Rapid uptake and slow depuration: Health risks following cyanotoxin accumulation in mussels?

Abstract

Freshwater cyanobacteria produce highly toxic secondary metabolites, which can be transported downstream by rivers and waterways into the sea. Estuarine and coastal aquaculture sites exposed to toxic cyanobacteria raise concerns that shellfish may accumulate and transfer cyanotoxins in the food web. This study aims to describe the competitive pattern of uptake and depuration of a wide range of microcystins (MC-LR, MC-LF, MC-LW, MC-LY, [Asp3]-MC-LR/[Dha7]-MC-LR, MC-HilR) and nodularins (NOD cyclic and linear) within the common blue mussel Mytilus edulis exposed to a combined culture of Microcystis aeruginosa and Nodularia spumigena into the coastal environment. Different distribution profiles of MCs/NODs in the experimental system were observed. The majority of MCs/NODs were present intracellularly which is representative of healthy cyanobacterial cultures, with MC-LR and NOD the most abundant analogues. Higher removal rate was observed for NOD (≈96%) compared to MCs (≈50%) from the water phase. Accumulation of toxins in M. edulis was fast, reaching up to 3.4 μg/g shellfish tissue four days after the end of the 3-days exposure period, with NOD (1.72 μg/g) and MC-LR (0.74 μg/g) as the dominant toxins, followed by MC-LF (0.35 μg/g) and MC-LW (0.31 μg/g). Following the end of the exposure period depuration was incomplete after 27 days (0.49 μg/g of MCs/NODs). MCs/NODs were also present in faecal material and extrapallial fluid after 24 h of exposure with MCs the main contributors to the total cyanotoxin load in faecal material and NOD in the extrapallial fluid. Maximum concentration of MCs/NODs accumulated in a typical portion of mussels (20 mussels, ≈4 g each) was beyond greater the acute, seasonal and lifetime tolerable daily intake. Even after 27 days of depuration, consuming mussels harvested during even short term harmful algae blooms in close proximity to shellfish beds might carry a high health risk, highlighting the need for testing.

In situ use of bivalves and passive samplers to reveal water contamination by microcystins along a freshwater-marine continuum in France

“…The %var of MC-YR was similar between phytoplankton and mussel tissues, and decreased in mussel tissues along the salinity gradient from 13% at E1 to 0% at M. The MC-LR variant showed a similar and stable %var between mussel and phytoplankton samples at the three estuarine sites, suggesting that M. edulis accumulated MC-LR and MC-YR in proportions similar to what they ingest. This observation is in contradiction to the lower MC-LR ratio observed in mussel tissues compared to cyanobacteria at freshwater sites of this study and in the laboratory exposure of M. edulis to M. aeruginosa (Camacho et al, 2021). While the MC-RR variant occurred more frequently in tissues of A. anatina than in phytoplankton at freshwater sites, the contrary was observed at estuarine sites where the %var of MC-RR decreased in mussels along the salinity gradients (from 42% at E1 to 6% at M) despite a concomitant increase in phytoplankton (from 28% at E1 to 66% at M).…”

“…Passive integrators like SPATT have been developed, but their use is limited because the samplers only adsorb extracellular cyanotoxins and they are subject to rapid clogging and saturation, which shortens their useful life (Kudela, 2011). Bivalves, filter-feeders with high filtration rates, have been proposed as tools for detecting the presence of MC-producing cyanobacteria in water (Preece et al, 2015; gland, mainly after ingestion of MC-producing cyanobacteria and to a lesser extent through the filtration of dissolved toxins (Ferrão-Filho and Kozlowsky-Suzuki, 2011;Gkelis et al, 2006;Camacho et al, 2021).…”

A Feasibility Study into the Production of a Mussel Matrix Reference Material for the Cyanobacterial Toxins Microcystins and Nodularins

“…Cyanotoxin-contaminated mussel tissues were produced as detailed previously [ 26 ] and as described in the methods section. A culture of Mycrocystis aeruginosa utilized for shellfish feeding contained the microcystin (MC) variants (MC-LR, LW, LF, HilR, LY and desmethyl MC-LR (dmMC-LR, constituting [D-Asp 3 ]MC-LR and/or [Dha 7 ]MC-LR).…”

“…Nodularin-R (NOD-R), along with a low number of structural analogues, is produced by Nodularia spumigena which thrives in brackish water [ 16 ], thereby resulting in impacts in both freshwater and saline environments [ 17 , 18 , 19 ]. Human health impacts from cyanotoxins have occurred through drinking from contaminated water supplies, recreational exposure, aerosol exposure under certain meteorological conditions and through eating contaminated aquatic foodstuffs, health food supplements, or even terrestrial foods irrigated with contaminated water [ 17 , 18 , 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 ]. In recent years, the risk from cyanotoxin poisoning following human consumption of seafood contaminated with cyanotoxins has been highlighted, with shellfish being one of the primary routes of toxins through to higher trophic levels [ 6 , 13 , 14 , 27 , 28 , 29 ] and in some instances with toxin concentrations reaching dangerously high levels (reviewed by [ 6 ]).…”

“…The need for such a RM prompted the culturing of toxic Microcystis and Nodularia with subsequent feeding studies in mussels in a controlled laboratory environment to assess the uptake and depuration of toxins within mussel tissues [ 26 ], with the resulting tissue materials utilized for RM preparation and characterization. The aim was to produce a shellfish tissue cyanotoxin RM which was fully characterised and provided proof of concept for future development of a fully certified shellfish RM containing a wide range of toxins from cyanobacterial origin.…”