Evolution of ribosomal protein network architectures

Abstract

To perform an accurate protein synthesis, ribosomes accomplish complex tasks involving the long-range communication between its functional centres such as the peptidyl transfer centre, the tRNA bindings sites and the peptide exit tunnel. How information is transmitted between these sites remains one of the major challenges in current ribosome research. Many experimental studies have revealed that some r-proteins play essential roles in remote communication and the possible involvement of r-protein networks in these processes have been recently proposed. Our phylogenetic, structural and mathematical study reveals that of the three kingdom’s r-protein networks converged towards non-random graphs where r-proteins collectively coevolved to optimize interconnection between functional centres. The massive acquisition of conserved aromatic residues at the interfaces and along the extensions of the newly connected eukaryotic r-proteins also highlights that a strong selective pressure acts on their sequences probably for the formation of new allosteric pathways in the network.

Towards the Idea of Molecular Brains

“…A recent interdisciplinary study has shown how r-protein networks have evolved toward a growing complexity through the coevolution of the r-protein extensions and the increasing number of connexions [ 46 ]. This revealed that network expansion is produced by the collective (co)-evolution of r-proteins leading to an asymmetrical evolution of the two subunits.…”

“…On the other hand, new types of molecular networks have been recently discovered in the ribosomes [ 44 , 45 , 46 ]. These “neuron-like” ribosomal protein (r-protein) networks display new properties compared to other “classical” biological networks [ 47 ]: they form mostly permanent connections through long disordered filaments and phylogenetically conserved tiny interfaces that have been compared to “molecular synapses”.…”

“…These “neuron-like” ribosomal protein (r-protein) networks display new properties compared to other “classical” biological networks [ 47 ]: they form mostly permanent connections through long disordered filaments and phylogenetically conserved tiny interfaces that have been compared to “molecular synapses”. These networks have evolved to optimise the interconnections between ribosome functional centres, thus presenting a “functional” analogy with simple sensorimotor networks [ 46 ] ( Figure 2 ). They also probably use a new type of allosteric mechanism involving key aromatic amino acids.…”

Spatially Enriched Paralog Rearrangements Argue Functionally Diverse Ribosomes Arise during Cold Acclimation in Arabidopsis

“…The functional centers of ribosomes actively communicate to perform ribosomal functions. The communication among functional centers is optimized by the coevolution of a non-random RP network [89]. These RP graphs harbor specific neuron-like properties that led to the realization of RPs being instrumental in the process of information transfer across ribosomal complexes [90,91].…”

Untitled

“…These proteins are colocalized in bacterial and archaeal ribosomes and have very similar structures, related by a circular permutation. Here we refer to them with their classical domain names bL33 and aL42 [90] for clarity, however we and others have proposed that they should share the name uL33 [88,91]. We probed whether TwinCons can detect the ancestral relationship within the composite alignment of bL33 and aL42.…”