Early Evolution of Life: Study of Ribosome Evolution Challenges 'RNA World' Hypothesis
ScienceDaily (Mar. 12, 2012) — In the beginning -- of the ribosome, the cell's protein-building workbench -- there were ribonucleic acids, the molecules we call RNA that today perform a host of vital functions in cells. And according to a new analysis, even before the ribosome's many working parts were recruited for protein synthesis, proteins also were on the scene and interacting with RNA. This finding challenges a long-held hypothesis about the early evolution of life.
The researchers constructed an evolutionary history of the RNA and protein components of the ribosome. Older components are shown in red; more recent ones are blue. The two timelines “showed great congruence” and suggest that ribosomal proteins co-evolved with ribosomal RNAs. (Credit: Image by Derek and Gustavo Caetano-Anollés)
The study appears in the journalPLoS ONE.
The "RNA world" hypothesis, first promoted in 1986 in a paper in the journal Nature and defended and elaborated on for more than 25 years, posits that the first stages of molecular evolution involved RNA and not proteins, and that proteins (and DNA) emerged later, said University of Illinois crop sciences and Institute for Genomic Biology professor Gustavo Caetano-Anollés, who led the new study. "I'm convinced that the RNA world (hypothesis) is not correct," Caetano-Anollés said. "That world of nucleic acids could not have existed if not tethered to proteins."
The ribosome is a "ribonucleoprotein machine," a complex that can have as many as 80 proteins interacting with multiple RNA molecules, so it makes sense that this assemblage is the result of a long and complicated process of gradual co-evolution, Caetano-Anollés said. Furthermore, "you can't get RNA to perform the molecular function of protein synthesis that is necessary for the cell by itself."
Proponents of the RNA world hypothesis make basic assumptions about the evolutionary origins of the ribosome without proper scientific support, Caetano-Anollés said. The most fundamental of these assumptions is that the part of the ribosome that is responsible for protein synthesis, the peptidyl transferase center (PTC) active site, is the most ancient.
In the new analysis, Caetano-Anollés and graduate student Ajith Harish (now a postdoctoral researcher at Lund University in Sweden) subjected the universal protein and RNA components of the ribosome to rigorous molecular analyses -- mining them for evolutionary information embedded in their structures. (They also analyzed the thermodynamic properties of the ribosomal RNAs.) They used this information to generate timelines of the evolutionary history of the ribosomal RNAs and proteins.
These two, independently generated "family trees" of ribosomal proteins and ribosomal RNAs showed "great congruence" with one another, Caetano-Anollés said. Proteins surrounding the PTC, for example, were as old as the ribosomal RNAs that form that site. In fact, the PTC appeared in evolution just after the two primary subunits that make up the ribosome came together, with RNA bridges forming between them to stabilize the association.
The timelines suggest that the PTC appeared well after other regions of the protein-RNA complex, Caetano-Anollés said. This strongly suggests, first, that proteins were around before ribosomal RNAs were recruited to help build them, and second, that the ribosomal RNAs were engaged in some other task before they picked up the role of aiding in protein synthesis, he said.
"This is the crucial piece of the puzzle," Caetano-Anollés said. "If the evolutionary build-up of ribosomal proteins and RNA and the interactions between them occurred gradually, step-by-step, the origin of the ribosome cannot be the product of an RNA world. Instead, it must be the product of a ribonucleoprotein world, an ancient world that resembles our own. It appears the basic building blocks of the machinery of the cell have always been the same from the beginning of life to the present: evolving and interacting proteins and RNA molecules."
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Ribosomal History Reveals Origins of Modern Protein Synthesis
Ajith Harish¤, Gustavo Caetano-Anollés*
Evolutionary Bioinformatics Laboratory, Department of Crop Sciences, University of Illinois, Urbana-Champaign, Illinois, United States of America
Abstract
The origin and evolution of the ribosome is central to our understanding of the cellular world. Most hypotheses posit that the ribosome originated in the peptidyl transferase center of the large ribosomal subunit. However, these proposals do not link protein synthesis to RNA recognition and do not use a phylogenetic comparative framework to study ribosomal evolution. Here we infer evolution of the structural components of the ribosome. Phylogenetic methods widely used in morphometrics are applied directly to RNA structures of thousands of molecules and to a census of protein structures in hundreds of genomes. We find that components of the small subunit involved in ribosomal processivity evolved earlier than the catalytic peptidyl transferase center responsible for protein synthesis. Remarkably, subunit RNA and proteins coevolved, starting with interactions between the oldest proteins (S12 and S17) and the oldest substructure (the ribosomal ratchet) in the small subunit and ending with the rise of a modern multi-subunit ribosome. Ancestral ribonucleoprotein components show similarities to in vitro evolved RNA replicase ribozymes and protein structures in extant replication machinery. Our study therefore provides important clues about the chicken-or-egg dilemma associated with the central dogma of molecular biology by showing that ribosomal history is driven by the gradual structural accretion of protein and RNA structures. Most importantly, results suggest that functionally important and conserved regions of the ribosome were recruited and could be relics of an ancient ribonucleoprotein world.
Citation: Harish A, Caetano-Anollés G (2012) Ribosomal History Reveals Origins of Modern Protein Synthesis. PLoS ONE 7(3): e32776. doi:10.1371/journal.pone.0032776
Editor: Stephen R. Proulx, University of California Santa Barbara, United States of America
Received: November 20, 2011; Accepted: January 30, 2012; Published: March 12, 2012
Copyright: © 2012 Harish, Caetano-Anolles. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The authors thank the National Science Foundation (grants MCB-0343126 and MCB-074983607 to GCA) and the United Soybean Board for funding. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
* E-mail: gca@illinois.edu
¤ Current address: Section of Microbial Ecology, Department of Biology, Lund University, Lund, Sweden
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O MEC/SEMTEC/PNLEM não pode mais continuar aprovando livros didáticos de Biologia do ensino médio contendo fraudes e distorções de evidências científicas a favor do fato, Fato, FATO da evolução química e biológica.
V. Excia deve mandar servidores competentes e isentos, verificar o flagrante descompasso da verdade científica revelada na literatura científica desde a última parte do século 20 dessas teorias científicas, e que é OMITIDA INTENCIONALMENTE pelos autores desses livros aprovados. Denunciamos isso em 2003 e 2005, e quem foi Ministro naquela ocasião, nada fez!
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