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Scientific Reports Aug 2023Nitrogen (N) and phosphorus (P) are essential elements whose availability promotes successful growth of phytoplankton and governs aquatic primary productivity. In this...
Nitrogen (N) and phosphorus (P) are essential elements whose availability promotes successful growth of phytoplankton and governs aquatic primary productivity. In this study, we investigated the effect of N and/or P deficiency on the sexual reproduction of Prorocentrum cordatum, the dinoflagellate with the haplontic life cycle which causes harmful algal blooms worldwide. In P. cordatum cultures, N and the combined N and P deficiency led to the arrest of the cell cycle in the G/G phases and attenuation of cell culture growth. We observed, that P, but not N deficiency triggered the transition in the life cycle of P. cordatum from vegetative to the sexual stage. This resulted in a sharp increase in percentage of cells with relative nuclear DNA content 2C (zygotes) and the appearance of cells with relative nuclear DNA content 4C (dividing zygotes). Subsequent supplementation with phosphate stimulated meiosis and led to a noticeable increase in the 4C cell number (dividing zygotes). Additionally, we performed transcriptomic data analysis and identified putative phosphate transporters and enzymes involved in the phosphate uptake and regulation of its metabolism by P. cordatum. These include high- and low-affinity inorganic phosphate transporters, atypical alkaline phosphatase, purple acid phosphatases and SPX domain-containing proteins.
Topics: Dinoflagellida; Phosphorus; Reproduction; Phosphates; Meiosis
PubMed: 37648777
DOI: 10.1038/s41598-023-41339-3 -
Microbiome Jul 2022The importance of symbiosis has long been recognized on coral reefs, where the photosynthetic dinoflagellates of corals (Symbiodiniaceae) are the primary symbiont....
BACKGROUND
The importance of symbiosis has long been recognized on coral reefs, where the photosynthetic dinoflagellates of corals (Symbiodiniaceae) are the primary symbiont. Numerous studies have now shown that a diverse assemblage of prokaryotes also make-up part of the microbiome of corals. A subset of these prokaryotes is capable of fixing nitrogen, known as diazotrophs, and is also present in the microbiome of scleractinian corals where they have been shown to supplement the holobiont nitrogen budget. Here, an analysis of the microbiomes of 16 coral species collected from Australia, Curaçao, and Hawai'i using three different marker genes (16S rRNA, nifH, and ITS2) is presented. These data were used to examine the effects of biogeography, coral traits, and ecological life history characteristics on the composition and diversity of the microbiome in corals and their diazotrophic communities.
RESULTS
The prokaryotic microbiome community composition (i.e., beta diversity) based on the 16S rRNA gene varied between sites and ecological life history characteristics, but coral morphology was the most significant factor affecting the microbiome of the corals studied. For 15 of the corals studied, only two species Pocillopora acuta and Seriotopora hystrix, both brooders, showed a weak relationship between the 16S rRNA gene community structure and the diazotrophic members of the microbiome using the nifH marker gene, suggesting that many corals support a microbiome with diazotrophic capabilities. The order Rhizobiales, a taxon that contains primarily diazotrophs, are common members of the coral microbiome and were eight times greater in relative abundances in Hawai'i compared to corals from either Curacao or Australia. However, for the diazotrophic component of the coral microbiome, only host species significantly influenced the composition and diversity of the community.
CONCLUSIONS
The roles and interactions between members of the coral holobiont are still not well understood, especially critical functions provided by the coral microbiome (e.g., nitrogen fixation), and the variation of these functions across species. The findings presented here show the significant effect of morphology, a coral "super trait," on the overall community structure of the microbiome in corals and that there is a strong association of the diazotrophic community within the microbiome of corals. However, the underlying coral traits linking the effects of host species on diazotrophic communities remain unknown. Video Abstract.
Topics: Animals; Anthozoa; Coral Reefs; Dinoflagellida; Microbiota; Nitrogen; RNA, Ribosomal, 16S; Symbiosis
PubMed: 35902906
DOI: 10.1186/s40168-022-01308-w -
Environmental Microbiology Dec 2022Protistan algae (phytoplankton) dominate coastal upwelling ecosystems where they form massive blooms that support the world's most important fisheries and constitute an...
