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Dinoflagellate Biology in the Omics Era

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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Systems Microbiology".

Deadline for manuscript submissions: closed (31 December 2019) | Viewed by 75448

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Prof. Dr. David Morse

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Institut de Recherche en BiologieVégétale, Département de Sciences Biologiques, Université de Montréal, 4101 Sherbrooke east, Montréal, QC H1X 2B2, Canada
Interests: cellular biology; dinoflagellates; circadian biology

Prof. Dr. Senjie Lin

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Department of Marine Sciences, University of Connecticut, Groton, CT 06340, USA
Interests: marine algae; eukaryotic microbes; molecular ecology; functional genomics; microbial interactions
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Dear Colleagues,

Dinoflagellates are important players in the marine ecosystem, as they are involved in coral symbiosis, can cause the formation of harmful algal blooms and contribute an important fraction of the ocean’s primary production. Furthermore, dinoflagellates have many unusual cellular features, including chromosomes that remain condensed throughout the cell cycle without histones, chloroplasts that are derived from a secondary endosymbiosis, and an ability to synthesize a wide range of toxins.

For this Special Issue of Microorganisms, we invite you to send contributions concerning any aspect of dinoflagellate biology examined using genomics, transcriptomics, proteomics or metabolomics.

Prof. Dr. David Morse
Prof. Dr. Senjie Lin
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Biology of Dinoflagellates: Advances in the Last 25 Years (1987-2012) in Microorganisms (8 articles)

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22 pages, 2161 KiB

Open AccessArticle

Functional Genomics Differentiate Inherent and Environmentally Influenced Traits in Dinoflagellate and Diatom Communities

by Stephanie Elferink, Uwe John, Stefan Neuhaus and Sylke Wohlrab

Microorganisms 2020, 8(4), 567; https://doi.org/10.3390/microorganisms8040567 - 15 Apr 2020

Cited by 16 | Viewed by 3770

Abstract

Dinoflagellates and diatoms are among the most prominent microeukaryotic plankton groups, and they have evolved different functional traits reflecting their roles within ecosystems. However, links between their metabolic processes and functional traits within different environmental contexts warrant further study. The functional biodiversity of dinoflagellates and diatoms was accessed with metatranscriptomics using Pfam protein domains as proxies for functional processes. Despite the overall geographic similarity of functional responses, abiotic (i.e., temperature and salinity; ~800 Pfam domains) and biotic (i.e., taxonomic group; ~1500 Pfam domains) factors influencing particular functional responses were identified. Salinity and temperature were identified as the main drivers of community composition. Higher temperatures were associated with an increase of Pfam domains involved in energy metabolism and a decrease of processes associated with translation and the sulfur cycle. Salinity changes were correlated with the biosynthesis of secondary metabolites (e.g., terpenoids and polyketides) and signal transduction processes, indicating an overall strong effect on the biota. The abundance of dinoflagellates was positively correlated with nitrogen metabolism, vesicular transport and signal transduction, highlighting their link to biotic interactions (more so than diatoms) and suggesting the central role of species interactions in the evolution of dinoflagellates. Diatoms were associated with metabolites (e.g., isoprenoids and carotenoids), as well as lysine degradation, which highlights their ecological role as important primary producers and indicates the physiological importance of these metabolic pathways for diatoms in their natural environment. These approaches and gathered information will support ecological questions concerning the marine ecosystem state and metabolic interactions in the marine environment. Full article

(This article belongs to the Special Issue Dinoflagellate Biology in the Omics Era)

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14 pages, 2880 KiB

Open AccessArticle

Genome Improvement and Core Gene Set Refinement of Fugacium kawagutii

by Tangcheng Li, Liying Yu, Bo Song, Yue Song, Ling Li, Xin Lin and Senjie Lin

Microorganisms 2020, 8(1), 102; https://doi.org/10.3390/microorganisms8010102 - 11 Jan 2020

