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Modelling the Stoichiometric Regulation of C-Rich Toxins in Marine Dinoflagellates.

Pinna A, Pezzolesi L, Pistocchi R, Vanucci S, Ciavatta S, Polimene L - PLoS ONE (2015)

Bottom Line: The highest values of cellular toxin are in fact mainly associated with a high carbon to nutrient cellular ratio.The analysis of simulations and their comparison with experimental data provided a conceptual model linking toxin production and nutritional status in this species.The model was also qualitatively validated by using independent literature data, and the results indicate that our formulation can be also used to simulate toxin dynamics in other dinoflagellates.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological, Geological and Environmental Sciences (BiGeA)-University of Bologna, Via Sant'Alberto 163, 48123 Ravenna, Italy; Plymouth Marine Laboratory, Prospect Place, The Hoe, PL1 3DH Plymouth, United Kingdom.

ABSTRACT
Toxin production in marine microalgae was previously shown to be tightly coupled with cellular stoichiometry. The highest values of cellular toxin are in fact mainly associated with a high carbon to nutrient cellular ratio. In particular, the cellular accumulation of C-rich toxins (i.e., with C:N > 6.6) can be stimulated by both N and P deficiency. Dinoflagellates are the main producers of C-rich toxins and may represent a serious threat for human health and the marine ecosystem. As such, the development of a numerical model able to predict how toxin production is stimulated by nutrient supply/deficiency is of primary utility for both scientific and management purposes. In this work we have developed a mechanistic model describing the stoichiometric regulation of C-rich toxins in marine dinoflagellates. To this purpose, a new formulation describing toxin production and fate was embedded in the European Regional Seas Ecosystem Model (ERSEM), here simplified to describe a monospecific batch culture. Toxin production was assumed to be composed by two distinct additive terms; the first is a constant fraction of algal production and is assumed to take place at any physiological conditions. The second term is assumed to be dependent on algal biomass and to be stimulated by internal nutrient deficiency. By using these assumptions, the model reproduced the concentrations and temporal evolution of toxins observed in cultures of Ostreopsis cf. ovata, a benthic/epiphytic dinoflagellate producing C-rich toxins named ovatoxins. The analysis of simulations and their comparison with experimental data provided a conceptual model linking toxin production and nutritional status in this species. The model was also qualitatively validated by using independent literature data, and the results indicate that our formulation can be also used to simulate toxin dynamics in other dinoflagellates. Our model represents an important step towards the simulation and prediction of marine algal toxicity.

No MeSH data available.


Related in: MedlinePlus

Sensitivity analysis with respect to selected model processes (experiment S1-3, see the text for explanation).(A) simulated and observed intracellular toxin; (B) modelled and observed chlorophyll to carbon ratio (Chl:C). (C) external toxin concentrations simulated with and without bacteria (bac). Data (with standard deviation) are also displayed.
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pone.0139046.g005: Sensitivity analysis with respect to selected model processes (experiment S1-3, see the text for explanation).(A) simulated and observed intracellular toxin; (B) modelled and observed chlorophyll to carbon ratio (Chl:C). (C) external toxin concentrations simulated with and without bacteria (bac). Data (with standard deviation) are also displayed.

Mentions: The results of the sensitivity simulations S1, S2 and S3 (Fig 5) showed that all the investigated processes significantly improved the simulations, taking the model output closer to the observed values. As expected, the reduction in basal respiration (S1) affected only the simulation of the last few days of the experiment, when the nutrient stress was high. Conversely, the nutrient dependent reduction in chlorophyll synthesis (S2) and the nutrient-dependent enhancement of toxin production (S3) affected the simulation since the very beginning of the experiment. The effect of nutrients on chlorophyll synthesis, which was assumed to begin at a relatively high nutrient to carbon internal ratio (see Table 1 and Fig 6), was also particularly important for the realistic simulation of the chlorophyll to carbon ratio, as evident in Fig 5B. The simulation without bacteria component produced identical results with respect to the simulation with bacteria with the only exception of the external toxin (Fig 5C). Without bacteria, the model predicted an accumulation of external toxin (reaching 40 mg C m-3 at day 35) which was not observed in the experimental data.


