José I. Carreto

Mycosporine-Like Amino Acids: Relevant Secondary Metabolites. Chemical and Ecological Aspects

Taxonomically diverse marine, freshwater and terrestrial organisms have evolved the capacity to synthesize, accumulate and metabolize a variety of UV-absorbing substances called mycosporine-like amino acids (MAAs) as part of an overall strategy to diminish the direct and indirect damaging effects of environmental ultraviolet radiation (UVR). Whereas the enzymatic machinery to synthesize MAAs was probably inherited from cyanobacteria ancestors via the endosymbionts hypothesis, metazoans lack this biochemical pathway, but can acquire and metabolize these compounds by trophic transference, symbiotic or bacterial association. In this review we describe the structure and physicochemical properties of MAAs, including the recently discovered compounds and the modern methods used for their isolation and identification, updating previous reviews. On this basis, we review the metabolism and distribution of this unique class of metabolites among marine organism.

Palythine-threonine, a major novel mycosporine-like amino acid (MAA) isolated from the hermatypic coral Pocillopora capitata.

Using a high-resolution reverse-phase liquid chromatography method we found that the tissues of the hermatypic coral Pocillopora capitata (collected in Santiago Bay, Mexico) contain a high diversity of primary and secondary mycosporine-like amino acids (MAAs) typical of some reef-building coral species: mycosporine-glycine, shinorine, porphyra-334, mycosporine-methylamine-serine, mycosporine-methylamine-threonine, palythine-serine, palythine and one additional novel predominant MAA, with an absorbance maximum of 320 nm. Here we document the isolation and characterization of this novel MAA from the coral P. capitata. Using low multi-stage mass analyses of deuterated and non deuterated compounds, high-resolution mass analyses (Time of Flight, TOF) and other techniques, this novel compound was characterized as palythine-threonine. Palythine-threonine was also present in high concentrations in the corals Pocillopora eydouxi and Stylophora pistillata indicating a wider distribution of this MAA among reef-building corals. From structural considerations we suggest that palythine-threonine is formed by decarboxylation of porphyra-334 followed by demethylation of mycosporine-methylamine-threonine.

In Vitro cis–trans Photoisomerization of Palythene and Usujirene. Implications on the In Vivo Transformation of Mycosporine-like Amino Acids¶

The in vitro photoinduced reactions of the mycosporine‐like amino acids (MAA) usujirene and palythene were studied by monochromatic stationary irradiation at 366 nm. High‐performance liquid chromatography analysis of the irradiated aqueous solution of usujirene indicated a low photoreactivity on the basis of the observed photodecomposition quantum yield of ϕ−U= (2.86 ± 0.80) × 10−5, which can be partially accounted for by the cis–trans photoisomerization of usujirene to palythene (ϕU→P=[1.71 ± 0.13]× 10−5). However, palythene in aqueous solution showed a higher photostability than did usujirene under equivalent conditions, establishing a photostationary mixture of cis–trans isomers with a relative composition of palythene–usujirene (11:1). These results may explain the preferential in vivo accumulation of palythene relative to that of usujirene observed in several dinoflagellate species.

Mycosporine-like amino acid content in the sea anemones Aulactinia marplatensis, Oulactis muscosa and Anthothoe chilensis

The occurrence of mycosporine-like amino acids (MAAs) in the sea anemones Aulactinia marplatensis (Zamponi, 1977), Oulactis muscosa (Drayton in Dana, 1846) and Anthothoe chilensis (Lesson, 1830), from the rocky intertidal habitats on the coast of Mar del Plata, Argentina, was assessed by HPLC. The pattern of MAAs in the mussel Brachidontes rodriguezi, main component of the diet for A. marplatensis and O. muscosa, was as well determined. The results were comparatively analyzed together and with previously reported MAA content in species mainly of the genus Anthopleura. The correlation between the MAA concentration and light availability of their habitats is in line with the photoprotective role assigned to the compounds. The high proportion of mycosporine-taurine in the three species and the results for the evaluation of MAAs in the mussels point to a non-dietary origin or a regulated biotransformation metabolism of dietary MAAs and/or their precursors that is common to sea anemones.