Cited by 23 | Viewed by 5135

Abstract

Cataloging an accurate functional gene set for the Symbiodiniaceae species is crucial for addressing biological questions of dinoflagellate symbiosis with corals and other invertebrates. To improve the gene models of Fugacium kawagutii, we conducted high-throughput chromosome conformation capture (Hi-C) for the genome and Illumina combined with PacBio sequencing for the transcriptome to achieve a new genome assembly and gene prediction. A 0.937-Gbp assembly of F. kawagutii were obtained, with a N50 > 13 Mbp and the longest scaffold of 121 Mbp capped with telomere motif at both ends. Gene annotation produced 45,192 protein-coding genes, among which, 11,984 are new compared to previous versions of the genome. The newly identified genes are mainly enriched in 38 KEGG pathways including N-Glycan biosynthesis, mRNA surveillance pathway, cell cycle, autophagy, mitophagy, and fatty acid synthesis, which are important for symbiosis, nutrition, and reproduction. The newly identified genes also included those encoding O-methyltransferase (O-MT), 3-dehydroquinate synthase, homologous-pairing protein 2-like (HOP2) and meiosis protein 2 (MEI2), which function in mycosporine-like amino acids (MAAs) biosynthesis and sexual reproduction, respectively. The improved version of the gene set (Fugka_Geneset _V3) raised transcriptomic read mapping rate from 33% to 54% and BUSCO match from 29% to 55%. Further differential gene expression analysis yielded a set of stably expressed genes under variable trace metal conditions, of which 115 with annotated functions have recently been found to be stably expressed under three other conditions, thus further developing the “core gene set” of F. kawagutii. This improved genome will prove useful for future Symbiodiniaceae transcriptomic, gene structure, and gene expression studies, and the refined “core gene set” will be a valuable resource from which to develop reference genes for gene expression studies. Full article

(This article belongs to the Special Issue Dinoflagellate Biology in the Omics Era)

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12 pages, 5156 KiB

Open AccessArticle

Cell Cycle, Division Rate, and Feeding of the Heterotroph Phalacroma rotundatum in a Chilean Fjord

by Patricio A. Díaz, Iván Pérez-Santos, Gonzalo Álvarez, Michael Araya, Francisco Álvarez and Beatriz Reguera

Microorganisms 2019, 7(10), 451; https://doi.org/10.3390/microorganisms7100451 - 14 Oct 2019

Cited by 2 | Viewed by 2827

Abstract

Phalacroma rotundatum is a rare cosmopolitan heterotrophic dinoflagellate. This species, included in the IOC-UNESCO Taxonomic Reference List of Harmful Microalgae, may be a diarrhetic shellfish poisoning (DSP) toxin vector, but little is known about its ecophysiology and behavior. A vertical net haul collected during the austral summer of 2018 in Reloncaví Sound (Chilean Patagonia) revealed an unusually abundant population of P. rotundatum and prompted intensive 24 h sampling on 16–17 January to study the cell cycle and feeding behavior of this species. Hydrographic measurements from a buoy revealed the local characteristic estuarine circulation, with a brackish surface layer (salinity 26–28) separated from saltier, colder bottom waters by a pycnocline at a depth modulated by the tidal regime. A high proportion of P. rotundatum cells were packed with digestive vacuoles (peak of 70% at 14:00), and phased cell division (µ = 0.46 d⁻¹) occurred 3 h after sunrise. The division time (T_D) was 2 h. This is the first cell cycle study of P. rotundatum. The results here disagree with those of previous field studies that considered asynchronous division in some Dinophysis species to be related to heterotrophic feeding. They also question the very specific prey requirements, Tiarina fusus, reported for P. rotundatum in northern Europe. Full article

(This article belongs to the Special Issue Dinoflagellate Biology in the Omics Era)

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10 pages, 1435 KiB

Open AccessArticle

Assessing Transcriptional Responses to Light by the Dinoflagellate Symbiodinium

by Bahareh Zaheri, Steve Dagenais-Bellefeuille, Bo Song and David Morse

Microorganisms 2019, 7(8), 261; https://doi.org/10.3390/microorganisms7080261 - 14 Aug 2019

Cited by 6 | Viewed by 3432

Abstract

The control of transcription is poorly understood in dinoflagellates, a group of protists whose permanently condensed chromosomes are formed without histones. Furthermore, while transcriptomes contain a number of proteins annotated as transcription factors, the majority of these are cold shock domain proteins which are also known to bind RNA, meaning the number of true transcription factors is unknown. Here we have assessed the transcriptional response to light in the photosynthetic species Symbiodinium kawagutii. We find that three genes previously reported to respond to light using qPCR do not show differential expression using northern blots or RNA-Seq. Interestingly, global transcript profiling by RNA-Seq at LD 0 (dawn) and LD 12 (dusk) found only seven light-regulated genes (FDR = 0.1). qPCR using three randomly selected genes out of the seven was only able to validate differential expression of two. We conclude that there is likely to be less light regulation of gene expression in dinoflagellates than previously thought and suggest that transcriptional responses to other stimuli should also be more thoroughly evaluated in this class of organisms. Full article

