History of the ribosome and the origin of translation
Anton S. Petrov a,1, Burak Gulen a, Ashlyn M. Norris a, Nicholas A. Kovacs a, Chad R. Bernier a, Kathryn A. Lanier a, George E. Fox b, Stephen C. Harvey c, Roger M. Wartell c, Nicholas V. Hud a, and Loren Dean Williams a,1
aSchool of Chemistry and Biochemistry, Georgia Institute of Technology, Atlanta, GA 30332;
bDepartment of Biology and Biochemistry, University of Houston, Houston, TX, 77204;
cSchool of Biology, Georgia Institute of Technology, Atlanta, GA 30332
Edited by David M. Hillis, The University of Texas at Austin, Austin, TX, and approved November 6, 2015 (received for review May 18, 2015)
Significance
The ribosome, in analogy with a tree, contains a record of its history, spanning 4 billion years of life on earth. The information contained within ribosomes connects us to the prehistory of biology. Details of ribosomal RNA variation, observed by comparing three-dimensional structures of ribosomes across the tree of life, form the basis of our molecular-level model of the origins and evolution of the translational system. We infer many steps in the evolution of translation, mapping out acquisition of structure and function, revealing much about how modern biology originated from ancestral chemical systems.
Abstract
We present a molecular-level model for the origin and evolution of the translation system, using a 3D comparative method. In this model, the ribosome evolved by accretion, recursively adding expansion segments, iteratively growing, subsuming, and freezing the rRNA. Functions of expansion segments in the ancestral ribosome are assigned by correspondence with their functions in the extant ribosome. The model explains the evolution of the large ribosomal subunit, the small ribosomal subunit, tRNA, and mRNA. Prokaryotic ribosomes evolved in six phases, sequentially acquiring capabilities for RNA folding, catalysis, subunit association, correlated evolution, decoding, energy-driven translocation, and surface proteinization. Two additional phases exclusive to eukaryotes led to tentacle-like rRNA expansions. In this model, ribosomal proteinization was a driving force for the broad adoption of proteins in other biological processes. The exit tunnel was clearly a central theme of all phases of ribosomal evolution and was continuously extended and rigidified. In the primitive noncoding ribosome, proto-mRNA and the small ribosomal subunit acted as cofactors, positioning the activated ends of tRNAs within the peptidyl transferase center. This association linked the evolution of the large and small ribosomal subunits, proto-mRNA, and tRNA.
RNA evolution translation origin of life A-minor interactions
Footnotes
1To whom correspondence may be addressed.
Email: anton.petrov{at}biology.gatech.edu or
loren.williams{at}chemistry.gatech.edu.
Author contributions: A.S.P., C.R.B., G.E.F., S.C.H., R.M.W., N.V.H., and L.D.W. designed research; A.S.P., B.G., A.M.N., N.A.K., and K.A.L. performed research; C.R.B. contributed new reagents/analytic tools; A.S.P., B.G., A.M.N., N.A.K., C.R.B., and K.A.L. analyzed data; A.S.P. and B.G. prepared the figures; and A.S.P., G.E.F., S.C.H., R.M.W., N.V.H., and L.D.W. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1509761112/-/DCSupplemental.
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