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 freeliving 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.

Rapid protein evolution, organellar reductions, and invasive intronic elements in the marine aerobic parasite dinoflagellate Amoebophrya spp

“…We identified a truncated DinoSL motif (13 nucleotides, representing 60% of the DinoSL motif; Fig. S 5 ) at the 5′-end of at least 18.5% (A25) and 37.8% (A120) of the transcripts, a similar value found in other published data [ 13 , 25 ]. These truncated motifs likely derive from a single complete (22 nucleotides) DinoSL-like coding sequence that was also detected in each genome (Fig.…”

Integrated omics unveil the secondary metabolic landscape of a basal dinoflagellate

“…This genome included~30% repetitive elements composed of simple repeats (1.97%), low complexity repeats (0.39%), satellite repeats (0.02%), LINEs (0.02%), LTR elements (0.03%), DNA elements (0.1%), and unclassified repeats (27.4%) (Additional file 2: Supplementary Tables 3 and 4). The abundance of repetitive elements may drive genome evolution in dinoflagellates, as reported in Symbiodiniaceae and Polarella glacialis genomes (16-68%) [6,7]. Comparative analysis of intron and exon features of A. gibbosum provides additional insights into expansion of dinoflagellate genomes (Table 1).…”

“…The persistent condensed state of dinoflagellate chromosomes and their liquid crystalline organization, loss of nucleosomal chromatin packaging, use of 5hydroxymethyluracil in nuclear genomic DNA, and huge genomes of some dinoflagellates (≥ 100 Gbp) are anomalous for eukaryotes [3][4][5]. Recently, the critical role of tandem-duplicated, unidirectional, single-exon genes to survive in cold, low-light environments was reported in two draft genomes (~2.8 Gb and~3.0 Gb) of the free-living dinoflagellate, Polarella glacialis [6]. Even with ongoing genomic efforts, understanding of dinoflagellate toxin biosynthesis remains elusive due to their unusually large genomes and limited biosynthetic surveys [4][5][6][7][8][9][10].…”

“…Recently, the critical role of tandem-duplicated, unidirectional, single-exon genes to survive in cold, low-light environments was reported in two draft genomes (~2.8 Gb and~3.0 Gb) of the free-living dinoflagellate, Polarella glacialis [6]. Even with ongoing genomic efforts, understanding of dinoflagellate toxin biosynthesis remains elusive due to their unusually large genomes and limited biosynthetic surveys [4][5][6][7][8][9][10].…”

Red Algal Extremophiles: Novel Genes and Paradigms

“…Although the Cyanidiophyceae have HGTs as approximately 1% of their gene inventory and this makes them good models for studying this process, they are certainly not unique. Many other extremophilic eukaryotes have HGTs, ranging from protists like ciliates and dinoflagellates [29,30] to desiccation and radiation-tolerant animals like rotifers [31]. One example is ice-binding proteins in Arctic/Antarctic diatoms that were acquired from prokaryotes or viruses that survive cold temperatures, giving diatoms the ability to more easily adapt to polar climates [32].…”