(This article belongs to the Special Issue Dinoflagellate Biology in the Omics Era)

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28 pages, 3023 KiB

Open AccessArticle

Metagenomic Sequencing Identifies Highly Diverse Assemblages of Dinoflagellate Cysts in Sediments from Ships’ Ballast Tanks

by Lixia Shang, Zhangxi Hu, Yunyan Deng, Yuyang Liu, Xinyu Zhai, Zhaoyang Chai, Xiaohan Liu, Zifeng Zhan, Fred C. Dobbs and Ying Zhong Tang

Microorganisms 2019, 7(8), 250; https://doi.org/10.3390/microorganisms7080250 - 09 Aug 2019

Cited by 30 | Viewed by 5776

Abstract

Ships’ ballast tanks have long been known as vectors for the introduction of organisms. We applied next-generation sequencing to detect dinoflagellates (mainly as cysts) in 32 ballast tank sediments collected during 2001–2003 from ships entering the Great Lakes or Chesapeake Bay and subsequently archived. Seventy-three dinoflagellates were fully identified to species level by this metagenomic approach and single-cell polymerase chain reaction (PCR)-based sequencing, including 19 toxic species, 36 harmful algal bloom (HAB) forming species, 22 previously unreported as producing cysts, and 55 reported from ballast tank sediments for the first time (including 13 freshwater species), plus 545 operational taxonomic units (OTUs) not fully identified due to a lack of reference sequences, indicating tank sediments are repositories of many previously undocumented taxa. Analyses indicated great heterogeneity of species composition among samples from different sources. Light and scanning electron microscopy and single-cell PCR sequencing supported and confirmed results of the metagenomic approach. This study increases the number of fully identified dinoflagellate species from ballast tank sediments to 142 (>50% increase). From the perspective of ballast water management, the high diversity and spatiotemporal heterogeneity of dinoflagellates in ballast tanks argues for continuing research and stringent adherence to procedures intended to prevent unintended introduction of non-indigenous toxic and HAB-forming species. Full article

(This article belongs to the Special Issue Dinoflagellate Biology in the Omics Era)

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13 pages, 1541 KiB

Open AccessArticle

Non-Conventional Metal Ion Cofactor Requirement of Dinoflagellate Alkaline Phosphatase and Translational Regulation by Phosphorus Limitation

by Xin Lin, Chentao Guo, Ling Li, Tangcheng Li and Senjie Lin

Microorganisms 2019, 7(8), 232; https://doi.org/10.3390/microorganisms7080232 - 01 Aug 2019

Cited by 7 | Viewed by 3318

Abstract

Alkaline phosphatase (AP) enables marine phytoplankton to utilize dissolved organic phosphorus (DOP) when dissolved inorganic phosphate (DIP) is depleted in the ocean. Dinoflagellate AP (Dino-AP) represents a newly classified atypical type of AP, PhoA^aty. Despite While being a conventional AP, PhoA^EC is known to recruit Zn²⁺ and Mg²⁺ in the active center, and the cofactors required by PhoA^aty have been contended and remain unclear. In this study, we investigated the metal ion requirement of AP in five dinoflagellate species. After AP activity was eliminated by using EDTA to chelate metal ions, the enzymatic activity could be recovered by the supplementation of Ca²⁺, Mg²⁺ and Mn²⁺ in all cases but not by that of Zn²⁺. Furthermore, the same analysis conducted on the purified recombinant ACAAP (AP of Amphidinium carterae) verified that the enzyme could be activated by Ca²⁺, Mg²⁺, and Mn²⁺ but not Zn²⁺. We further developed an antiserum against ACAAP, and a western blot analysis using this antibody showed a remarkable up-regulation of ACAAP under a phosphate limitation, consistent with elevated AP activity. The unconventional metal cofactor requirement of Dino-AP may be an adaptation to trace metal limitations in the ocean, which warrants further research to understand the niche differentiation between dinoflagellates and other phytoplankton that use Zn–Mg AP in utilizing DOP. Full article

(This article belongs to the Special Issue Dinoflagellate Biology in the Omics Era)