Protistan algae (phytoplankton) dominate coastal upwelling ecosystems where they form massive blooms that support the world's most important fisheries and constitute an important sink for atmospheric CO . Bloom initiation is well understood, but the biotic and abiotic forces that shape short-term dynamics in community composition are still poorly characterized. Here, high-frequency (daily) changes in relative abundance dynamics of the metabolically active protistan community were followed via expressed 18S V4 rRNA genes (RNA) throughout two algal blooms during the spring of 2018 and 2019 in Santa Monica Bay (central Southern California Bight). A diatom bloom formed after wind-driven, nutrient upwelling events in both years, but different taxa dominated each year. Whereas diatoms bloomed following elevated nutrients and declined after depletion each year, a massive dinoflagellate bloom manifested under relatively low inorganic nitrogen conditions following diatom bloom senescence in 2019 but not 2018. Network analysis revealed associations between diatoms and cercozoan putative parasitic taxa and syndinean parasites during 2019 that may have influenced the demise of the diatoms, and the transition to a dinoflagellate-dominated bloom.
Topics: Ecosystem; Bays; Eutrophication; Phytoplankton; Diatoms; Dinoflagellida
PubMed: 35880671
DOI: 10.1111/1462-2920.16137 -
Marine Drugs May 2022The dinoflagellate , often called , is a potentially toxic alga found in algal blooms. Volatile compounds released by the alga might carry important information, e.g.,...
The dinoflagellate , often called , is a potentially toxic alga found in algal blooms. Volatile compounds released by the alga might carry important information, e.g., on its physiological state, and may act as chemical messengers. We report here the identification of volatile organic compounds emitted by two strains, xenic CCMP 1529 and axenic CCMP 1329. The volatiles released during culture were identified despite their low production rates, using sensitive methods such as open-system-stripping analysis (OSSA) on Tenax TA desorption tubes, thermodesorption, cryofocusing and GC/MS-analysis. The analyses revealed 16 compounds released from the xenic strain and 52 compounds from the axenic strain. The majority of compounds were apocarotenoids, aromatic compounds and small oxylipins, but new natural products such as 3,7-dimethyl-4-octanolide were also identified and synthesized. The large difference of compound composition between xenic and axenic algae will be discussed.
Topics: Dinoflagellida; Eutrophication; Gas Chromatography-Mass Spectrometry; Volatile Organic Compounds
PubMed: 35736174
DOI: 10.3390/md20060371 -
Toxins Sep 2021As a sequel to our previous report of the existence of species-specific protein/peptide expression profiles (PEPs) acquired by mass spectrometry in some dinoflagellates,...
As a sequel to our previous report of the existence of species-specific protein/peptide expression profiles (PEPs) acquired by mass spectrometry in some dinoflagellates, we established, with the help of a plasma-membrane-impermeable labeling agent, a surface amphiesmal protein extraction method (SAPE) to label and capture species-specific surface proteins (SSSPs) as well as saxitoxins-producing-species-specific surface proteins (Stx-SSPs) that face the extracellular space (i.e., SSSPs and Stx-SSPs). Five selected toxic dinoflagellates, , and were used in this study. Transcriptomic databases of these five species were also constructed. With the aid of liquid chromatography linked-tandem mass spectrometry (LC-MS/MS) and the transcriptomic databases of these species, extracellularly facing membrane proteomes of the five different species were identified. Within these proteomes, 16 extracellular-facing and functionally significant transport proteins were found. Furthermore, 10 SSSPs and 6 Stx-SSPs were identified as amphiesmal proteins but not facing outward to the extracellular environment. We also found SSSPs and Stx-SSPs in the proteomes. The potential functional correlation of these proteins towards the production of saxitoxins in dinoflagellates and the degree of species specificity were discussed accordingly.
