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.2024 Sep 11;15(9):1195.
doi: 10.3390/genes15091195.

A Proposal for the RNAome at the Dawn of the Last Universal Common Ancestor

Affiliations

A Proposal for the RNAome at the Dawn of the Last Universal Common Ancestor

Miryam Palacios-Pérez et al. Genes (Basel)..

Abstract

From the most ancient RNAs, which followed an RNY pattern and folded into small hairpins, modern RNA molecules evolved by two different pathways, dubbed Extended Genetic Code 1 and 2, finally conforming to the current standard genetic code. Herein, we describe the evolutionary path of the RNAome based on these evolutionary routes. In general, all the RNA molecules analysed contain portions encoded by both genetic codes, but crucial features seem to be better recovered by Extended 2 triplets. In particular, the whole Peptidyl Transferase Centre, anti-Shine-Dalgarno motif, and a characteristic quadruplet of the RNA moiety of RNAse-P are clearly unveiled. Differences between bacteria and archaea are also detected; in most cases, the biological sequences are more stable than their controls. We then describe an evolutionary trajectory of the RNAome formation, based on two complementary evolutionary routes: one leading to the formation of essentials, while the other complemented the molecules, with the cooperative assembly of their constituents giving rise to modern RNAs.

Keywords: FUCA; LUCA; RNA; RNY code; evolution of genetic code; extended genetic codes 1 and 2; primeval genetic code.

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Conflict of interest statement

The authors declare no conflicts of interest. All content, analysis, and conclusions presented in this paper are entirely original.