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40 pages, 2846 KiB

Open AccessArticle

DNA Damage Response Pathways in Dinoflagellates

by Chongping Li and Joseph Tin Yum Wong

Microorganisms 2019, 7(7), 191; https://doi.org/10.3390/microorganisms7070191 - 05 Jul 2019

Cited by 7 | Viewed by 7705

Abstract

Dinoflagellates are a general group of phytoplankton, ubiquitous in aquatic environments. Most dinoflagellates are non-obligate autotrophs, subjected to potential physical and chemical DNA-damaging agents, including UV irradiation, in the euphotic zone. Delay of cell cycles by irradiation, as part of DNA damage responses (DDRs), could potentially lead to growth inhibition, contributing to major errors in the estimation of primary productivity and interpretations of photo-inhibition. Their liquid crystalline chromosomes (LCCs) have large amount of abnormal bases, restricted placement of coding sequences at the chromosomes periphery, and tandem repeat-encoded genes. These chromosome characteristics, their large genome sizes, as well as the lack of architectural nucleosomes, likely contribute to possible differential responses to DNA damage agents. In this study, we sought potential dinoflagellate orthologues of eukaryotic DNA damage repair pathways, and the linking pathway with cell-cycle control in three dinoflagellate species. It appeared that major orthologues in photoreactivation, base excision repair, nucleotide excision repair, mismatch repair, double-strand break repair and homologous recombination repair are well represented in dinoflagellate genomes. Future studies should address possible differential DNA damage responses of dinoflagellates over other planktonic groups, especially in relation to possible shift of life-cycle transitions in responses to UV irradiation. This may have a potential role in the persistence of dinoflagellate red tides with the advent of climatic change. Full article

(This article belongs to the Special Issue Dinoflagellate Biology in the Omics Era)

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9 pages, 1972 KiB

Open AccessArticle

Fugacium Spliced Leader Genes Identified from Stranded RNA-Seq Datasets

by Yue Song, Bahareh Zaheri, Min Liu, Sunil Kumar Sahu, Huan Liu, Wenbin Chen, Bo Song and David Morse

Microorganisms 2019, 7(6), 171; https://doi.org/10.3390/microorganisms7060171 - 11 Jun 2019

Cited by 3 | Viewed by 3632

Abstract

Trans-splicing mechanisms have been documented in many lineages that are widely distributed phylogenetically, including dinoflagellates. The spliced leader (SL) sequence itself is conserved in dinoflagellates, although its gene sequences and arrangements have diversified within or across different species. In this study, we present 18 Fugacium kawagutii SL genes identified from stranded RNA-seq reads. These genes typically have a single SL but can contain several partial SLs with lengths ranging from 103 to 292 bp. Unexpectedly, we find the SL gene transcripts contain sequences upstream of the canonical SL, suggesting that generation of mature transcripts will require additional modifications following trans-splicing. We have also identified 13 SL-like genes whose expression levels and length are comparable to Dino-SL genes. Lastly, introns in these genes were identified and a new site for Sm-protein binding was proposed. Overall, this study provides a strategy for fast identification of SL genes and identifies new sequences of F. kawagutii SL genes to supplement our understanding of trans-splicing. Full article

(This article belongs to the Special Issue Dinoflagellate Biology in the Omics Era)

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25 pages, 3775 KiB

Open AccessArticle

Transcriptomic Responses to Thermal Stress and Varied Phosphorus Conditions in Fugacium kawagutii

by Senjie Lin, Liying Yu and Huan Zhang

Microorganisms 2019, 7(4), 96; https://doi.org/10.3390/microorganisms7040096 - 02 Apr 2019

