Intron-rich dinoflagellate genomes driven by Introner transposable elements of unprecedented diversity

Roy, Scott William; Gozashti, Landen; Bowser, Bradley A.; Weinstein, Brooke N.; Larue, Graham E.; Corbett-Detig, Russell

doi:10.1016/j.cub.2022.11.046

Cited by 8 publications

(6 citation statements)

References 47 publications

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“…Interestingly, a substantial proportion (64.8%) of the 85,849 genes in P. cordatum are dispersed duplicates (Fig. 1e and Additional File 3: Table S5), suggesting that most duplication events occurred independently; alternatively, collinearity of duplicated blocks was disrupted by extensive rearrangements, due in part to the abundant transposable elements, as expected in dinoflagellate genomes [21,55,56]. We found significantly enriched (p ≤ 0.01) gene functions in the distinct types of gene duplicates (Fig.…”

Section: P Cordatum Genome Reveals Hallmarks Of Bloom-forming Dinofla...mentioning

confidence: 73%

“…Therefore, the elevated G+C content of the P. cordatum genome does not appear to be a signature of heat resistance, and instead may be favored by selection to ensure high fidelity of transcription (i.e., G-C base pairs are more thermally stable) in open oceans. The long introns and presence of introner elements in the genome points to active transposition, i.e., non-autonomous DNA transposons, in contributing to the extensive rearrangement and duplication of genes [45,46,55], and to the large genome size with many functionally redundant but slightly different transcript isoforms that provide rich adaptive resources in frequent changing environments in the aquatic realm.…”

Section: Discussionmentioning

confidence: 99%

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Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate

Dougan,

Deng,

Wöhlbrand

et al. 2023

Genome Biol

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Background “Red tides” are harmful algal blooms caused by dinoflagellate microalgae that accumulate toxins lethal to other organisms, including humans via consumption of contaminated seafood. These algal blooms are driven by a combination of environmental factors including nutrient enrichment, particularly in warm waters, and are increasingly frequent. The molecular, regulatory, and evolutionary mechanisms that underlie the heat stress response in these harmful bloom-forming algal species remain little understood, due in part to the limited genomic resources from dinoflagellates, complicated by the large sizes of genomes, exhibiting features atypical of eukaryotes. Results We present the de novo assembled genome (~ 4.75 Gbp with 85,849 protein-coding genes), transcriptome, proteome, and metabolome from Prorocentrum cordatum, a globally abundant, bloom-forming dinoflagellate. Using axenic algal cultures, we study the molecular mechanisms that underpin the algal response to heat stress, which is relevant to current ocean warming trends. We present the first evidence of a complementary interplay between RNA editing and exon usage that regulates the expression and functional diversity of biomolecules, reflected by reduction in photosynthesis, central metabolism, and protein synthesis. These results reveal genomic signatures and post-transcriptional regulation for the first time in a pelagic dinoflagellate. Conclusions Our multi-omics analyses uncover the molecular response to heat stress in an important bloom-forming algal species, which is driven by complex gene structures in a large, high-G+C genome, combined with multi-level transcriptional regulation. The dynamics and interplay of molecular regulatory mechanisms may explain in part how dinoflagellates diversified to become some of the most ecologically successful organisms on Earth.

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Section: P Cordatum Genome Reveals Hallmarks Of Bloom-forming Dinofla...mentioning

confidence: 73%

Section: Discussionmentioning

confidence: 99%

Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate

Dougan,

Deng,

Wöhlbrand

et al. 2023

Genome Biol

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“…Their decline coincides with increases in the number of spliceosomal introns in both the large subunit (LSU) and small subunit (SSU) genes [19]. Introners appear to be a type of spliceosomal intron capable of rapid spread through genomes either by reverse splicing or transposition [5,11–13,20]. Although the link between DNA transposons and group I introns is more tenuous, both use endonucleases that target specific “homing” sites [21].…”

Section: Discussionmentioning

confidence: 99%

“…Eukaryotic genomes contain not only group I, group II, and archaeal introns, but also introns classified as spliceosomal, introners, group III, and twintrons. Spliceosomal introns (requiring spliceosomes), introners and group III introns are related to group II introns [6,10], although some reports place introners as diverging from DNA transposons [11–13]. Twintrons are introns within other introns and have been documented for groups I, II, and III [14].…”

Section: Introductionmentioning

confidence: 99%

Introns are derived from transposons

Rogers

Bendich

2023

Preprint

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Introns and transposons exhibit many similar features, but the connections between them have yet to be firmly established. Group I introns have commonalities with DNA transposons, while group II introns share many features with retrotransposons. Here, we report the results of an analysis of 214 introns (including group I, group II, group III, twintrons, spliceosomal, and archaeal introns) from members of seven major taxa (within Eukarya, Bacteria, and Archaea) that all have direct repeats at or near both exon/intron borders, indicating that they were inserted via transposition events. Border sequence analysis indicates that after splicing, most mature transcripts would be functionally compromised because they do not restore the DNA sequence information before intron insertion. Transposons and introns thus appear to be members of a diverse assemblage of parasitic mobile genetic elements that secondarily may benefit their host cell and have expanded greatly in eukaryotes from their presumed prokaryotic ancestors.

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“…The majority of dinoflagellate genes are thought to be post-transcriptionally regulated with pre-mRNA transcripts processed through spliced leader trans-splicing ( Zhang et al, 2009 ; Murray et al, 2016 ). Additionally, high numbers of introns per gene have been reported in dinoflagellates, and a recent study that reconstructed intron evolution in five dinoflagellate genomes found evidence for recently active Introners, which are a type of genetic element that creates copies of itself that insert into many genes across the genome ( Roy et al, 2023 ). Furthermore, alternative splicing is a hallmark of eukaryotic post-transcriptional gene regulation in which alternatively spliced pre-mRNA transcripts (i.e., introns and exons) result in multiple distinct mRNA transcript isoforms with distinct, and sometimes antagonistic fates.…”

Section: Discussionmentioning

confidence: 99%

Physiology governing diatom vs. dinoflagellate bloom and decline in coastal Santa Monica Bay

Ollison,

Hu,

Hopper

et al. 2023

Front. Microbiol.

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Algal blooms on the Southern California coast are typically dominated by diatom and dinoflagellate taxa, and are governed by their physiological responses to environmental cues; however, we lack a predictive understanding of the environmental controls underlying the establishment and persistence of these distinct bloom events. In this study, we examined gene expression among the numerically dominant diatom and dinoflagellate taxa during spring upwelling bloom events to compare the physiological underpinnings of diatom vs. dinoflagellate bloom dynamics. Diatoms, which bloomed following upwelling events, expressed genes related to dissolved inorganic nitrogen utilization, and genes related to the catabolism of chitin that may have prolonged their bloom duration following nitrogen depletion. Conversely, dinoflagellates bloomed under depleted inorganic nitrogen conditions, exhibited less variation in transcriptional activity, and expressed few genes associated with dissolved inorganic nutrients during their bloom. Dinoflagellate profiles exhibited evidence of proteolysis and heterotrophy that may have enabled them to bloom to high abundances under depleted inorganic nutrients. Taken together, diatom and dinoflagellate transcriptional profiles illustrated guild-specific physiologies that are tuned to respond to and thrive under distinct environmental “windows of opportunity.”

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Intron-rich dinoflagellate genomes driven by Introner transposable elements of unprecedented diversity

Cited by 8 publications

References 47 publications

Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate

Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate

Introns are derived from transposons

Physiology governing diatom vs. dinoflagellate bloom and decline in coastal Santa Monica Bay

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