A Mediterranean Alexandrium taylorii (Dinophyceae) Strain Produces Goniodomin A and Lytic Compounds but Not Paralytic Shellfish Toxins

Abstract

Species of the dinophyte genus Alexandrium are widely distributed and are notorious bloom formers and producers of various potent phycotoxins. The species Alexandrium taylorii is known to form recurrent and dense blooms in the Mediterranean, but its toxin production potential is poorly studied. Here we investigated toxin production potential of a Mediterranean A. taylorii clonal strain by combining state-of-the-art screening for various toxins known to be produced within Alexandrium with a sound morphological and molecular designation of the studied strain. As shown by a detailed thecal plate analysis, morphology of the A. taylorii strain AY7T from the Adriatic Sea conformed with the original species description. Moreover, newly obtained Large Subunit (LSU) and Internal Transcribed Spacers (ITS) rDNA sequences perfectly matched with the majority of other Mediterranean A. taylorii strains from the databases. Based on both ion pair chromatography coupled to post-column derivatization and fluorescence detection (LC-FLD) and liquid chromatography coupled to tandem mass spectrometry (LC-MS/MS) analysis it is shown that A. taylorii AY7T does not produce paralytic shellfish toxins (PST) above a detection limit of ca. 1 fg cell−1, and also lacks any traces of spirolides and gymnodimines. The strain caused cell lysis of protistan species due to poorly characterized lytic compounds, with a density of 185 cells mL−1 causing 50% cell lysis of cryptophyte bioassay target cells (EC50). As shown here for the first time A. taylorii AY7T produced goniodomin A (GDA) at a cellular level of 11.7 pg cell−1. This first report of goniodomin (GD) production of A. taylorii supports the close evolutionary relationship of A. taylorii to other identified GD-producing Alexandrium species. As GD have been causatively linked to fish kills, future studies of Mediterranean A. taylorii blooms should include analysis of GD and should draw attention to potential links to fish kills or other environmental damage.

Unknown Extracellular and Bioactive Metabolites of the Genus Alexandrium: A Review of Overlooked Toxins

“…Confirmed negative for PSP by [141,153,154], negative also in [127,128] (but no details on LOD). (z) Mediterranean strains of A. taylorii do not produce PSP [3,4] nor spiroimines, but do produce Goniodomin A [3]. A Pacific strain designated as A. taylorii without accompanying sequence data has been claimed as a PSP producer [155], but this report is questionable and needs re-investigation: the cell quotas were very low and the "toxin profile" had a 100% match with the PSP profile of a A. ostenfeldii strain which was simultaneously studied, and thus strain cross-contamination and not PSP production of A. taylorii is the likely cause of this report.…”

“…Recent compelling evidence shows that goniodomin and GDA in fact are the same compound [111]. Later reports added that GDA is also produced by A. monilatum (J.F.Howell) Balech [112], A. pseudogonyaulax (Biecheler) Horiguchi ex K.Yuki and Y.Fukuyo [113], and A. taylorii Balech [3]. In 2008 an isomer of GDA was structurally elucidated and named GDB [114].…”

“…However, few studies highlighted deleterious effects of non-PST but lytic strains. For example, lytic compounds of "A. taylorii" (A. taylorii is regarded as a non-PST-producing species [3], but note that in the study of Emura and collaborators [180] no strain identifier, no morphology and no sequence data were provided, which would allow confirmation of the Alexandrium species determination) were shown to be toxic against Artemia salina [180]. The crustaceans were immobilised and died when exposed to the supernatant or the whole culture.…”

“…This is largely related to the ability of several Alexandrium species to produce paralytic shellfish toxins (PSTs; saxitoxin and analogues) responsible for life-threatening human poisoning (paralytic shellfish poisoning, PSP) trough consumption of contaminated seafood [1]. Other species of Alexandrium may produce other phycotoxins such as the spirolides and/or gymnodimines produced by A. ostenfeldii (Paulsen) Balech and Tangen (reported as A. peruvianum by [2]), or goniodomins Toxins 2021, 13, 905 2 of 39 produced by a few other Alexandrium species [3]. Moreover, many species are described to produce poorly characterised extracellular compounds with lytic capacity [4].…”

Alexandrium spp.: From Toxicity to Potential Biotechnological Benefits

“…Antiproliferative activity on melanoma (A2058) and normal human lung fibroblast (MRC-5) [26,32] A. taylori Balech Goniodomin A, Hemolytic substances Effects on oyster larvae, sea-monkey mortality [65,66] PSP = paralytic shellfish poisoning; PSTs = paralytic shellfish toxins. * only some strains were found to be toxic.…”