Modelling the Stoichiometric Regulation of C-Rich Toxins in Marine Dinoflagellates.

Pinna A, Pezzolesi L, Pistocchi R, Vanucci S, Ciavatta S, Polimene L - PLoS ONE (2015)

Sensitivity analysis with respect to selected model processes (experiment S1-3, see the text for explanation).(A) simulated and observed intracellular toxin; (B) modelled and observed chlorophyll to carbon ratio (Chl:C). (C) external toxin concentrations simulated with and without bacteria (bac). Data (with standard deviation) are also displayed.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4580455&req=5

pone.0139046.g005: Sensitivity analysis with respect to selected model processes (experiment S1-3, see the text for explanation).(A) simulated and observed intracellular toxin; (B) modelled and observed chlorophyll to carbon ratio (Chl:C). (C) external toxin concentrations simulated with and without bacteria (bac). Data (with standard deviation) are also displayed.
Mentions: The results of the sensitivity simulations S1, S2 and S3 (Fig 5) showed that all the investigated processes significantly improved the simulations, taking the model output closer to the observed values. As expected, the reduction in basal respiration (S1) affected only the simulation of the last few days of the experiment, when the nutrient stress was high. Conversely, the nutrient dependent reduction in chlorophyll synthesis (S2) and the nutrient-dependent enhancement of toxin production (S3) affected the simulation since the very beginning of the experiment. The effect of nutrients on chlorophyll synthesis, which was assumed to begin at a relatively high nutrient to carbon internal ratio (see Table 1 and Fig 6), was also particularly important for the realistic simulation of the chlorophyll to carbon ratio, as evident in Fig 5B. The simulation without bacteria component produced identical results with respect to the simulation with bacteria with the only exception of the external toxin (Fig 5C). Without bacteria, the model predicted an accumulation of external toxin (reaching 40 mg C m-3 at day 35) which was not observed in the experimental data.

Bottom Line: The highest values of cellular toxin are in fact mainly associated with a high carbon to nutrient cellular ratio.The analysis of simulations and their comparison with experimental data provided a conceptual model linking toxin production and nutritional status in this species.The model was also qualitatively validated by using independent literature data, and the results indicate that our formulation can be also used to simulate toxin dynamics in other dinoflagellates.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological, Geological and Environmental Sciences (BiGeA)-University of Bologna, Via Sant'Alberto 163, 48123 Ravenna, Italy; Plymouth Marine Laboratory, Prospect Place, The Hoe, PL1 3DH Plymouth, United Kingdom.

ABSTRACT
Toxin production in marine microalgae was previously shown to be tightly coupled with cellular stoichiometry. The highest values of cellular toxin are in fact mainly associated with a high carbon to nutrient cellular ratio. In particular, the cellular accumulation of C-rich toxins (i.e., with C:N > 6.6) can be stimulated by both N and P deficiency. Dinoflagellates are the main producers of C-rich toxins and may represent a serious threat for human health and the marine ecosystem. As such, the development of a numerical model able to predict how toxin production is stimulated by nutrient supply/deficiency is of primary utility for both scientific and management purposes. In this work we have developed a mechanistic model describing the stoichiometric regulation of C-rich toxins in marine dinoflagellates. To this purpose, a new formulation describing toxin production and fate was embedded in the European Regional Seas Ecosystem Model (ERSEM), here simplified to describe a monospecific batch culture. Toxin production was assumed to be composed by two distinct additive terms; the first is a constant fraction of algal production and is assumed to take place at any physiological conditions. The second term is assumed to be dependent on algal biomass and to be stimulated by internal nutrient deficiency. By using these assumptions, the model reproduced the concentrations and temporal evolution of toxins observed in cultures of Ostreopsis cf. ovata, a benthic/epiphytic dinoflagellate producing C-rich toxins named ovatoxins. The analysis of simulations and their comparison with experimental data provided a conceptual model linking toxin production and nutritional status in this species. The model was also qualitatively validated by using independent literature data, and the results indicate that our formulation can be also used to simulate toxin dynamics in other dinoflagellates. Our model represents an important step towards the simulation and prediction of marine algal toxicity.

No MeSH data available.


Related in: MedlinePlus