Sunlight concurrently reduces Prymnesium parvum elicited acute toxicity to fish and prymnesins

Taylor, Raegyn B.; Hill, Bridgett N.; Langan, Laura M.; Chambliss, C. Kevin; Brooks, Bryan W.

doi:10.1016/j.chemosphere.2020.127927

Cited by 14 publications

(7 citation statements)

References 34 publications

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“…We obtained Hi-C scaffolded, highly contiguous genome assemblies of two P. parvum strains from Texas: UTEX 2797 and 12B1. UTEX 2797 was selected for sequencing due to its use in numerous toxicology and physiology experiments of P. parvum ( e.g., 19,20,22,[27][28][29][30][31][32]. However, preliminary analysis of k-mer frequencies revealed that UTEX 2797 displays high sequence-level heterozygosity (Fig.…”

Section: Resultsmentioning

confidence: 99%

Extreme genome diversity and cryptic speciation in a harmful algal bloom forming eukaryote

Wisecaver

Auber

Pendleton

et al. 2022

Preprint

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Harmful algal blooms (HABs) of the toxic haptophyte Prymnesium parvum are a recurrent problem in many inland and estuarine waters around the world. Strains of P. parvum vary in the toxins they produce and in other physiological traits associated with HABs, but the genetic basis for this variation is unknown. To investigate genome diversity in this morphospecies, we generated genome assemblies for fifteen phylogenetically and geographically diverse strains of P. parvum including Hi-C guided, near-chromosome level assemblies for two strains. Comparative analysis revealed considerable DNA content variation between strains, ranging from 115 Mbp to 845 Mbp. Strains included haploids, diploids, and polyploids, but not all differences in DNA content were due to variation in genome copy number. Haploid genome size between strains of different chemotypes differed by as much as 243 Mbp. Syntenic and phylogenetic analyses indicate that UTEX 2797, a common laboratory strain from Texas, is a hybrid that retains two phylogenetically distinct haplotypes. Investigation of gene families variably present across strains identified several functional categories associated with metabolism, including candidates for the biosynthesis of toxic metabolites, as well as genome size variation, including recent proliferations of transposable elements. Together, our results indicate that P. parvum is comprised of multiple cryptic species. These genomes provide a robust phylogenetic and genomic framework for investigations into the eco-physiological consequences of the intra- and inter-specific genetic variation present in P. parvum and demonstrate the need for similar resources for other HAB-forming morphospecies.

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Section: Resultsmentioning

confidence: 99%

Extreme genome diversity and cryptic speciation in a harmful algal bloom forming eukaryote

Wisecaver

Auber

Pendleton

et al. 2022

Preprint

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“…A number of environmental factors such as pH, irradiance/sunlight, temperature, salinity, and nutrient availability have an impact on the growth of P . parvum , toxin content and toxin production (Hill et al 2020 ; Manning and La Claire 2010 ; Medić et al 2022 ; Svenssen et al 2019 ; Taylor et al 2021 ). However, many more studies are required to understand the production and release of PRMs.…”

Section: Discussionmentioning

confidence: 99%

Cytotoxicity of Prymnesium parvum extracts and prymnesin analogs on epithelial fish gill cells RTgill-W1 and the human colon cell line HCEC-1CT

Varga,

Prause,

Riepl

et al. 2024

Arch Toxicol

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Harmful algal blooms kill fish populations worldwide, as exemplified by the haptophyte microalga Prymnesium parvum. The suspected causative agents are prymnesins, categorized as A-, B-, and C-types based on backbone carbon atoms. Impacts of P. parvum extracts and purified prymnesins were tested on the epithelial rainbow trout fish gill cell line RTgill-W1 and on the human colon epithelial cells HCEC-1CT. Cytotoxic potencies ranked A > C > B-type with concentrations spanning from low (A- and C-type) to middle (B-type) nM ranges. Although RTgill-W1 cells were about twofold more sensitive than HCEC-1CT, the cytotoxicity of prymnesins is not limited to fish gills. Both cell lines responded rapidly to prymnesins; with EC50 values for B-types in RTgill-W1 cells of 110 ± 11 nM and 41.5 ± 0.6 nM after incubations times of 3 and 24 h. Results of fluorescence imaging and measured lytic effects suggest plasma membrane interactions. Postulating an osmotic imbalance as mechanisms of toxicity, incubations with prymnesins in media lacking either Cl−, Na+, or Ca2+ were performed. Cl− removal reduced morphometric rearrangements observed in RTgill-W1 and cytotoxicity in HCEC-1CT cells. Ca2+-free medium in RTgill-W1 cells exacerbated effects on the cell nuclei. Prymnesin composition of different P. parvum strains showed that analog composition within one type scarcely influenced the cytotoxic potential, while analog type potentially dictate potency. Overall, A-type prymnesins were the most potent ones in both cell lines followed by the C-types, and lastly B-types. Disturbance of Ca2+ and Cl− ionoregulation may be integral to prymnesin toxicity.

