they have unique features not found in conventional computer-based neural network”

  • It has been proposed that these networks may play at a molecular scale, a role analogous to a sensory-motor nervous system, to assist and synchronize protein biosynthesis during translation

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Summary

Introduction

More than twenty years ago, Dennis Bray proposed, on the basis of his analysis of bacterial chemotaxis, the idea that proteins may constitute computational elements in cells [1] This seminal work suggested that “in unicellular organisms, protein-based circuits act in place of a nervous system to control the behaviour” and that “because of the high degree of interconnection, systems of interacting proteins act as neural networks trained by the evolution to respond appropriately to patterns of extracellular stimuli” [1]. This study has shown that r-protein networks form complex circuits that differ from most known protein networks, in that they remain physically interconnected These networks displayed some features of communication networks and an intriguing functional analogy with sensory-motor circuits found in simple organisms. This cross-disciplinary analysis opens new perspectives about the mechanisms of information transfer and processing in ribosomes and may provide new conceptual frameworks for the understanding of the behaviours of unicellular organisms

An Extensive Flow of Information
Ribosome Choreography during Protein Biosynthesis
Ribosome Heterogeneity and Open Questions
Ribosome Behaviour
The r-Protein–Neuron Equivalence
Sensing the Ribosomal Functional Sites
Molecular Synapses and Wires
Nervous-Like Circuits in the Ribosome?

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