Abstract
The 16 S rRNA sequence has long been used uncritically as a molecular clock to infer phylogenetic relationships among prokaryotes without fully elucidating the evolutionary changes that this molecule undergoes. In this study, we investigated the functional evolvability of 16 S rRNA, using comparative RNA function analyses between the 16 S rRNAs of Escherichia coli (Proteobacteria) and Acidobacteria (78% identity, 334 nucleotide differences) in the common genetic background of E. coli. While the growth phenotype of an E. coli mutant harboring the acidobacterial gene was disrupted significantly, it was restored almost completely following introduction of a 16 S rRNA sequence with a single base-pair variation in helix 44; the remaining 332 nucleotides were thus functionally similar to those of E. coli. Our results suggest that 16 S rRNAs share an inflexible cradle structure formed by ribosomal proteins and have evolved by accumulating species-specific yet functionally similar mutations. While this experimental evidence suggests the neutral evolvability of 16 S rRNA genes and hence satisfies the necessary requirements to use the sequence as a molecular clock, it also implies the promiscuous nature of the 16 S rRNA gene, i.e., the occurrence of horizontal gene transfer among bacteria.
Highlights
The ribosome is an RNA-centered and highly complex ribonucleoprotein particle, in which mRNA-encoded genetic information is translated into proteins[1, 2]
Our experimental results revealed that 332 (99.4%) nucleotides in the acidobacterial 16 S rRNA gene were functionally similar to those in E. coli genetic background, providing strong evidence that the primitive 16 S rRNAs were held by a common framework of ribosomal proteins and accumulated lineage-specific neutral mutations during evolution
We identified a clone of the 16 S rRNA gene from an acidobacterial species showing a minimal sequence identity of 78.4% to that of E. coli (16SEco) (Supplementary Table 1)
Summary
The ribosome is an RNA-centered and highly complex ribonucleoprotein particle, in which mRNA-encoded genetic information is translated into proteins[1, 2]. Our experimental results revealed that 332 (99.4%) nucleotides in the acidobacterial 16 S rRNA gene were functionally similar to those in E. coli genetic background, providing strong evidence that the primitive 16 S rRNAs were held by a common framework of ribosomal proteins and accumulated lineage-specific neutral mutations during evolution. While this functional similarity in distantly related 16 S rRNAs seemingly assures the use of these sequences as a reliable clock, it suggests a unique evolutionary characteristic of the gene; 16 S rRNA is quite amenable to HGT, highlighting the promiscuous nature of the gene
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