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“…In a previous study, the suspect list for Skeletonema spp was published (51). For the present study, we assembled a suspect list for Prymnesium parvum as well, using different databases: compound, reaction, pathway, and enzyme databases such as Kyoto Encyclopedia of Genes and Genomes (KEGG) (64–66), Comprehensive Marine Natural Products Database (CMNPD) (67), Chemical Entities of Biological Interest (ChEBI) (68), PubChem (69, 70), Universal Protein Resource (UniProt) (71), BRaunschweig ENzyme DAtabase (BRENDA) (72), MetaboLights (73, 74), MetaCyc (75, 76), and different publications on P. parvum metabolites (77–82). Suspect list was curated with RDKit (83), PubChemPy (84), and pybatchclassyfire (85).…”

Section: Methodsmentioning

confidence: 99%

Analysis of Metabolomics and Transcriptomics Data to Assess Interactions in Microalgal Co-culture ofSkeletonema marinoiandPrymnesium parvum

Zulfiqar,

Abel,

Barth

et al. 2023

Preprint

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In marine ecosystems, microbial communities often interact using specialised metabolites, which play a central role in shaping the dynamics of the ecological networks and maintaining the balance of the ecosystem. With metabolomics and transcriptomics analyses, this study explores the interactions between two marine microalgae,Skeletonema marinoiandPrymnesium parvum, grown in mono-cultures and non-contact co-cultures. As a growth indicator, the photosynthetic potential, measured via fluorescence, suggested chemical interaction betweenS. marinoiandP. parvum. Using Liquid Chromatography-Mass Spectrometry (LC-MS) data, we identified 346 and 521 differentially produced features in the endo- and exometabolome ofS. marinoiandP. parvum, respectively. Despite limited tandem mass spectrometry data (MS2) for these features, we structurally annotated 14 compounds, most of which were previously under-studied specialised metabolites. Differential gene expression analysis was then performed on the transcriptomes of the microalgae, which uncovered differentially expressed genes involved in energy metabolism and cellular repair for both species. These metabolic and transcriptomics changes depict the adaptation of both species in the co-culture. However, further data acquisition and investigation will be necessary to confirm the type of interaction and the underlying mechanisms.ImportanceMarine microalgae have great ecological importance and biochemical potential. Among these microbes are the diatomSkeletonema marinoi, known for its marine biogeochemical cycling, and the haptophytePrymnesium parvum, which poses adverse environmental consequences. Given these opposing roles for the two cosmopolitan microalgae, we designed a study using untargeted metabolomics and transcriptomics to acquire a comprehensive snapshot of their interactions, grown as mono-cultures and co-cultures. The statistical analysis of the chlorophyllafluorescence levels, and the metabolomics and transcriptomics dataset revealed metabolic communication occurring among the two species via specialised metabolites and activated cellular repair mechanisms. These findings reveal the complexity of the interactions within marine microbial ecosystems, offering a foundation for future research to understand and harness marine ecological systems.

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Sunlight concurrently reduces Prymnesium parvum elicited acute toxicity to fish and prymnesins

Cited by 14 publications

References 34 publications

Extreme genome diversity and cryptic speciation in a harmful algal bloom forming eukaryote

Extreme genome diversity and cryptic speciation in a harmful algal bloom forming eukaryote

Cytotoxicity of Prymnesium parvum extracts and prymnesin analogs on epithelial fish gill cells RTgill-W1 and the human colon cell line HCEC-1CT

Analysis of Metabolomics and Transcriptomics Data to Assess Interactions in Microalgal Co-culture ofSkeletonema marinoiandPrymnesium parvum

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