Polarella glacialis genomes encode tandem repeats of single-exon genes with functions critical to adaptation of dinoflagellates

Abstract

Dinoflagellates are taxonomically diverse, ecologically important phytoplankton in marine and freshwater environments. Here, we present two draft diploid genome assemblies of the free-living dinoflagellate Polarella glacialis, isolated from the Arctic and Antarctica. For each genome, guided using full-length transcriptome data, we predicted >50,000 high-quality genes. About 68% of the genome is repetitive sequence; long terminal repeats likely contribute to intra-species structural divergence and distinct genome sizes (3.0 and 2.7 Gbp).Of all genes, ~40% are encoded unidirectionally, ~25% comprised of single exons. Multigenome comparison unveiled genes specific to P. glacialis and a common, putatively bacterial, origin of ice-binding domains in cold-adapted dinoflagellates. Our results elucidate how selection acts within the context of a complex genome structure to facilitate local adaptation. Since most dinoflagellate genes are constitutively expressed, Polarella glacialis has enhanced transcriptional responses via unidirectional, tandem duplication of single-exon genes that encode functions critical to survival in cold, low-light environments. health risks 6 . Some taxa have specialised to inhabit extreme environments, such as those found in the brine channels of polar sea ice 7-10 .Thus far, available genome data of dinoflagellates are largely restricted to symbiotic or parasitic species [11][12][13][14][15][16][17] . These lineages were chosen for sequencing because their genomes are relatively small, i.e. 0.12-4.8 Gbp. In comparison, genomes of other free-living dinoflagellates are much larger in size, ranging from ~7 Gbp in the psychrophile Polarella glacialis, to over 200 Gbp in Prorocentrum sp. based on DAPI-staining of DNA content 18 .Repeat content has been estimated at >55% in the genome sequences of some free-living dinoflagellates 19,20 ; single-exon genes have also been described 21 . Given that most dinoflagellate lineages are free-living, whole genome sequences of these taxa are critical to understand the molecular mechanisms that underpin their successful diversification in specialised environmental niches.Polarella glacialis, a psychrophilic (cold-adapted) free-living species, represents an excellent system for genomic studies of dinoflagellates for three reasons. First, it is closely related to Symbiodiniaceae (both in Order Suessiales), the family that contains the coral reef symbionts, e.g. Symbiodinium and related genera. Second, P. glacialis has been reported only in polar regions. Studying the P. glacialis genome can thus provide a first glimpse into molecular mechanisms that underlie both the evolutionary transition of dinoflagellates from a free-living to a symbiotic lifestyle, and the adaptation to extreme environments. Third, the estimated genome size of P. glacialis is still in the smaller range (~7 Gbp 18 ) of all dinoflagellate taxa, which presents a technical advantage in terms of allowing efficient genome assembly and gene prediction.

Structural rearrangements drive extensive genome divergence between symbiotic and free-living Symbiodinium

“…Tandem duplication of exons and genes is common in dinoflagellates, and may serve as an adaptive mechanism to enhance functions relevant for their biology 22,23 . Whereas in some dinoflagellates genes in tandem arrays can have hundreds of copies, e.g.…”

“…Retroposition is another gene-duplication mechanism known to impact genome evolution of Symbiodiniaceae and other dinoflagellates 22,27 . To survey retroposition in genomes of S. tridacnidorum and S. natans , we searched for relicts of the dinoflagellate spliced-leader (DinoSL) sequence in upstream regions of all predicted genes.…”

“…2) further supports the enhanced activity of retrotransposition in S. tridacnidorum . Although LINEs display high sequence divergence (Kimura distance 34 20-30), potentially a remnant from an ancient burst of this type of element common to all Suessiales 3,22 , most LTRs and DNA transposons are largely conserved (Kimura distance < 5), suggesting that they may be active (Fig. 4).…”

Evidence That Inconsistent Gene Prediction Can Mislead Analysis of Dinoflagellate Genomes

“…The impact of these biases intensified when comparing de novo assembled genomes of dinoflagellates, because genome sequences among closely related taxa (e.g., the symbiodiniacean taxa studied here) are known to be highly dissimilar (Lin et al 2015, Liu et al 2018, Stephens et al 2019, and little reference data are available. In addition to the quality of genome assembly, the biases introduced by different gene-prediction approaches can significantly impact the downstream comparative genomic analyses and affect subsequent biological interpretations.…”

“…In addition to the quality of genome assembly, the biases introduced by different gene-prediction approaches can significantly impact the downstream comparative genomic analyses and affect subsequent biological interpretations. The impact of these biases intensified when comparing de novo assembled genomes of dinoflagellates, because genome sequences among closely related taxa (e.g., the symbiodiniacean taxa studied here) are known to be highly dissimilar (Lin et al 2015, Liu et al 2018, Stephens et al 2019, and little reference data are available. In this situation, we urge the research community to consider a consistent gene-prediction work-…”