Computing the origin and evolution of the ribosome from its structure — Uncovering processes of macromolecular accretion benefiting synthetic biology

Abstract

Accretion occurs pervasively in nature at widely different timeframes. The process also manifests in the evolution of macromolecules. Here we review recent computational and structural biology studies of evolutionary accretion that make use of the ideographic (historical, retrodictive) and nomothetic (universal, predictive) scientific frameworks. Computational studies uncover explicit timelines of accretion of structural parts in molecular repertoires and molecules. Phylogenetic trees of protein structural domains and proteomes and their molecular functions were built from a genomic census of millions of encoded proteins and associated terminal Gene Ontology terms. Trees reveal a ‘metabolic-first’ origin of proteins, the late development of translation, and a patchwork distribution of proteins in biological networks mediated by molecular recruitment. Similarly, the natural history of ancient RNA molecules inferred from trees of molecular substructures built from a census of molecular features shows patchwork-like accretion patterns. Ideographic analyses of ribosomal history uncover the early appearance of structures supporting mRNA decoding and tRNA translocation, the coevolution of ribosomal proteins and RNA, and a first evolutionary transition that brings ribosomal subunits together into a processive protein biosynthetic complex. Nomothetic structural biology studies of tertiary interactions and ancient insertions in rRNA complement these findings, once concentric layering assumptions are removed. Patterns of coaxial helical stacking reveal a frustrated dynamics of outward and inward ribosomal growth possibly mediated by structural grafting. The early rise of the ribosomal ‘turnstile’ suggests an evolutionary transition in natural biological computation. Results make explicit the need to understand processes of molecular growth and information transfer of macromolecules.

Piecemeal Buildup of the Genetic Code, Ribosomes, and Genomes from Primordial tRNA Building Blocks

“…We note that in most cases the recruited parts become physically associated with the growing system, with b of Equation (2) representing the growing system and a the accreted part. Examples of accretion of these kinds are macromolecular complexes such as the ATP synthases and the ribosome [25,26]. The F-type and A/V-type synthases are multi-subunit complexes responsible for membrane-coupled energy conversion reactions.…”

“…Using phylogenomic methods we have shown that the synthase complexes developed gradually by addition of structural domains, starting with the ring structures of the rotating head, followed by the central stalk (the axle), and ending with the structures that regulate their motion (the stators) [25]. Similarly, the ribosome has been shown to grow in evolution by addition of helical segments to the evolving molecules [26], complying with the principle of continuity that sustains evolutionary thinking and explaining the formation of highly sophisticated macromolecular machinery.…”

“…The structural makeup of the ribosome provides information about its possible growth by covalent joining of primordial tRNA pieces [26]. Identification of putative insertions of “branch” helices onto preexisting coaxially stacked “trunk” helices in crystallographic models of the ribosome showed that not all insertions support the outward and gradual growth of ribosomal structures [88].…”

Commentary: History of the ribosome and the origin of translation

“…Cladistic methodology has been successfully applied to the study of molecular evolution. For example, phylogenetic characters describing the length and stability of RNA helical segments or the abundance of protein structural domains in genomes have been used to build phylogenetic trees of molecules and proteomes, respectively (reviewed in Caetano-Anollés and Caetano-Anollés, 2015a). These methodologies have been recently extended to study the origin and evolution of the ribosome (Harish and Caetano-Anollés, 2012).…”

“…The inset describes a network interaction diagram of the same junction in a different structure, again showing the h33-h34 stacked helices (redrawn from Lescoute and Westhof, 2006). Any claim that the coaxially stacked h33-h34 is a branch that “caps” an older h32 trunk is ad hoc , erases the original IF signature, and introduces a serious ambiguity (see Figure 10C and discussion in Caetano-Anollés and Caetano-Anollés, 2015a), which defeats the entire algorithmic implementation. (D) Road blocks to outward growth create multiple ribosomal origins.…”