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

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.

Microbial dynamics during harmful dinoflagellate Ostreopsis cf. ovata growth: Bacterial succession and viral abundance pattern

“…cf. ovata toxins (Pinna et al., ), are also known to be increasingly released from the exponential to the stationary phase (Pezzolesi et al., , ; Vanucci, Pezzolesi, et al., ; Vanucci, Guerrini, et al., ). Successively, Rhodobacteraceae genera such as Labrenzia and Dinoroseobacter may have also responded to a renewed availability of low molecular weight compounds by Bacteroidetes algal‐derived matter remineralization (Buchan et al., ; Fernández‐Gómez et al., ; Teeling et al., ) at the algal stationary phase.…”

“…ovata bloom Vanucci, Guidi, et al, 2016). According to secondary colonizer traits typical of Flammeovirgaceae (Kim et al, 2013;Nedashkovskaya & Ludwig, 2011), the high contribution of Fabibacter (Pinna et al, 2015), are also known to be increasingly released from the exponential to the stationary phase (Pezzolesi et al, 2014. Successively, Rhodobacteraceae genera such as Labrenzia and Dinoroseobacter may have also responded to a renewed availability of low molecular weight compounds by Bacteroidetes algal-derived matter remineralization (Buchan et al, 2014;Fernández-Gómez et al, 2013;Teeling et al, 2012) at the algal stationary phase.…”

Decadal reanalysis of biogeochemical indicators and fluxes in the North West European shelf‐sea ecosystem

“…Numerous works demonstrate the skill of ERSEM in representing marine ecosystem processes and reproducing ocean observations. Model validations have used univariate and multivariate analysis [e.g., Allen and Somerfield, 2009;Saux-Picart et al, 2012;de Mora et al, 2013de Mora et al, , 2016 in model applications ranging from zerodimensional process studies [e.g., Pinna et al, 2015] to global simulations [Kwiatkowski et al, 2014;de Mora et al, 2016]. In particular, the state-of-art version applied in this work was flexible and skilled in simulating multiannual time series of nutrients, chlorophyll, oxygen, particulate organic and dissolved inorganic carbon, as well as reproducing emerging properties (phytoplankton stoichiometry and average community structure) observed in three contrasting sites in coastal, shelf, and open ocean [Butensch€ on et al, 2015;de Mora et al, 2016].…”

Effects of N and P availability on carbon allocation in the toxic dinoflagellate Ostreopsis cf. ovata

“…Nutrient depletion has been reported to affect toxicity with contrasting results, either decreasing the toxin content in an Adriatic strain (Vanucci et al, 2012b) and/or increasing the haemolytic activity of a Tyrrhenian strain, particularly in N deficient cultures (Vidyarathna and Grane ´li, 2013). The role of bacteria in remineralizing the organic matter, likely releasing N and P, resulted important in the growth population dynamics and in the toxin degradation (Vanucci et al, 2012a;Pinna et al, 2015). On one hand, environmental factors have been observed to substantially alter O. cf.…”