Ancestral Insertions and Expansions of rRNA do not Support an Origin of the Ribosome in Its Peptidyl Transferase Center

Abstract

Phylogenetic reconstruction of ribosomal history suggests that the ribonucleoprotein complex originated in structures supporting RNA decoding and ribosomal mechanics. A recent study of accretion of ancestral expansion segments of rRNA, however, contends that the large subunit of the ribosome originated in its peptidyl transferase center (PTC). Here I re-analyze the rRNA insertion data that supports this claim. Analysis of a crucial three-way junction connecting the long-helical coaxial branch that supports the PTC to the L1 stalk and its translocation functions reveals an incorrect branch-to-trunk insertion assignment that is in conflict with the PTC-centered accretion model. Instead, the insertion supports the ancestral origin of translocation. Similarly, an insertion linking a terminal coaxial trunk that holds the L7-12 stalk and its GTPase center to a seven-way junction of the molecule again questions the early origin of the PTC. Unwarranted assumptions, dismissals of conflicting data, structural insertion ambiguities, and lack of phylogenetic information compromise the construction of an unequivocal insertion-based model of macromolecular accretion. Results prompt integration of phylogenetic and structure-based models to address RNA junction growth and evolutionary constraints acting on ribosomal structure.

Fig. 1

The trunk-branch directionality of putative ancestral insertions of expansion segments suggests an origin of the large rRNA molecule in ribosomal mechanics and not the PTC. a AES39 (red) supports translocation functions of the L1 stalk and AES1-5 (yellow) supports protein biosynthesis. Structural criteria and modeling by energy minimization indicates that the H75 branch of AES1 likely inserted into the H76-H79 trunk of AES39 that was originally stabilized by coaxial stacking. b Similarly, the preexistent AES 23 trunk (red) supports the L7-12 stalk and its GTPase center and the AES22 (blue) branch connects to the rest of the seven-way junction and to the bulk of the rRNA molecule, including the PTC (see detail with secondary structure model). Atomic features of insertions can be seen in Fig. S2. The red-yellow-blue colorings reflect a phylogenetically derived timeline, with red being old (Harish and Caetano-Anollés 2012) (Color figure online)