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On the expansion of ribosomal proteins and RNAs in eukaryotes

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Abstract

While the ribosome constitution is similar in all biota, there is a considerable increase in size of both ribosomal proteins (RPs) and RNAs in eukaryotes as compared to archaea and bacteria. This is pronounced in the large (60S) ribosomal subunit (LSU). In addition to enlargement (apparently maximized already in lower eukarya), the RP changes include increases in fraction, segregation and clustering of basic residues, and decrease in hydrophobicity. The acidic fraction is lower in eukaryote as compared to prokaryote RPs. In all eukaryote groups tested, the LSU RPs have significantly higher content of basic residues and homobasic segments than the SSU RPs. The vertebrate LSU RPs have much higher sequestration of basic residues than those of bacteria, archaea and even of the lower eukarya. The basic clusters are highly aligned in the vertebrate, but less in the lower eukarya, and only within families in archaea and bacteria. Increase in the basicity of RPs, besides helping transport to the nucleus, should promote stability of the assembled ribosome as well as the association with translocons and other intracellular matrix proteins. The size and GC nucleotide bias of the expansion segments of large LSU rRNAs also culminate in the vertebrate, and should support ribosome association with the endoplasmic reticulum and other intracellular networks. However, the expansion and nucleotide bias of eukaryote LSU rRNAs do not clearly correlate with changes in ionic parameters of LSU ribosomal proteins.

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Abbreviations

aa:

Amino acid(s)

nt:

Nucleotide(s)

EO:

Ribosomal proteins found only in eukaryotes

EA:

Ribosomal proteins aligning between eukaryotes and archaea

EAB:

Ribosomal proteins aligning among eukaryotes, archaea and bacteria

ES:

Expansion segment(s) of ribosomal RNAs

LSU:

The large cytoplasmic ribosome subunit (50S in bacteria and archaea, 60S in eukaryotes)

SSU:

The small cytoplasmic ribosome subunit (30S in bacteria and archaea, 40S in eukaryotes)

sec:

A translocon component

srp:

A signal recognition particle component

PCN:

Homoionic cluster with >2 and ≥50 % ionic residues

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Acknowledgments

This study was partly supported by the U.S. National Institutes of Health Grant HD13703.

Conflict of interest

The authors declare no conflict of interest related to his study.

Note added in proof

While this survey was considered for publication, Fedyukina, Jennaro and Cavagnero (J Biol Chem 2014, M113.507707) reported differences in hydropathy and basicity of ribosomal proteins between halophile and non-halophile prokaryotes, and also presented evidence for homoionic charge segregation in these proteins [in accord with our current and previous observations (Parker et al. 2012)].

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Authors and Affiliations

  1. Department of Microbiology and Molecular Cell Sciences, University of Memphis, Memphis, TN, 38152, USA

    Michael S. Parker

  2. Department of Psychiatry, University of Cincinnati College of Medicine, Cincinnati, OH, 45263, USA

    Renu Sah & Floyd R. Sallee

  3. Department of Surgery, University of Cincinnati College of Medicine, Cincinnati, OH, 45263, USA

    Ambikaipakan Balasubramaniam

  4. Department of Pharmacology, University of Tennessee Health Sciences Center, Memphis, TN, 38163, USA

    Edwards A. Park & Steven L. Parker

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  1. Michael S. Parker
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Correspondence to Steven L. Parker.

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Parker, M.S., Sah, R., Balasubramaniam, A. et al. On the expansion of ribosomal proteins and RNAs in eukaryotes. Amino Acids 46, 1589–1604 (2014). https://doi.org/10.1007/s00726-014-1704-4

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