New Knowledge on Distribution and Abundance of Toxic Microalgal Species and Related Toxins in the Northwestern Black Sea

Abstract

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 (Dinophysis acuminata, Dinophysis acuta, Gonyaulax spinifera, and Karlodinium veneficum) 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 Dinophysis acuta and pectenotoxins, and between Lingulodinium polyedra and Protoceratium reticulatum 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.

Keywords: Black Sea; light microscopy; metabarcoding; phycotoxins; toxic microalgae.

Figure 1

Boxplots of environmental variables (average value for the sampling layer): T, temperature (°C); S, salinity (PSU); DO, dissolved oxygen (mg L⁻¹); Fl, fluorescence (mg m⁻³); SD, water transparency—Secchi depth (m).

Figure 2

Geographic distribution and abundance (ng NT⁻¹) of toxin variants in the 20–50 µm size fraction (toxin variant abbreviations are listed in Table S6).

Figure 3

Geographic distribution and abundance (ng NT⁻¹) of toxin variants in the 50–200 µm size fraction (toxin variant abbreviations are listed in Table S7).

Figure 4

Correlation analysis between the toxic dinoflagellate species and the relevant toxin variants by fractions: (a,c) 20−50 µm fraction; (b,d) 50−200 µm fraction. Circle size and color intensity are proportional to the Spearman’s rho correlation coefficients. Empty spaces denote non-significant correlation (two-tailed p-value > 0.05). Dinophysis acuminata (D.acum.), Dinophysis acuta (D.acut.), Phalacroma rotundatum (Ph.rot.), Gonyaulax spinifera (G.spin.), Lingulodinium polyedra (L.poly.), Protoceratium reticulatum (P.reti.). *a,b Dinophysis caudata and D. sacculus were excluded from the analysis because they were detected at a limited number of stations. Toxin variant abbreviations are listed in Tables S6 and S7.

Figure 4

Correlation analysis between the toxic dinoflagellate species and the relevant toxin variants by fractions: (a,c) 20−50 µm fraction; (b,d) 50−200 µm fraction. Circle size and color intensity are proportional to the Spearman’s rho correlation coefficients. Empty spaces denote non-significant correlation (two-tailed p-value > 0.05). Dinophysis acuminata (D.acum.), Dinophysis acuta (D.acut.), Phalacroma rotundatum (Ph.rot.), Gonyaulax spinifera (G.spin.), Lingulodinium polyedra (L.poly.), Protoceratium reticulatum (P.reti.). *a,b Dinophysis caudata and D. sacculus were excluded from the analysis because they were detected at a limited number of stations. Toxin variant abbreviations are listed in Tables S6 and S7.

Figure 5

RDA correlation triplot (scaling type 1—lc scores—angles between vectors of response variables and explanatory variables reflect linear correlation) between the environmental variables and cell abundance data with fitted site scores. (T—temperature, S—salinity, Fl—fluorescence, DO—dissolved oxygen, SD—water transparency; D.acum.—Dinophysis acuminata, D.acut.—Dinophysis acuta, Ph.rot.—Phalacroma rotundatum, G.spin.—Gonyaulax spinifera, L.poly.—Lingulodinium polyedra, P.reti.—Protoceratium reticulatum). The green numbers represent stations.

Figure 6

CCA biplot—(scaling type 1—lc scores)—toxin variant concentration scores constrained to environmental gradients (in situ environmental explanatory dataset, and toxin concentration response matrix). T, temperature; S, salinity; Fl, fluorescence; DO, dissolved oxygen; SD, water transparency. Toxin variant abbreviations are listed in Tables S6 and S7).

Figure 7

Study area and sampling stations.