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. 2022 Nov 28;20(12):748.
doi: 10.3390/md20120748.

Rapid Biotic and Abiotic Transformation of Toxins produced by Ostreopsis. cf. ovata

Eva Ternon  1   2 , Olivier P Thomas  3 , Rodolphe Lemée  2 , William H Gerwick  1   4
Affiliations

Rapid Biotic and Abiotic Transformation of Toxins produced by Ostreopsis. cf. ovata

Eva Ternon et al. Mar Drugs. .

Abstract

The dinoflagellate Ostreopsis cf. ovata produces several families of toxic polyketides. Despite only a few field measurements of these phycotoxins in seawater and aerosols, they are believed to be responsible for dermatitis and the toxic inhalations reported during blooms of this species. Therefore, the stability of these compounds in seawater is essential to understanding the causes of these symptoms, however, this has never been assessed. In the current study, the optimization of a solid phase extraction (SPE) procedure was first performed to ensure the most efficient extraction of all phycotoxins known to be produced by this strain, including the recently described liguriatoxins. The SPE cartridge SDBL® under non acidified conditions offered the best option. The stability of the ovatoxins and the liguriatoxins under biotic and abiotic stress was assessed by exposing the spent medium of a culture of Ostreopsis cf. ovata to its bacterial consortium and natural sunlight. A rapid biotic transformation was detected for both families of compounds. When exposed to bacteria, the half-lives of the ovatoxins were reached before 10 h and at 36 h, 97% of these toxins had been transformed. The half-lives of the liguriatoxins were 10 h under these conditions. Photolysis (abiotic degradation) of the ovatoxins (T1/2 < 36 h) was faster than for the liguriatoxins (T1/2 > 62 h). Although none of the catabolites of these phycotoxins were thoroughly identified, an untargeted metabolomics approach combined with molecular networking highlighted the presence of several compounds exhibiting structural similarities with the ovatoxins. Additional work should confirm the preliminary findings on these potential ovatoxins’ catabolites and their biological properties. The rapid transformation of O. cf. ovata’s phycotoxins introduces questions concerning their presence in seawater and their dispersion in the sea spray aerosols. The compounds involved in the toxic inhalations and dermatitis often experienced by beachgoers may stem from the catabolites of these toxins or even unrelated and as yet unidentified compounds.

Keywords: Ostreopsis cf. ovata; catabolites; metabolomics; ova- and liguriatoxins.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Relative waterborne OVTX and LGTX compositions in 10-day old spent culture medium of O. cf. ovata assessed by Ultra-High Pressure Liquid Chromatography coupled to High Resolution Mass Spectrometry (UHPLC-HRMS).
Figure 2
Figure 2
Boxplots comparing the mean intensities of the ions (A) m/z 1315.2546 (OVTX-a), (B) m/z 1337.2705 (OVTX-b), (C) m/z 987.0342 (LGTX-a), (D) m/z 1043.0673 (LGTX-b) and (E) m/z 1072.0619 (LGTX-c), in acidified (FA) and non-acidified samples. Sorbents are C18 (octadecyl bonded silica), HLB (Polymeric Phase), PPL (Styrene Divinyl Benzene), SDBL (Styrene Divinyl Benzene), StrataX (Polymeric phase). Statistical significance was assessed with the following threshold: * 0.05 < p < 0.5; ** 0.005 < p < 0.05, *** p < 0.005. Black stars compare acidified versus non acidified conditions for one sorbent type, whereas red stars compare one sorbent type to the SDBL sorbent.
Figure 2
Figure 2
Boxplots comparing the mean intensities of the ions (A) m/z 1315.2546 (OVTX-a), (B) m/z 1337.2705 (OVTX-b), (C) m/z 987.0342 (LGTX-a), (D) m/z 1043.0673 (LGTX-b) and (E) m/z 1072.0619 (LGTX-c), in acidified (FA) and non-acidified samples. Sorbents are C18 (octadecyl bonded silica), HLB (Polymeric Phase), PPL (Styrene Divinyl Benzene), SDBL (Styrene Divinyl Benzene), StrataX (Polymeric phase). Statistical significance was assessed with the following threshold: * 0.05 < p < 0.5; ** 0.005 < p < 0.05, *** p < 0.005. Black stars compare acidified versus non acidified conditions for one sorbent type, whereas red stars compare one sorbent type to the SDBL sorbent.
Figure 3
Figure 3
Degradation percentages normalized to control samples (BLK) collected at the same sampling times (%) and their standard deviation for LGTX-a, LGTX-b, LGTX-c, OVTX-a and OVTX-b, under conditions of bacteria exposure (BACT) at 10, 36 and 62 h or natural sunlight (PHOT) at 36 and 62 h.
Figure 4
Figure 4
Molecular network representing the relationships between the ions detected in the three treatments: BLK (light blue), PHOT (yellow) and BACT (red). Grey pies represent either L1 media or analytical blanks. Rectangles mark the three clusters A, B and C mentioned in the text as well as two group of compounds, high molecular weight (>2000 Da, red) and RVTX-type ions (pink). The lost ions listed in Table 1 are marked with a colored border: dark blue for the PHOT treatment, orange for the BACT treatment and purple when the ions are lost in both PHOT and BACT treatments. The singletons corresponding to OVTX-a, OVTX-b and LGTX-c are also indicated.
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