The distribution, diversity, and importance of 16S rRNA gene introns in the order Thermoproteales.

Zackary J Jay,William P Inskeep

doi:10.1186/s13062-015-0065-6

Abstract

BackgroundIntron sequences are common in 16S rRNA genes of specific thermophilic lineages of Archaea, specifically the Thermoproteales (phylum Crenarchaeota). Environmental sequencing (16S rRNA gene and metagenome) from geothermal habitats in Yellowstone National Park (YNP) has expanded the available datasets for investigating 16S rRNA gene introns. The objectives of this study were to characterize and curate archaeal 16S rRNA gene introns from high-temperature habitats, evaluate the conservation and distribution of archaeal 16S rRNA introns in geothermal systems, and determine which “universal” archaeal 16S rRNA gene primers are impacted by the presence of intron sequences.ResultsSeveral new introns were identified and their insertion loci were constrained to thirteen locations across the 16S rRNA gene. Many of these introns encode homing endonucleases, although some introns were short or partial sequences. Pyrobaculum, Thermoproteus, and Caldivirga 16S rRNA genes contained the most abundant and diverse intron sequences. Phylogenetic analysis of introns revealed that sequences within the same locus are distributed biogeographically. The most diverse set of introns were observed in a high-temperature, circumneutral (pH 6) sulfur sediment environment, which also contained the greatest diversity of different Thermoproteales phylotypes.ConclusionsThe widespread presence of introns in the Thermoproteales indicates a high probability of misalignments using different “universal” 16S rRNA primers employed in environmental microbial community analysis.ReviewersThis article was reviewed by Dr. Eugene Koonin and Dr. W. Ford Doolittle.Electronic supplementary materialThe online version of this article (doi:10.1186/s13062-015-0065-6) contains supplementary material, which is available to authorized users.

Highlights

Intron sequences are common in 16S rRNA genes of specific thermophilic lineages of Archaea, the Thermoproteales
The objectives of this study were to (i) characterize and curate all archaeal 16S rRNA gene introns found within currently available genomes and environmental sequence databases, (ii) perform a phylogenetic analysis to evaluate the conservation and distribution of archaeal 16S rRNA introns in geothermal systems, and (iii) determine which “universal” archaeal 16S rRNA gene primers are interrupted by the presence of intron sequences
Intron sequences were confined to 13 loci across the 16S rRNA gene (Fig. 1, Table 1)

Summary

Introduction

Intron sequences are common in 16S rRNA genes of specific thermophilic lineages of Archaea, the Thermoproteales (phylum Crenarchaeota). The objectives of this study were to characterize and curate archaeal 16S rRNA gene introns from high-temperature habitats, evaluate the conservation and distribution of archaeal 16S rRNA introns in geothermal systems, and determine which “universal” archaeal 16S rRNA gene primers are impacted by the presence of intron sequences. Several lineages within the domain Archaea contain 16S rRNA gene introns, which are mobile genetic elements that do not appear to impact the host’s growth or metabolism. The orders Desulfurococcales and Thermoproteales contain 23S rRNA and tRNA gene introns; the limited number of genomes in these orders prevents a robust analysis of the diversity and distribution of introns in these genes.

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