Topics: Algal Proteins; Chromatography, Liquid; Dinoflagellida; Proteome; Protozoan Proteins; Species Specificity; Tandem Mass Spectrometry
PubMed: 34564629
DOI: 10.3390/toxins13090624 -
Microbiome Mar 2021Phytoplankton blooms are frequent events in coastal areas and increase the production of organic matter that initially shapes the growth of opportunistic heterotrophic...
BACKGROUND
Phytoplankton blooms are frequent events in coastal areas and increase the production of organic matter that initially shapes the growth of opportunistic heterotrophic bacteria. However, it is unclear how these opportunists are involved in the transformation of dissolved organic matter (DOM) when blooms occur and the subsequent impacts on biogeochemical cycles.
RESULTS
We used a combination of genomic, proteomic, and metabolomic approaches to study bacterial diversity, genome traits, and metabolic responses to assess the source and lability of DOM in a spring coastal bloom of Akashiwo sanguinea. We identified molecules that significantly increased during bloom development, predominantly belonging to amino acids, dipeptides, lipids, nucleotides, and nucleosides. The opportunistic members of the bacterial genera Polaribacter, Lentibacter, and Litoricola represented a significant proportion of the free-living and particle-associated bacterial assemblages during the stationary phase of the bloom. Polaribacter marinivivus, Lentibacter algarum, and Litoricola marina were isolated and their genomes exhibited streamlining characterized by small genome size and low GC content and non-coding densities, as well as a smaller number of transporters and peptidases compared to closely related species. However, the core proteomes identified house-keeping functions, such as various substrate transporters, peptidases, motility, chemotaxis, and antioxidants, in response to bloom-derived DOM. We observed a unique metabolic signature for the three species in the utilization of multiple dissolved organic nitrogen compounds. The metabolomic data showed that amino acids and dipeptides (such as isoleucine and proline) were preferentially taken up by P. marinivivus and L. algarum, whereas nucleotides and nucleosides (such as adenosine and purine) were preferentially selected by L. marina.
CONCLUSIONS
The results suggest that the enriched DOM in stationary phase of phytoplankton bloom is a result of ammonium depletion. This environment drives genomic streamlining of opportunistic bacteria to exploit their preferred nitrogen-containing compounds and maintain nutrient cycling. Video abstract.
Topics: Dinoflagellida; Flavobacteriaceae; Gammaproteobacteria; Nitrogen Compounds; Proteomics; Rhodobacteraceae
PubMed: 33762013
DOI: 10.1186/s40168-021-01022-z -
Marine Drugs May 2021Toxic dinoflagellate spp. produce saxitoxins (STXs), whose biosynthesis pathway is affected by temperature. However, the link between the regulation of the relevant...
Toxic dinoflagellate spp. produce saxitoxins (STXs), whose biosynthesis pathway is affected by temperature. However, the link between the regulation of the relevant genes and STXs' accumulation and temperature is insufficiently understood. In the present study, we evaluated the effects of temperature on cellular STXs and the expression of two core STX biosynthesis genes ( and ) in the toxic dinoflagellate Alex03 isolated from Korean waters. We analyzed the growth rate, toxin profiles, and gene responses in cells exposed to different temperatures, including long-term adaptation (12, 16, and 20 °C) and cold and heat stresses. Temperature significantly affected the growth of , with optimal growth (0.49 division/day) at 16 °C and the largest cell size (30.5 µm) at 12 °C. High concentration of STXs eq were detected in cells cultured at 16 °C (86.3 fmol/cell) and exposed to cold stress at 20→12 °C (96.6 fmol/cell) compared to those at 20 °C and exposed to heat stress. Quantitative real-time PCR (qRT-PCR) revealed significant gene expression changes of in cells cultured at 16 °C (1.8-fold) and cold shock at 20→16 °C (9.9-fold). In addition, was significantly induced in cells exposed to cold shocks (20→16 °C; 19.5-fold) and heat stress (12→20 °C; 25.6-fold). Principal component analysis (PCA) revealed that low temperature (12 and 16 °C) and cold stress were positively related with STXs' production and gene expression levels. These results suggest that temperature may affect the toxicity and regulation of STX biosynthesis genes in dinoflagellates.
