Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions

Abstract

Background: Dinoflagellates are taxonomically diverse and ecologically important phytoplankton that are ubiquitously present in marine and freshwater environments. Mostly photosynthetic, dinoflagellates provide the basis of aquatic primary production; most taxa are free-living, while some can form symbiotic and parasitic associations with other organisms. However, knowledge of the molecular mechanisms that underpin the adaptation of these organisms to diverse ecological niches is limited by the scarce availability of genomic data, partly due to their large genome sizes estimated up to 250 Gbp. Currently available dinoflagellate genome data are restricted to Symbiodiniaceae (particularly symbionts of reef-building corals) and parasitic lineages, from taxa that have smaller genome size ranges, while genomic information from more diverse free-living species is still lacking.

Results: Here, we present two draft diploid genome assemblies of the free-living dinoflagellate Polarella glacialis, isolated from the Arctic and Antarctica. We found that about 68% of the genomes are composed of repetitive sequence, with long terminal repeats likely contributing to intra-species structural divergence and distinct genome sizes (3.0 and 2.7 Gbp). For each genome, guided using full-length transcriptome data, we predicted > 50,000 high-quality protein-coding genes, of which ~40% are in unidirectional gene clusters and ~25% comprise single exons. Multi-genome comparison unveiled genes specific to P. glacialis and a common, putatively bacterial origin of ice-binding domains in cold-adapted dinoflagellates.

Conclusions: Our results elucidate how selection acts within the context of a complex genome structure to facilitate local adaptation. Because 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 polar environments. These genomes provide a foundational reference for future research on dinoflagellate evolution.

Keywords: Cold adaptation; Dinoflagellates; Genome evolution; Genomics; Polarella glacialis.

Fig. 1

Genomes of Polarella glacialis and repeat content. a GenomeScope 21-mer profile for CCMP1383. b Identification of conserved core eukaryote genes (using CEGMA) in the assembled P. glacialis genomes of CCMP1383 and CCMP2088 compared to the assembled genomes of Cladocopium goreaui and Fugacium kawagutii [12]. c Interspersed repeat landscape and proportion of distinct repeat classes in the assembled genome of CCMP1383, studied using sequence divergence under the Kimura evolutionary model. d Percentage of 3-mers in the assembled genome and the sequence data for CCMP1383 for the ten most abundant 3-mers

Fig. 2

DinoSL-type full-length transcripts in P. glacialis. a Percentage of DinoSL-type transcripts of P. glacialis based on the identified start position along the DinoSL sequence, shown for positions 1 through 12. b Structure and number of DinoSL and/or relic DinoSL containing IsoSeq transcripts from each isolate. c Distribution of distances (in bp) between DinoSL-type transcriptional units shown for transcriptomes of CCMP1383 and CCMP2088

Fig. 3

Comparison of predicted gene models between the two P. glacialis genomes. a The comparison of predicted proteins in CCMP1383 against those in CCMP2088 is shown, incorporating evidence from the corresponding transcriptome data. b Scenario of RNA editing that would disrupt the alignment of a transcript to the genome

Fig. 4

Intergenic regions and tandemly repeated genes. a Distribution of the sizes of intergenic regions (in bp; ≤ 30,000 bp) shown for the assembled P. glacialis genomes of CCMP1383 and CCMP2088. b Frequency of strand-orientation changes in ten-gene windows generated from the predicted genes from isolates of P. glacialis, Symbiodiniaceae, and the other alveolates of Tetrahymena thermophilia (ciliate) and Plasmodium falciparum 3D7 (apicomplexan). c The number of tandemly repeated and/or single-exon genes in CCMP1383 and CCMP2088, shown for genes encoding bacteriorhodopsin and peridinin chlorophyll a-binding proteins

Fig. 5

Evolutionary history of ice-binding domains in P. glacialis and dinoflagellates. Only a small part of the 1080-taxon maximum likelihood protein tree is shown. Support values, based on 2000 ultrafast bootstrap approximations, are shown at the internal nodes. Only values > 50% are shown. The unit of branch length is the number of substitutions per site

Fig. 6

Genome features of Polarella glacialis as a psychrophilic, free-living dinoflagellate. Summary of key genome features of P. glacialis, focusing on unidirectionality of coding genes, tandemly repeated genes, and single-exon genes