Early Genotoxic and Cytotoxic Effects of the Toxic Dinoflagellate Prorocentrum lima in the Mussel Mytilus galloprovincialis

Abstract

Okadaic acid (OA) and dinophysistoxins (DTXs) are the main toxins responsible for diarrhetic shellfish poisoning (DSP) intoxications during harmful algal blooms (HABs). Although the genotoxic and cytotoxic responses to OA have been evaluated in vitro, the in vivo effects of these toxins have not yet been fully explored. The present work fills this gap by evaluating the in vivo effects of the exposure to the DSP-toxin-producing dinoflagellate Prorocentrum lima during the simulation of an early HAB episode in the mussel Mytilus galloprovincialis. The obtained results revealed that in vivo exposure to this toxic microalgae induced early genotoxicity in hemocytes, as a consequence of oxidative DNA damage. In addition, the DNA damage observed in gill cells seems to be mainly influenced by exposure time and P. lima concentration, similarly to the case of the oxidative damage found in hemocytes exposed in vitro to OA. In both cell types, the absence of DNA damage at low toxin concentrations is consistent with the notion suggesting that this level of toxicity does not disturb the antioxidant balance. Lastly, in vivo exposure to growing P. lima cell densities increased apoptosis but not necrosis, probably due to the presence of a high number of protein apoptosis inhibitors in molluscs. Overall, this work sheds light into the in vivo genotoxic and cytotoxic effects of P. lima. In doing so, it also demonstrates for the first time the potential of the modified (OGG1) comet assay for assessing oxidative DNA damage caused by marine toxins in marine invertebrates.

Accumulation and Tissue Distribution of Dinophysitoxin-1 and Dinophysitoxin-3 in the Mussel Crenomytilus grayanus Feeding on the Benthic Dinoflagellate Prorocentrum foraminosum

“…The observed levels of DNA strand breaks were considered as low. Similar levels of DNA strand breaks have been observed in similar research in the control group, meaning that this level of DNA strand breaks is considered normal [ 14 ]. The obtained results revealed the absence of significant levels of DNA damage in C. grayanus gills and digestive gland cells after 12 days of feeding on P. foraminosum , despite the fact that the active forms of DTX-1 were present at a high concentration.…”

“…The role of transforming the active toxin to DTX-3 is supposed to protect bivalves from DSTs activity [ 13 ]. However, these protective mechanisms may not always be effective, as it has recently been shown that a high density of Prorocentrum lima may cause oxidative DNA damage in haemocytes of the mussel Mytilus galloprovincialis [ 14 ].…”

Transcriptomic and Epigenetic Responses to Environmental Stress in Marine Bivalves with a Focus on Harmful Algal Blooms

“…The choice of gill tissue as model system in the present work was motivated by previous reports indicating that gills are the part of the organism first contacted by biotoxins during HABs, experiencing substantial DNA damage , Prego-Faraldo et al 2016.…”

“…During HABs, large amounts of potentially harmful biotoxins are produced and recruited into the human food chain through their accumulation by edible marine organisms , Plakas et al 2008. These biotoxins, among other relevant effects, have the ability to cause DNA damage, both in marine organisms and human consumers of contaminated shellfish , Prego-Faraldo et al 2016.…”

“…Coastal areas bear the brunt of HABs, impacting marine communities and commercial resources, especially the aquaculture industry. Consequently, bivalve molluscs are generally used as sentinel organisms to study HAB pollution , Prego-Faraldo et al 2016.…”