Topics: Cell Enlargement; Cell Proliferation; Cold Temperature; Cold-Shock Response; Dinoflagellida; Gene Expression Regulation; Principal Component Analysis; Protein Biosynthesis; Protozoan Proteins; Saxitoxin
PubMed: 34064031
DOI: 10.3390/md19060291 -
MSphere Aug 2023The marine, bloom-forming dinoflagellate CCMP 1329 (formerly ) has a genome atypical of eukaryotes, with a large size of ~4.15 Gbp, organized in plentiful, highly...
The marine, bloom-forming dinoflagellate CCMP 1329 (formerly ) 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 . 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), 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 belongs to the harmful algal bloom-forming, marine dinoflagellates and has a recently assembled genome. We present a detailed 3D reconstruction of the 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.
Topics: Dinoflagellida; Proteomics; Ecosystem; Cell Nucleus; Nuclear Proteins
PubMed: 37358287
DOI: 10.1128/msphere.00038-23 -
Scientific Reports Nov 2022As coral reefs face warming oceans and increased coral bleaching, a whitening of the coral due to loss of microalgal endosymbionts, the possibility of evolutionary...
As coral reefs face warming oceans and increased coral bleaching, a whitening of the coral due to loss of microalgal endosymbionts, the possibility of evolutionary rescue offers some hope for reef persistence. In tightly linked mutualisms, evolutionary rescue may occur through evolution of the host and/or endosymbionts. Many obligate mutualisms are composed of relatively small, fast-growing symbionts with greater potential to evolve on ecologically relevant time scales than their relatively large, slower growing hosts. Numerous jellyfish species harbor closely related endosymbiont taxa to other cnidarian species such as coral, and are commonly used as a model system for investigating cnidarian mutualisms. We examined the potential for adaptation of the upside-down jellyfish Cassiopea xamachana to increased temperature via evolution of its microalgal endosymbiont, Symbiodinium microadriaticum. We quantified trait variation among five algal genotypes in response to three temperatures (26 °C, 30 °C, and 32 °C) and fitness of hosts infected with each genotype. All genotypes showed positive growth rates at each temperature, but rates of respiration and photosynthesis decreased with increased temperature. Responses varied among genotypes but were unrelated to genetic similarity. The effect of temperature on asexual reproduction and the timing of development in the host also depended on the genotype of the symbiont. Natural selection could favor different algal genotypes at different temperatures, affecting host fitness. This eco-evolutionary interaction may be a critical component of understanding species resilience in increasingly stressful environments.
Topics: Animals; Temperature; Coral Reefs; Anthozoa; Dinoflagellida; Symbiosis; Genotype
PubMed: 36319835
DOI: 10.1038/s41598-022-23244-3 -
Toxins Oct 2022Numerous potentially toxic plankton species commonly occur in the Black Sea, and phycotoxins have been reported. However, the taxonomy, phycotoxin profiles, and...
Numerous potentially toxic plankton species commonly occur in the Black Sea, and phycotoxins have been reported. However, the taxonomy, phycotoxin profiles, and distribution of harmful microalgae in the basin are still understudied. An integrated microscopic (light microscopy) and molecular (18S rRNA gene metabarcoding and qPCR) approach complemented with toxin analysis was applied at 41 stations in the northwestern part of the Black Sea for better taxonomic coverage and toxin profiling in natural populations. The combined dataset included 20 potentially toxic species, some of which (, , , and ) were detected in over 95% of the stations. In parallel, pectenotoxins (PTX-2 as a major toxin) were registered in all samples, and yessotoxins were present at most of the sampling points. PTX-1 and PTX-13, as well as some YTX variants, were recorded for the first time in the basin. A positive correlation was found between the cell abundance of and pectenotoxins, and between and and yessotoxins. Toxic microalgae and toxin variant abundance and spatial distribution was associated with environmental parameters. Despite the low levels of the identified phycotoxins and their low oral toxicity, chronic toxic exposure could represent an ecosystem and human health hazard.
Topics: Humans; Marine Toxins; Microalgae; Ecosystem; Black Sea; Dinoflagellida
PubMed: 36287954
DOI: 10.3390/toxins14100685