Abstract
Absorption and accumulation of bioavailable cyanobacterial metabolites (including cyanotoxins) are likely in fish after senescence and the rupturing of cells during bloom episodes. We determined the toxicity of cyanopeptides identified from two strains of Microcystis (M. panniformis MIRS-04 and M. aeruginosa NPDC-01) in a freshwater tropical fish, Astyanax altiparanae (yellowtail tetra, lambari). Aqueous extracts of both Microcystis strains were prepared in order to simulate realistic fish exposure to these substances in a freshwater environment. Both strains were selected because previous assays evidenced the presence of microcystins (MCs) in MIRS-04 and lack of cyanotoxins in NPDC-01. Identification of cyanobacterial secondary metabolites was performed by LC-HR-QTOF-MS and quantification of the MC-LR was carried out by LC-QqQ-MS/MS. MIRS-04 produces the MCs MC-LR, MC-LY and MC-HilR as well as micropeptins B, 973, 959 and k139. NPCD-01 biosynthetizes microginins FR1, FR2/FR4 and SD-755, but does not produce MCs. Larval fish survival and changes in morphology were assessed for 96 h exposure to aqueous extracts of both strains at environmentally relevant concentrations from 0.1 to 0.5 mg (dry weight)/mL, corresponding to 0.15 to 0.74 μg/mL of MC-LR (considering dried amounts of MIRS-04 for comparison). Fish mortality increased with concentration and time of exposure for both strains of Microcystis. The frequencies of morphological abnormalities increased with concentration in both strains, and included abdominal and pericardial oedema, and spinal curvature. Results demonstrate that toxicity was not solely caused by MCs, other classes of cyanobacterial secondary metabolites contributed to the observed toxicity.
Highlights
The occurrence of cyanobacterial blooms and the presence of some water soluble-cyanotoxins are well documented in several inland water bodies worldwide [1]
The aims of this study were the following: (i) characterize by LC-HR-QTOF-MS the most common secondary metabolites produced by these two species of cyanobacteria; (ii) quantify microcystin variants by LC-QqQ-MS/MS; and, (iii) determine whether the larvae of the freshwater tropical fish Astyanax altiparanae are affected by water-soluble compounds produced by two strains of Microcystis
Dynamics of cyanopeptides in the aquatic food web are available in the literature; only a few ecotoxicological studies with peptides other than toxins have been published so far [45]. The toxicity of these compounds seems to be low and in inhibition activity assays, some linear and cyclic peptides show extremely low IC50 for several key enzymes in the metabolism [27,46,47]. Considering these aspects, we evaluated the possible synergy and potential toxicity of different polar metabolites produced by two species of cyanobacteria that were previously classified as microcystin-producer and non-producer on the larva development of A. altiparanae, one of the most common fish species in tropical Brazilian water bodies [48,49] Astyanax altiparanae is a non-migratory omnivorous fish native from Brazil and the Astyanax genus has an abundance of species distributed throughout the Neotropical region [49,50]
Summary
The occurrence of cyanobacterial blooms and the presence of some water soluble-cyanotoxins are well documented in several inland water bodies worldwide [1]. Cyanotoxins such as cyclic peptide microcystins and nodularins, lipopolysaccharides and some alkaloids (i.e., anatoxins, saxitoxins, cylindrospermopsins and lyngbyatoxins) are well known and produced by common freshwater cyanobacterial species (i.e., Microcystis, Cylindrospermosis and Anabaena genera) [2]. Cyanobacteria produce a wide range of biologically active secondary metabolites for which only some classes have been fully characterized and assessed for toxicity [4]. There are relatively few in vivo studies on the effects of secondary metabolites of cyanobacteria, but those that have been conducted indicate these substances can be important, including for the detection of allelopathy in some cyanometabolites with other competitive species in the environment, antifeeding and antibiotic effects [8,9], and developmental toxicity in fish exposed during early life history stages [10,11]
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