Abstract
Ribosomal loci represent a major tool for investigating environmental diversity and community structure via high-throughput marker gene studies of eukaryotes (e.g. 18S rRNA). Since the estimation of species’ abundance is a major goal of environmental studies (by counting numbers of sequences), understanding the patterns of rRNA copy number across species will be critical for informing such high-throughput approaches. Such knowledge is critical, given that ribosomal RNA genes exist within multi-copy repeated arrays in a genome. Here we measured the repeat copy number for six nematode species by mapping the sequences from whole genome shotgun libraries against reference sequences for their rRNA repeat. This revealed a 6-fold variation in repeat copy number amongst taxa investigated, with levels of intragenomic variation ranging from 56 to 323 copies of the rRNA array. By applying the same approach to four C. elegans mutation accumulation lines propagated by repeated bottlenecking for an average of ~400 generations, we find on average a 2-fold increase in repeat copy number (rate of increase in rRNA estimated at 0.0285-0.3414 copies per generation), suggesting that rRNA repeat copy number is subject to selection. Within each Caenorhabditis species, the majority of intragenomic variation found across the rRNA repeat was observed within gene regions (18S, 28S, 5.8S), suggesting that such intragenomic variation is not a product of selection for rRNA coding function. We find that the dramatic variation in repeat copy number among these six nematode genomes would limit the use of rRNA in estimates of organismal abundance. In addition, the unique pattern of variation within a single genome was uncorrelated with patterns of divergence between species, reflecting a strong signature of natural selection for rRNA function. A better understanding of the factors that control or affect copy number in these arrays, as well as their rates and patterns of evolution, will be critical for informing estimates of global biodiversity.
Highlights
The ribosome is a fundamental component of the eukaryotic cell, and nuclear genes encoding the ribosomal subunits have long been the focus of intensive empirical study
The ability to detect extremely small sub-segment expansions may exceed the resolution of this analysis, this data suggests that Ribosomal RNA genes (rRNA) repeat expansions and deletions generally involve the entire rRNA cluster
The number of complete rRNA repeats appeared to vary widely, with estimates ranging from 56 copies in C. briggsae up to 323 copies in C. brenneri
Summary
The ribosome is a fundamental component of the eukaryotic cell, and nuclear genes encoding the ribosomal subunits have long been the focus of intensive empirical study. Ribosomal RNA genes have been used as markers for phylogeny reconstruction [3], diversity analysis [4,5], and genome evolution studies [6] These loci are amenable to PCRbased assays due to their pseudo-orthology and the large amount of existing data readily available in public sequence databases. Despite their popularity and utility, we continue to have a poor understanding of polymorphism and copy number variation in rRNA loci across diverse eukaryotic taxa. Quantifying this variation, and pinpointing the selective forces that impact rRNA variation, will be paramount for building a global view of biodiversity, population-level processes, and speciation
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