Cited by 27 | Viewed by 5372

Abstract

Coral reef-associated Symbiodiniaceae live in tropical and oligotrophic environments and are prone to heat and nutrient stress. How their metabolic pathways respond to pulses of warming and phosphorus (P) depletion is underexplored. Here, we conducted RNA-seq analysis to investigate transcriptomic responses to thermal stress, phosphate deprivation, and organic phosphorus (OP) replacement in Fugacium kawagutii. Using dual-algorithm (edgeR and NOIseq) to remedy the problem of no replicates, we conservatively found 357 differentially expressed genes (DEGs) under heat stress, potentially regulating cell wall modulation and the transport of iron, oxygen, and major nutrients. About 396 DEGs were detected under P deprivation and 671 under OP utilization, both mostly up-regulated and potentially involved in photosystem and defensome, despite different KEGG pathway enrichments. Additionally, we identified 221 genes that showed relatively stable expression levels across all conditions (likely core genes), mostly catalytic and binding proteins. This study reveals a wide range of, and in many cases previously unrecognized, molecular mechanisms in F. kawagutii to cope with heat stress and phosphorus-deficiency stress. Their quantitative expression dynamics, however, requires further verification with triplicated experiments, and the data reported here only provide clues for generating testable hypotheses about molecular mechanisms underpinning responses and adaptation in F. kawagutii to temperature and nutrient stresses. Full article

(This article belongs to the Special Issue Dinoflagellate Biology in the Omics Era)

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25 pages, 1203 KiB

Open AccessReview

Omics Analysis for Dinoflagellates Biology Research

by Yali Bi, Fangzhong Wang and Weiwen Zhang

Microorganisms 2019, 7(9), 288; https://doi.org/10.3390/microorganisms7090288 - 23 Aug 2019

Cited by 18 | Viewed by 5569

Abstract

Dinoflagellates are important primary producers for marine ecosystems and are also responsible for certain essential components in human foods. However, they are also notorious for their ability to form harmful algal blooms, and cause shellfish poisoning. Although much work has been devoted to dinoflagellates in recent decades, our understanding of them at a molecular level is still limited owing to some of their challenging biological properties, such as large genome size, permanently condensed liquid-crystalline chromosomes, and the 10-fold lower ratio of protein to DNA than other eukaryotic species. In recent years, omics technologies, such as genomics, transcriptomics, proteomics, and metabolomics, have been applied to the study of marine dinoflagellates and have uncovered many new physiological and metabolic characteristics of dinoflagellates. In this article, we review recent application of omics technologies in revealing some of the unusual features of dinoflagellate genomes and molecular mechanisms relevant to their biology, including the mechanism of harmful algal bloom formations, toxin biosynthesis, symbiosis, lipid biosynthesis, as well as species identification and evolution. We also discuss the challenges and provide prospective further study directions and applications of dinoflagellates. Full article

(This article belongs to the Special Issue Dinoflagellate Biology in the Omics Era)

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19 pages, 1503 KiB

Open AccessReview

The Biochemistry and Evolution of the Dinoflagellate Nucleus

by Sebastian G. Gornik, Ian Hu, Imen Lassadi and Ross F. Waller

Microorganisms 2019, 7(8), 245; https://doi.org/10.3390/microorganisms7080245 - 08 Aug 2019

Cited by 25 | Viewed by 7678

Abstract

Dinoflagellates are known to possess a highly aberrant nucleus—the so-called dinokaryon—that exhibits a multitude of exceptional biological features. These include: (1) Permanently condensed chromosomes; (2) DNA in a cholesteric liquid crystalline state, (3) extremely large DNA content (up to 200 pg); and, perhaps most strikingly, (4) a deficit of histones—the canonical building blocks of all eukaryotic chromatin. Dinoflagellates belong to the Alveolata clade (dinoflagellates, apicomplexans, and ciliates) and, therefore, the biological oddities observed in dinoflagellate nuclei are derived character states. Understanding the sequence of changes that led to the dinokaryon has been difficult in the past with poor resolution of dinoflagellate phylogeny. Moreover, lack of knowledge of their molecular composition has constrained our understanding of the molecular properties of these derived nuclei. However, recent advances in the resolution of the phylogeny of dinoflagellates, particularly of the early branching taxa; the realization that divergent histone genes are present; and the discovery of dinoflagellate-specific nuclear proteins that were acquired early in dinoflagellate evolution have all thrown new light nature and evolution of the dinokaryon. Full article

(This article belongs to the Special Issue Dinoflagellate Biology in the Omics Era)

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29 pages, 2672 KiB

Open AccessReview

The Genetic Basis of Toxin Biosynthesis in Dinoflagellates

by Arjun Verma, Abanti Barua, Rendy Ruvindy, Henna Savela, Penelope A. Ajani and Shauna A. Murray

Microorganisms 2019, 7(8), 222; https://doi.org/10.3390/microorganisms7080222 - 29 Jul 2019

