Phylogenetic Network Analysis Revealed the Occurrence of Horizontal Gene Transfer of 16S rRNA in the Genus Enterobacter

Mitsuharu Sato,Kentaro Miyazaki

doi:10.3389/fmicb.2017.02225

Abstract

Horizontal gene transfer (HGT) is a ubiquitous genetic event in bacterial evolution, but it seldom occurs for genes involved in highly complex supramolecules (or biosystems), which consist of many gene products. The ribosome is one such supramolecule, but several bacteria harbor dissimilar and/or chimeric 16S rRNAs in their genomes, suggesting the occurrence of HGT of this gene. However, we know little about whether the genes actually experience HGT and, if so, the frequency of such a transfer. This is primarily because the methods currently employed for phylogenetic analysis (e.g., neighbor-joining, maximum likelihood, and maximum parsimony) of 16S rRNA genes assume point mutation-driven tree-shape evolution as an evolutionary model, which is intrinsically inappropriate to decipher the evolutionary history for genes driven by recombination. To address this issue, we applied a phylogenetic network analysis, which has been used previously for detection of genetic recombination in homologous alleles, to the 16S rRNA gene. We focused on the genus Enterobacter, whose phylogenetic relationships inferred by multi-locus sequence alignment analysis and 16S rRNA sequences are incompatible. All 10 complete genomic sequences were retrieved from the NCBI database, in which 71 16S rRNA genes were included. Neighbor-joining analysis demonstrated that the genes residing in the same genomes clustered, indicating the occurrence of intragenomic recombination. However, as suggested by the low bootstrap values, evolutionary relationships between the clusters were uncertain. We then applied phylogenetic network analysis to representative sequences from each cluster. We found three ancestral 16S rRNA groups; the others were likely created through recursive recombination between the ancestors and chimeric descendants. Despite the large sequence changes caused by the recombination events, the RNA secondary structures were conserved. Successive intergenomic and intragenomic recombination thus shaped the evolution of 16S rRNA genes in the genus Enterobacter.

Highlights

Based on the structural complexity of the ribosome (Brodersen et al, 2002; Klein et al, 2004; Schuwirth et al, 2005), it was believed that each ribosomal component is species-specific and the genes have seldom experienced Horizontal gene transfer (HGT) (Jain et al, 1999)
This indicates the occurrence of intragenomic recombination between the copies (Hillis et al, 1991; Liao, 1999, 2000)
We identified at least five intergenomic recombination events within the Enterobacter genome

Summary

Introduction

Based on the structural complexity of the ribosome (Brodersen et al, 2002; Klein et al, 2004; Schuwirth et al, 2005), it was believed that each ribosomal component is species-specific and the genes have seldom experienced HGT (Jain et al, 1999). One unique feature of rRNA genes is that the genomes of many bacteria contain several copies (Stoddard et al, 2015). In E. coli, the frequency of such intragenomic recombination between 16S rRNA genes is as high as 5 × 10−9 per generation (Hashimoto et al, 2003). Such a high sequence similarity among the copies of the 16S rRNA gene is reported for bacterial genomes; bacterial species (genomes), which contain dissimilar (showing less than 98% sequence identity) 16S rRNA genes, are rare, counting for only 28 out of 2,143 genomes investigated (Tian et al, 2015)

Methods

Results

Conclusion