Ultrastructural organization of the chromatin elements in chromosomes of the dinoflagellate Prorocentrum minimum

Golyshev, Sergey A.; Berdieva, Mariia; Musinova, Yana R.; Sheval, Eugene V.; Skarlato, Sergei

doi:10.21685/1680-0826-2018-12-4-1

Cited by 2 publications

(2 citation statements)

References 25 publications

(32 reference statements)

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“…The chromosomes are tightly packed in the nucleus ( Fig. 1B ; Movie S2), which agrees with multiple observations previously reported for P. cordatum ( 48 ) and other dinoflagellates ( 10 , 38 , 40 , 49 ). The nucleolus was found to interact with several chromosomes ( Fig.…”

Section: Resultssupporting

confidence: 91%

The enigmatic nucleus of the marine dinoflagellate Prorocentrum cordatum

Kalvelage,

Wöhlbrand,

Schoon

et al. 2023

mSphere

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The marine, bloom-forming dinoflagellate Prorocentrum cordatum CCMP 1329 (formerly P. minimum ) has a genome atypical of eukaryotes, with a large size of ~4.15 Gbp, organized in plentiful, highly condensed chromosomes and packed in a dinoflagellate-specific nucleus (dinokaryon). Here, we apply microscopic and proteogenomic approaches to obtain new insights into this enigmatic nucleus of axenic P. cordatum . High-resolution focused ion beam/scanning electron microscopy analysis of the flattened nucleus revealed highest density of nuclear pores in the vicinity of the nucleolus, a total of 62 tightly packed chromosomes (~0.4–6.7 µm 3 ), and interaction of several chromosomes with the nucleolus and other nuclear structures. A specific procedure for enriching intact nuclei was developed to enable proteomic analyses of soluble and membrane protein-enriched fractions. These were analyzed with geLC and shotgun approaches employing ion-trap and timsTOF (trapped-ion-mobility-spectrometry time-of-flight) mass spectrometers, respectively. This allowed identification of 4,052 proteins (39% of unknown function), out of which 418 were predicted to serve specific nuclear functions; additional 531 proteins of unknown function could be allocated to the nucleus. Compaction of DNA despite very low histone abundance could be accomplished by highly abundant major basic nuclear proteins (HCc2-like). Several nuclear processes including DNA replication/repair and RNA processing/splicing can be fairly well explained on the proteogenomic level. By contrast, transcription and composition of the nuclear pore complex remain largely elusive. One may speculate that the large group of potential nuclear proteins with currently unknown functions may serve yet to be explored functions in nuclear processes differing from those of typical eukaryotic cells. IMPORTANCE Dinoflagellates form a highly diverse group of unicellular microalgae. They provide keystone species for the marine ecosystem and stand out among others by their very large, unusually organized genomes embedded in the nuclei markedly different from other eukaryotic cells. Functional insights into nuclear and other cell biological structures and processes of dinoflagellates have long been hampered by the paucity of available genomic sequences. The here studied cosmopolitan P. cordatum belongs to the harmful algal bloom-forming, marine dinoflagellates and has a recently de novo assembled genome. We present a detailed 3D reconstruction of the P. cordatum nucleus together with comprehensive proteogenomic insights into the protein equipment mastering the broad spectrum of nuclear processes. This study significantly advances our understanding of mechanisms and evolution of the conspicuous dinoflagellate cell biology.

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Section: Resultssupporting

confidence: 91%

The enigmatic nucleus of the marine dinoflagellate Prorocentrum cordatum

Kalvelage,

Wöhlbrand,

Schoon

et al. 2023

mSphere

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“…Given that mathematical deduction from this “higher-order waveform” was the basis of the previously proposed cholesteric model [35], the accompanying interpretation of a single cholesterite could not be substantiated; Ethanol (30%) was the fixative agent during the sample preparation for SIMS imaging of the divalent cation [16], however, ethanol (>20%) induced different structures in non-nucleosomal DNAs [36]. The secondary ion mass spectroscopic-imaged holes were likely to be actual space, incurred by ethanol-induced DNA structural changes, and an architectural protein core would not be consistent with low basic chromosomal protein concentrations [37,38]. Ethanol exhibited a conservation effect on LCC Mg 2+ concentrations, indicating that a proportion of higher divalent cation was attributed to counterions, which would not be disrupted by ethanol.…”

Section: Superhelical Plectonemic Modules (Spms) and Compartmentationmentioning

confidence: 99%

Architectural Organization of Dinoflagellate Liquid Crystalline Chromosomes

Wong

2019

Microorganisms

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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.

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Ultrastructural organization of the chromatin elements in chromosomes of the dinoflagellate Prorocentrum minimum

Cited by 2 publications

References 25 publications

The enigmatic nucleus of the marine dinoflagellate Prorocentrum cordatum

The enigmatic nucleus of the marine dinoflagellate Prorocentrum cordatum

Architectural Organization of Dinoflagellate Liquid Crystalline Chromosomes

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