Polyketide synthase genes and molecular trade-offs in the ichthyotoxic species Prymnesium parvum

Anestis, Konstantinos; Kohli, Gurjeet S.; Wohlrab, Sylke; Varga, Elisabeth; Larsen, Thomas Ostenfeld; Hansen, Per Juel; John, Uwe

doi:10.1016/j.scitotenv.2021.148878

Cited by 15 publications

(23 citation statements)

References 67 publications

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“…Because the most closely related haptophyte species with sequenced genomes were too divergent to serve as outgroups for a nucleotide-based phylogeny, a nonreversible substitution model was used to evaluate support for different root locations on the P. parvum species tree (42). The root with the highest likelihood score caused the C-type prymnesin producers to be paraphyletic, which is a phylogenetic pattern also observed in a prior 18S rDNA phylogeny (20). However, 'rootstrap' support for this root location was low (68%), and two alternative root locations, including one in which C-type producers were monophyletic, could not be rejected (AU tree topology test Pvalues > 0.1; 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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“…These toxins mostly kill fish and appear to have little effect on cattle or humans. Although harmful effects to humans are unknown, it is not recommended to consume dead or dying fish that have been exposed to P. parvum blooms [ 123 , 124 , 125 , 126 ].…”

Section: Polyether Ionophores Derived From Marine Algae and Invertebr...mentioning

confidence: 99%

Natural Polyether Ionophores and Their Pharmacological Profile

Dembitsky

2022

Marine Drugs

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This review is devoted to the study of the biological activity of polyether ionophores produced by bacteria, unicellular marine algae, red seaweeds, marine sponges, and coelenterates. Biological activities have been studied experimentally in various laboratories, as well as data obtained using QSAR (Quantitative Structure–Activity Relationships) algorithms. According to the data obtained, it was shown that polyether toxins exhibit strong antibacterial, antimicrobial, antifungal, antitumor, and other activities. Along with this, it was found that natural polyether ionophores exhibit such properties as antiparasitic, antiprotozoal, cytostatic, anti-mycoplasmal, and antieczema activities. In addition, polyethers have been found to be potential regulators of lipid metabolism or inhibitors of DNA synthesis. Further study of the mechanisms of action and the search for new polyether ionophores and their derivatives may provide more effective therapeutic natural polyether ionophores for the treatment of cancer and other diseases. For some polyether ionophores, 3D graphs are presented, which demonstrate the predicted and calculated activities. The data presented in this review will be of interest to pharmacologists, chemists, practical medicine, and the pharmaceutical industry.

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“…Toxin extraction and quantification was performed according to a previously described protocol (Svenssen et al , 2019), with small modifications as described in Anestis et al , 2021. In brief, cells were collected on 22 mm glass microfiber filters (Whatman GF/F, Maidstone, UK; nominal pore size: 0.7 μm). The biomass on each filter was extracted two times with 20 mL MeOH each using an ultrasonic batch for 30 min with a centrifugation step in between (4300 ×g for 15 min at 4 °C).…”

Section: Physiological Parameters Sampling and Processingmentioning

confidence: 99%

“…Polyketide synthase genes have previously been reported inP. parvum strains that produce different types of prymnesins (Anestis et al , 2021), however, the development of efficient genetic manipulation techniques would be required for better understanding of the connection between gene and product. In the current study, the expression of PKSs was strongly influenced by cell density, coinciding with higher cellular content of prymnesins.…”

Section: Polyketide Synthasesmentioning

confidence: 99%

“…The production of lytic compounds by P. parvum , whether studied using bioassays or by actual measurements of prymnesins, are known to be influenced by phosphorus (P) availability, light and temperature ( (Beszteri et al , 2012;Qin et al , 2020;Taylor et al , 2020Taylor et al , , 2021Medić et al , 2022). Most probably, prymnesins are produced by polyketide synthases (PKS) of the modular type I (Anestis et al , 2021). The release of lytic compounds by P. parvum into the surrounding water has been shown to assist feeding, via immobilization and lysis of the prey, which allows uptake of nutrients through either osmotrophy or phagotrophy (Skovgaard and Hansen, 2003;Tillmann, 2003).…”

Section: Introductionmentioning

confidence: 99%

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The relationship between toxicity and mixotrophy in bloom dynamics of the ichthyotoxic Prymnesium parvum

Anestis

Wohlrab

Varga

et al. 2022

Preprint

Self Cite

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Toxin production in planktonic protists is widespread and comprises an effective mechanism to eliminate competitors or grazers. Toxins released into the water can mediate the immobilization of prey for subsequent consumption or can mediate the lysis and uptake of the released nutrients. For the worldwide-distributed ichthyotoxic and mixotrophic haptophyte Prymnesium parvum, the relationship between toxin production; impact on co-occurring species, and mixotrophy remains blurred. In the current study, we show that changes in salinities (5 vs 30), phosphorous (P) availabilities (P-replete vs P-deplete) and cell densities affect growth, toxicity and mixotrophy in P. parvum. Cell density positively affected cellular toxin content by a factor of up to 10. Low salinity resulted in a higher mortality of the cryptophyte prey Teleaulax acuta, with ~80% of cells being lysed after 2 h of incubation. However, phagotrophic rates were higher in P-deplete conditions, independent of the salinity. Transcriptomic analysis of the monocultures revealed the up-regulation of genes involved in endocytosis under either low salinity and phosphorous, suggesting that this process is evolutionarily conserved, triggered by environmental stressors and independent of prey presence. Polyketide synthase genes, potentially involved in toxin biosynthesis, exhibited distinct expression patterns, depending on the physiological status, toxicity and with generally higher expression under the high cell density conditions. Overall, our study contributes to a better understanding of the dynamics between the two critical processes of toxin production and mixotrophy, and has important implications for bloom formation and its maintenance in this ecologically important species.

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Polyketide synthase genes and molecular trade-offs in the ichthyotoxic species Prymnesium parvum

Cited by 15 publications

References 67 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

Natural Polyether Ionophores and Their Pharmacological Profile

The relationship between toxicity and mixotrophy in bloom dynamics of the ichthyotoxic Prymnesium parvum

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