Small, but surprisingly repetitive genomes: transposon expansion and not polyploidy has driven a doubling in genome size in a metazoan species complex

Abstract

Background: The causes and consequences of genome size variation across Eukaryotes, which spans five orders of magnitude, have been hotly debated since before the advent of genome sequencing. Previous studies have mostly examined variation among larger taxonomic units (e.g., orders, or genera), while comparisons among closely related species are rare. Rotifers of the Brachionus plicatilis species complex exhibit a seven-fold variation in genome size and thus represent a unique opportunity to study such changes on a relatively short evolutionary timescale. Here, we sequenced and analysed the genomes of four species of this complex with nuclear DNA contents spanning 110-422 Mbp. To establish the likely mechanisms of genome size change, we analysed both sequencing read libraries and assemblies for signatures of polyploidy and repetitive element content. We also compared these genomes to that of B. calyciflorus, the closest relative with a sequenced genome (293 Mbp nuclear DNA content). Results: Despite the very large differences in genome size, we saw no evidence of ploidy level changes across the B. plicatilis complex. However, repetitive element content explained a large portion of genome size variation (at least 54%). The species with the largest genome, B. asplanchnoidis, has a strikingly high 44% repetitive element content, while the smaller B. plicatilis genomes contain between 14 and 25% repetitive elements. According to our analyses, the B. calyciflorus genome contains 39% repetitive elements, which is substantially higher than previously reported (21%), and suggests that high repetitive element load could be widespread in monogonont rotifers. Conclusions: Even though the genome sizes of these species are at the low end of the metazoan spectrum, their genomes contain substantial amounts of repetitive elements. Polyploidy does not appear to play a role in genome size variations in these species, and these variations can be mostly explained by changes in repetitive element content. This contradicts the naïve expectation that small genomes are streamlined, or less complex, and that large variations in nuclear DNA content between closely related species are due to polyploidy.

The genome, transcriptome, and proteome of the fish parasite Pomphorhynchus laevis (Acanthocephala)

“…With a total span of ca. 260 Mb, its size is within the range reported for bdelloids [67,68] but larger than draft genomes in monogononts [144][145][146][147]149]. In addition, the repetitive portion of the P. laevis genome (63%) is higher than corresponding values published for monogononts and bdelloids [68,146].…”

“…However, there may also be an underestimation in respect to the nuclear genomes of traditional rotifer taxa (see also [157]). In support of such a possibility, dnaPipeTE detected a repeat portion of up to 44% in Brachionus asplanchnoidis [144]. In any way, the non-repetitive portion of the P. laevis draft genome spans ca.…”

“…Thereby, the current draft genome of P. laevis consists of 4,021 contigs of 65 kb on average (contig N50 = 126,104 bp), making it one of the most coherent within the Rotifera-Acanthocephala clade (Table 1). Only the draft genomes in Brachionus calyciflorus, Brachionus koreanus and the Brachionus plicatilis species complex are less fragmented, but this coincides with either a much smaller size of the assembly (51 Mb [144], 85 Mb [145]), or the introduction of 6.41% [146] and 5.26% [147] of ambiguous bases (Ns) in the process of scaffolding. In contrast, we decided against such procedure and present a draft genome of P. laevis without any N.…”

“…On the other hand, low representation of SINEs seems to be common in the Rotifera-Acanthocephala clade. In B. calyciflorus and A. vaga, for example, SINEs make up only 0.00-0.08% of the repeats [144,146].…”

“…In fact, cytofluorometric measurements suggest that Adineta vaga and Philodina roseola have haploid genomes of about 245 Mb and 1,193 Mb, respectively (1 pg = 978 Mb;[151,154]). However, more revealing should be the comparison with size estimates of haploid genomes according to de novo assemblies, which span 129.6 Mb in B. calyciflorus and 51-115 Mb in the B. plicatilis species complex[144,146,149]. The corresponding estimates for bdelloids are in a higher range once more, with up to 217.9 Mb (A. vaga), 201.3 Mb (Adineta ricciae), 295.4 Mb (Rotaria macrura), and 337.6 Mb (R. magnacalcarata)[67,68].…”