Cited by 51 | Viewed by 10070

Abstract

In marine ecosystems, dinoflagellates can become highly abundant and even dominant at times, despite their comparatively slow growth rates. One factor that may play a role in their ecological success is the production of complex secondary metabolite compounds that can have anti-predator, allelopathic, or other toxic effects on marine organisms, and also cause seafood poisoning in humans. Our knowledge about the genes involved in toxin biosynthesis in dinoflagellates is currently limited due to the complex genomic features of these organisms. Most recently, the sequencing of dinoflagellate transcriptomes has provided us with valuable insights into the biosynthesis of polyketide and alkaloid-based toxin molecules in dinoflagellate species. This review synthesizes the recent progress that has been made in understanding the evolution, biosynthetic pathways, and gene regulation in dinoflagellates with the aid of transcriptomic and other molecular genetic tools, and provides a pathway for future studies of dinoflagellates in this exciting omics era. Full article

(This article belongs to the Special Issue Dinoflagellate Biology in the Omics Era)

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10 pages, 3732 KiB

Open AccessReview

Architectural Organization of Dinoflagellate Liquid Crystalline Chromosomes

by Joseph Tin Yum Wong

Microorganisms 2019, 7(2), 27; https://doi.org/10.3390/microorganisms7020027 - 22 Jan 2019

Cited by 17 | Viewed by 5209

Abstract

Dinoflagellates have some of the largest genome sizes, but lack architectural nucleosomes. Their liquid crystalline chromosomes (LCCs) are the only non-architectural protein-mediated chromosome packaging systems, having high degrees of DNA superhelicity, liquid crystalline condensation and high levels of chromosomal divalent cations. Recent observations on the reversible decompaction–recompaction of higher-order structures implicated that LCCs are composed of superhelical modules (SPMs) comprising highly supercoiled DNA. Orientated polarizing light photomicrography suggested the presence of three compartments with different packaging DNA density in LCCs. Recent and previous biophysical data suggest that LCCs are composed of: (a) the highly birefringent inner core compartment (i) with a high-density columnar-hexagonal mesophase (CH-m); (b) the lower-density core surface compartment (ii.1) consisting of a spiraling chromonema; (c) the birefringent-negative periphery compartment (ii.2) comprising peripheral chromosomal loops. C(ii.1) and C(ii.2) are in dynamic equilibrium, and can merge into a single compartment during dinomitosis, regulated through multiphasic reversible soft-matter phase transitions. Full article

(This article belongs to the Special Issue Dinoflagellate Biology in the Omics Era)

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22 pages, 1977 KiB

Open AccessReview

Distinctive Nuclear Features of Dinoflagellates with A Particular Focus on Histone and Histone-Replacement Proteins

by Sadaf Riaz, Zhenghong Sui, Zeeshan Niaz, Sohrab Khan, Yuan Liu and Haoxin Liu

Microorganisms 2018, 6(4), 128; https://doi.org/10.3390/microorganisms6040128 - 14 Dec 2018

Cited by 13 | Viewed by 5085

Abstract

Dinoflagellates are important eukaryotic microorganisms that play critical roles as producers and grazers, and cause harmful algal blooms. The unusual nuclei of dinoflagellates “dinokaryon” have led researchers to investigate their enigmatic nuclear features. Their nuclei are unusual in terms of their permanently condensed nucleosome-less chromatin, immense genome, low protein to DNA ratio, guanine-cytosine rich methylated DNA, and unique mitosis process. Furthermore, dinoflagellates are the only known group of eukaryotes that apparently lack histone proteins. Over the course of evolution, dinoflagellates have recruited other proteins, e.g., histone-like proteins (HLPs), from bacteria and dinoflagellates/viral nucleoproteins (DVNPs) from viruses as histone substitutes. Expression diversity of these nucleoproteins has greatly influenced the chromatin structure and gene expression regulation in dinoflagellates. Histone replacement proteins (HLPs and DVNPs) are hypothesized to perform a few similar roles as histone proteins do in other eukaryotes, i.e., gene expression regulation and repairing DNA. However, their role in bulk packaging of DNA is not significant as low amounts of proteins are associated with the gigantic genome. This review intends to summarize the discoveries encompassing unique nuclear features of dinoflagellates, particularly focusing on histone and histone replacement proteins. In addition, a comprehensive view of the evolution of dinoflagellate nuclei is presented. Full article

(This article belongs to the Special Issue Dinoflagellate Biology in the Omics Era)

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