Comprehensive Phylogenetic Analysis of Bacterial Group II Intron-Encoded ORFs Lacking the DNA Endonuclease Domain Reveals New Varieties

Nicolás Toro,Francisco Martínez-Abarca,Luis Menéndez-Arias

doi:10.1371/journal.pone.0055102

Nicolás Toro, Francisco Martínez-Abarca + Show 1 more

Open Access

https://doi.org/10.1371/journal.pone.0055102

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Abstract

Group II introns are self-splicing RNAs that act as mobile retroelements in the organelles of plants, fungi and protists. They are also widely distributed in bacteria, and are generally assumed to be the ancestors of nuclear spliceosomal introns. Most bacterial group II introns have a multifunctional intron-encoded protein (IEP) ORF within the ribozyme domain IV (DIV). This ORF encodes an N-terminal reverse transcriptase (RT) domain, followed by a putative RNA-binding domain with RNA splicing or maturase activity and, in some cases, a C-terminal DNA-binding (D) region followed by a DNA endonuclease (En) domain. In this study, we focused on bacterial group II intron ORF phylogenetic classes containing only reverse transcriptase/maturase open reading frames, with no recognizable D/En region (classes A, C, D, E, F and unclassified introns). On the basis of phylogenetic analyses of the maturase domain and its C-terminal extension, which appears to be a signature characteristic of ORF phylogenetic class, with support from the phylogeny inferred from the RT domain, we have revised the proposed new class F, defining new intron ORF varieties. Our results increase knowledge of the lineage of group II introns encoding proteins lacking the En-domain.

Highlights

Group II introns are self-splicing RNAs that act as mobile retroelements and are thought to be the ancestors of nuclear spliceosomal introns [1,2,3,4]
It is generally accepted that group II intron RNAs have coevolved with their intron-encoded protein (IEP), and phylogenetic analyses of group II intron-encoded open reading frames (ORFs) has resulted in their classification into several groups (A, B, C, D, E, F, CL1 [chloroplast-like 1], CL2 [chloroplast-like 2] and ML [mitochondrion-like])
We searched for new types of reverse transcriptase (RT)/maturase ORFs lacking the endonuclease domain, using the amino-acid consensus sequence obtained from the multiple sequence alignment (MSA) of domain X and the C-terminal extension for reported new class F and unclassified introns downloaded from the database for bacterial group II introns

Summary

Introduction

Group II introns are self-splicing RNAs that act as mobile retroelements and are thought to be the ancestors of nuclear spliceosomal introns [1,2,3,4]. Simon et al [15] performed a large-scale phylogenetic analysis of group II introns with sequence data for both the conserved RNA structure and the intron-encoded reverse transcriptase. They found that each ORF class, including class F, was a robust clade, but that the relationship between classes remained ambiguous. On the basis of consensus maturase and Cterminal amino-acid sequences, with additional support from the phylogeny inferred from the larger RT-domain, we extend current knowledge of intron ORF subclasses with no recognizable D/En region. Our results call into question the proposed new class F, but reveal the existence of additional group II intron ORF varieties

Materials and Methods

Results and Discussion

Conclusions