Figures

Figure 1
Figure 1
Logo sequences and 3D structures of ExGCs-encoded 5S rRNA. In (A) the Ex1-encoded 5S rRNAs from arc., Ex1-encoded portion (salmon) is superimposed with current 5S rRNA (1ffk purple, TM = 0.90526); in (B) the Ex2-encoded 5S rRNA from arc, Ex2-encoded portion (sky blue) is superimposed with current 5S rRNA (1ffk purple, TM = 0.91248); in (C) the Ex1-encoded 5S rRNA from bac., Ex1-encoded portion (salmon) is superimposed with current 5S rRNA (5gaf purple, TM = 0.89894); in (D) the Ex2-encoded 5S rRNA from bac., Ex2-encoded portion (sky blue) is superimposed with current 5S rRNA (5gaf purple, TM = 0.86637).
Figure 2
Figure 2
Subalignments (subalns.) extracted from the MSA of the ExGCs-encoded portion of 16S rRNAs anti-SD sequence context and the conservation profiles of the whole MSAs (grey strip below each one). In (A) the subaln. from arc. Ex1-encoded 16S rRNA, in (B) the subaln. from arc. Ex2-encoded 16S rRNA, in (C) the subaln. from bac. Ex1-encoded 16S rRNA, in (D) the subaln. from bac. Ex2-encoded 16S rRNA. In bacterial subalns., the antiSD sequence is marked by a red rectangle and the two essential adenines by a green rectangle.
Figure 3
Figure 3
Subalignments (subalns.) extracted from the MSA of the ExGCs-encoded portion of 23S rRNAs PTC and the conservation profiles of the whole MSAs (grey strip below each one). In (A) the subaln. from archaeal Ex1-encoded 23S rRNA, in (B) the subaln. from archaeal Ex2-encoded 23S rRNA, in (C) the subaln. from bacterial Ex1-encoded 23S rRNA, in (D) the subaln. from bacterial Ex2-encoded 23S rRNA. In all subalns., the PTC sequence is marked by a red rectangle, with the two essential nucleotides G2447 and A2451 by green rectangles.
Figure 3
Figure 3
Subalignments (subalns.) extracted from the MSA of the ExGCs-encoded portion of 23S rRNAs PTC and the conservation profiles of the whole MSAs (grey strip below each one). In (A) the subaln. from archaeal Ex1-encoded 23S rRNA, in (B) the subaln. from archaeal Ex2-encoded 23S rRNA, in (C) the subaln. from bacterial Ex1-encoded 23S rRNA, in (D) the subaln. from bacterial Ex2-encoded 23S rRNA. In all subalns., the PTC sequence is marked by a red rectangle, with the two essential nucleotides G2447 and A2451 by green rectangles.
Figure 4
Figure 4
Logo sequences, conservation profiles of the whole MSAs (grey strip below each logo), and 3D structures of ExGCs-encoded 6S rRNAs. In (A) the Ex1-encoded 6S rRNA from bac., Ex1-encoded portion (salmon) is superimposed with current 5S rRNA (4ue4 purple, TM = 0.24615); in (B) the Ex2-encoded 5S rRNA from bac., Ex2-encoded portion (sky blue) is superimposed with current 5S rRNA (4ue4 purple, TM = 0.32555).
Figure 5
Figure 5
Logo sequences from the MSAs of ExGCs-encoded SRP-RNAs and the sequences in the corresponding database [83,84], as well as their conservation profiles (grey strip below each logo). In (A) the Ex1-encoded archaeal SRP-RNAs; in (B) the Ex2-encoded archaeal SRP-RNAs; in (C) the Ex1-encoded small bacterial SRP-RNAs; in (D) the Ex2-encoded small bacterial SRP-RNAs; in (E) the Ex1-encoded large bacterial SRP-RNAs; in (F) the Ex2-encoded large bacterial SRP-RNAs.
Figure 6
Figure 6
Conservation profiles (grey strip) of the MSAs of ExGCs-encoded tmRNAs, as well as a structural comparison of the reconstructed 3D structure and the crystallographic structure. In (A), the Ex1-encoded tmRNAs, Ex1-encoded portion (salmon) is superimposed with current tmRNA (3iyq purple, TM = 0.72324); (B) the Ex2-encoded tmRNAs, Ex2-encoded portion (sky blue) is superimposed with current 5S rRNA (3iyq purple, TM = 0.94504).
Figure 7
Figure 7
Logo sequences and 3D structures of bacterial type A RNA-P encoded by ExGCs. In (E) the RNA-P encoded by Ex1, Ex1-encoded portion (salmon) is superimposed with current RNA-P (3q1q purple, TM = 0.49572); in (F) the RNA-P encoded by Ex2, the characteristic sequence GAGGAAMGUCC is marked by a red rectangle in logo sequence, whereas Ex2-encoded portion (sky blue) is superimposed with current RNA-P (3q1q purple, TM = 0.58195).
Figure 8
Figure 8
Logo sequence of the MSA of the ExGCs-encoded bacterial Gly-tRNA and the corresponding 3D reconstruction, with the anticodon GCC highlighted by a red square. In (C) the Ex1-encoded Gly-tRNA (salmon) is superimposed with current Gly-tRNA (4mgn purple, TM = 0.95597); in (D) the Ex2-encoded Gly-tRNA (sky blue) is superimposed with current Gly-tRNA (4mgn purple, TM = 0.78711).
Figure 9
Figure 9
Logo sequence of the MSA of the ExGCs-encoded bacterial Ala-tRNA and the corresponding 3D reconstruction, with the anticodon GGC highlighted by a red square. In (A) the Ex1-encoded Gly-tRNA (salmon) is superimposed with current Gly-tRNA (3wqz purple, TM = 0.9318); in (B) the Ex2-encoded Gly-tRNA (sky blue) is superimposed with current Gly-tRNA (3wqz purple, TM = 0.58445).
Figure 10
Figure 10
Logo sequence of the MSA of the ExGCs-encoded bacterial Met-tRNA and the corresponding 3D reconstruction, with the anticodon CAU highlighted by a red square. In (C) the Ex1-encoded Met-tRNA (salmon) is superimposed with current Met-tRNA (2csx purple, TM = 0.90839); in (D) the Ex2-encoded Met-tRNA (sky blue) is superimposed with current Met-tRNA (2csx purple, TM = 0.93308).
Figure 11
Figure 11
Logo sequence of the MSA of the ExGCs-encoded bacterial Phe-tRNA and the corresponding 3D reconstruction, with the anticodon GAA highlighted by a red square. In (C) the Ex1-encoded Phe-tRNA (salmon) is superimposed with current Phe-tRNA (3l0u purple, TM = 0.90501); in (D) the Ex2-encoded Phe-tRNA (sky blue) is superimposed with current Phe-tRNA (3l0u purple, TM = 0.64502).
Figure 12
Figure 12
Logo sequence of the MSA of the ExGCs-encoded bacterial Trp-tRNA and the corresponding 3D reconstruction, with the anticodon CCA highlighted by a red square. In (C) the Ex1-encoded Trp-tRNA (salmon) is superimposed with the current Trp-tRNA (4ycp purple, TM = 0.94164); in (D) the Ex2-encoded Trp-tRNA (sky blue) is superimposed with current Trp-tRNA (4ycp purple, TM = 0.82026).
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