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Journal of Molecular Evolution

, Volume 86, Issue 8, pp 581–592 | Cite as

Circular Permutation Obscures Universality of a Ribosomal Protein

  • Nicholas A. Kovacs
  • Petar I. Penev
  • Amitej Venapally
  • Anton S. Petrov
  • Loren Dean Williams
Original Article

Abstract

Functions, origins, and evolution of the translation system are best understood in the context of unambiguous and phylogenetically based taxonomy and nomenclature. Here, we map ribosomal proteins onto the tree of life and provide a nomenclature for ribosomal proteins that is consistent with phylogenetic relationships. We have increased the accuracy of homology relationships among ribosomal proteins, providing a more informative picture of their lineages. We demonstrate that bL33 (bacteria) and eL42 (archaea/eukarya) are homologs with common ancestry and acute similarities in sequence and structure. Their similarities were previously obscured by circular permutation. The most likely mechanism of permutation between bL33 and eL42 is duplication followed by fusion and deletion of both the first and last β-hairpins. bL33 and eL42 are composed of zinc ribbon protein folds, one of the most common zinc finger fold-groups of, and most frequently observed in translation-related domains. Bacterial-specific ribosomal protein bL33 and archaeal/eukaryotic-specific ribosomal protein eL42 are now both assigned the name of uL33, indicating a universal ribosomal protein. We provide a phylogenetic naming scheme for all ribosomal proteins that is based on phylogenetic relationships to be used as a tool for studying the systemics, evolution, and origins of the ribosome.

Keywords

Protein evolution Zinc ribbon Zinc finger Ribosome Tree of life Translation 

Abbreviations

DCC

Decoding center

PTC

Peptidyl transferase center

SSU

Small subunit

LSU

Large subunit

rRNA

Ribosomal RNA

rProtein

Ribosomal protein

PASE

Pairing adjusted sequence entropy

E. coli

Escherichia coli

EsCo

Escherichia coli

T. Thermophilus

Thermus thermophilus

ThTh

Thermus thermophilus

H. marismortui

Haloarcula marismortui

HaMa

Haloarcula marismortui

P. furiosus

Pyrococcus furiosus

PyFu

Pyrococcus furiosus

S. cerevisiae

Saccharomyces cerevisiae

SaCe

Saccharomyces cerevisiae

T. thermophila

Tetrahymena thermophila

TeTh

Tetrahymena thermophila

D. melanogaster

Drosophila melanogaster

DrMe

Drosophila melanogaster

H. sapiens

Homo sapiens

HoSa

Homo sapiens

P. falciparum

Plasmodium falciparum

PlFa

Plasmodium falciparum

T. brucei

Trypanosoma brucei

TrBr

Trypanosoma brucei

Notes

Acknowledgements

The authors would like to thank Dr. Hyman Hartman and Dr. Nenad Ban for discussions. The authors declare that they have no competing interests. This work was supported by National Aeronautics and Space Administration (Grant Numbers NNX16AJ28G and NNX16AJ29G) and NSF Grant 1713995.

Author Contributions

NAK, PIP, ASP, and LDW conceived the study. NAK, PIP, and AV collected and analyzed the data. NAK and PIP generated all the figures and tables. NAK, PIP, ASP, and LDW wrote the manuscript.

Supplementary material

239_2018_9869_MOESM1_ESM.pdf (43.2 mb)
Additional file 1: Supplementary Material for Circular Permutation Obscures Universality of a Ribosomal Protein (PDF 44246 KB)
239_2018_9869_MOESM2_ESM.aln (10 kb)
Datasets 1: Alignments of 67 bacterial species (ALN 9 KB)
239_2018_9869_MOESM3_ESM.aln (12 kb)
Datasets 2: Alignments of 52 archaeal species (ALN 12 KB)
239_2018_9869_MOESM4_ESM.aln (9 kb)
Datasets 3: Alignments of 30 eukaryotic species (ALN 8 KB)
239_2018_9869_MOESM5_ESM.aln (68 kb)
Datasets 4: Alignments of bL33 and aL42 for all species (ALN 67 KB)
239_2018_9869_MOESM6_ESM.aln (69 kb)
Datasets 5: Alignments of bL33 and aL42 for all species, bacterial sequences (bL33CP) have been permuted as described in the text (ALN 69 KB)

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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Chemistry and BiochemistryGeorgia Institute of TechnologyAtlantaUSA
  2. 2.School of Biological SciencesGeorgia Institute of TechnologyAtlantaUSA

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