Characterization of mycosporine-serine-glycine methyl ester, a major mycosporine-like amino acid from dinoflagellates: a mass spectrometry study.

Several unknown mycosporine‐like amino acids (MAAs) have been previously isolated from some cultured species of toxic dinoflagellates of the Alexandrium genus (Dinophyceae). One of them, originally called M‐333, was tentatively identified as a shinorine methyl ester, but the precise nature of this compound is still unknown. Using a high‐resolution reversed‐phase liquid chromatography mass spectrometry analyses (HPLC/MS), we found that natural populations of the red tide dinoflagellate Prorocentrum micans Ehrenberg showed a net dominance of M‐333 together with lesser amounts of other MAAs. We also documented the isolation and characterization of this MAA from natural dinoflagellate populations and from Alexandrium tamarense (Lebour) Balech cultures. Using a comparative fragmentation study in electrospray mass spectrometry between deuterated and non‐deuterated M‐333 compounds and synthesized mono and dimethyl esters of shinorine, this novel compound was characterized as mycosporine‐serine‐glycine methyl ester, a structure confirmed by nuclear magnetic resonance. These isobaric compounds can be differentiated by their fragmentation patterns in MS3 experiments because the extension and the specific site of the methylation changed the fragmentation pathway.

Photochemistry and Photophysics of Shinorine Dimethyl Ester

The photostability and photophysical properties of the dimethyl ester of the mycosporine‐like amino acid shinorine have been experimentally evaluated in aqueous solution and in the presence of direct micelles prepared with a cationic or an anionic detergent, respectively. In comparison with shinorine, the ester molecule increases the photostability, the fluorescence quantum yield and the fluorescence lifetime in water as well as in the micellar solutions. The effects are more pronounced in sodium dodecyl sulfate solutions and suggest that the electrostatic attractions with the micellar interface contribute to limit the movement of the molecules and influence the relative rate of their deactivation channels. However, the predominance of the nonradiative decay is maintained together with the UV photoprotective ability of this atypical mycosporine species.

Alexandrium tamarense/catenella Blooms in the Southwestern Atlantic: Paralytic Shellfish Toxin Production and Its Trophic Transference

Some species of the dinoflagellate genus Alexandrium (Halim) Balech produce potent neurotoxins called saxitoxins (STXs), which can be accumulated in several invertebrates whose ingestion can cause the human intoxication named paralytic shellfish poisoning (PSP). Many of these STXs are transferred through the food chain and thus can also affect a variety of wildlife. The species A. tamarense/catenella were mainly responsible for PSP in Southwestern Atlantic. However, unexpected patterns of diversity in genetic, reproductive compatibility, toxicity, and physiological response were found in several studies. The present review seeks to provide a broad overview of the species A. tamarense/catenella distribution, their toxicity and toxin composition in clonal isolates, and natural populations, using historical plankton, cyst, and toxin records. Also, the metabolic changes that occur in the toxic composition of primary and secondary consumers and the impact produced by their transference through the food chain are evaluated.

Removal of the toxic dinoflagellate Alexandrium tamarense (Dinophyta, Gonyaulacales) by Mnemiopsis leidyi (Ctenophora, Lobata) in controlled experimental conditions

The objective of the present study is to estimate the removal capability of the ctenophore Mnemiopsis leidyi (Ctenophora, Lobata) on cultures of the toxic dinoflagellate Alexandrium tamarense (Dinophyta, Gonyaulacales). For this purpose, observations on its clearance and survival rates were made in controlled experiments, using different A. tamarense cell concentrations. Mnemiopsis leidyi is able to remove dinoflagellates actively from the water column only at the lowest density tested (150 cells mL-1). Animals exposed to 300 cells mL-1 presented negative clearance and removal rates (survival= 67%). All ctenophores exposed at the highest concentrations of toxic dinoflagellates (600 cells mL-1) died after 4 h. Removal may occur mainly by incorporating and entangling cells in the mucus strands formed by the ctenophore, and in a lesser way by ingestion. Results indicate that higher concentrations of A. tamarense are fatally toxic to M. leidyi and that this ctenophore could control only the initial development of this dinoflagellate bloom.