Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria Microcystis aeruginosa and Chrysosporum ovalisporum

Abstract

Toxic cyanobacterial blooms are a major contaminant in inland aquatic ecosystems. Furthermore, toxic blooms are carried downstream by rivers and waterways to estuarine and coastal ecosystems. Concerning marine and estuarine animal species, very little is known about how these species are affected by the exposure to freshwater cyanobacteria and cyanotoxins. So far, most of the knowledge has been gathered from freshwater bivalve molluscs. This work aimed to infer the sensitivity of the marine mussel Mytilus galloprovincialis to single as well as mixed toxic cyanobacterial cultures and the underlying molecular responses mediated by toxic cyanobacteria. For this purpose, a mussel exposure experiment was outlined with two toxic cyanobacteria species, Microcystis aeruginosa and Chrysosporum ovalisporum at 1 × 105 cells/mL, resembling a natural cyanobacteria bloom. The estimated amount of toxins produced by M. aeruginosa and C. ovalisporum were respectively 0.023 pg/cell of microcystin-LR (MC-LR) and 7.854 pg/cell of cylindrospermopsin (CYN). After 15 days of exposure to single and mixed cyanobacteria, a depuration phase followed, during which mussels were fed only non-toxic microalga Parachlorella kessleri. The results showed that the marine mussel is able to filter toxic cyanobacteria at a rate equal or higher than the non-toxic microalga P. kessleri. Filtration rates observed after 15 days of feeding toxic microalgae were 1773.04 mL/ind.h (for M. aeruginosa), 2151.83 mL/ind.h (for C. ovalisporum), 1673.29 mL/ind.h (for the mixture of the 2 cyanobacteria) and 2539.25 mL/ind.h (for the non-toxic P. kessleri). Filtering toxic microalgae in combination resulted in the accumulation of 14.17 ng/g dw MC-LR and 92.08 ng/g dw CYN. Other physiological and biochemical endpoints (dry weight, byssus production, total protein and glycogen) measured in this work did not change significantly in the groups exposed to toxic cyanobacteria with regard to control group, suggesting that mussels were not affected with the toxic microalgae. Nevertheless, proteomics revealed changes in metabolism of mussels related to diet, specially evident in those fed on combined cyanobacteria. Changes in metabolic pathways related with protein folding and stabilization, cytoskeleton structure, and gene transcription/translation were observed after exposure and feeding toxic cyanobacteria. These changes occur in vital metabolic processes and may contribute to protect mussels from toxic effects of the toxins MC-LR and CYN.

The current situation and potential effects of climate change on the microbial load of marine bivalves of the Greek coastlines: an integrative review

“…Given that the depuration of STX within bivalves can be slowed by warming and acidification, this toxin may be retained for longer periods of time, increasing the risk to bivalve health (Braga et al ., 2018). Several studies revealed changes in metabolic pathways related to protein folding and stabilization, cytoskeleton structure, gene transcription/translation, feeding, behaviour, and energy balance in mussels after exposure and feeding toxic cyanobacteria (Juhel et al ., 2006; Oliveira et al ., 2020).…”

Review on Cyanobacterial Studies in Portugal: Current Impacts and Research Needs

“…Overall, results support the relative importance of the GST system as a protective mechanism to cope with MC-producing cyanobacterial blooms exposure which seems to be different between the bivalve species [56]. Despite the ability of cyanotoxins uptake and elimination, physiological alterations along with biochemical and genotoxic effects have been shown to be induced in bivalves by toxic cyanobacteria [39,57]. Studies with fish are in much lesser number when compared with bivalves.…”

“…A large-scale proteomic profiling, combining liquid chromatography and high-throughput MS analysis, was used to depict other molecular processes related to the response of bivalves to cyanotoxins like MCs and CYN. Sub-toxic effects of cyanotoxins were related for instance to changes in protein folding and stabilization, cytoskeleton structure, and gene transcription/translation [39].…”

Environmentally Friendly and Cost-Effective Approaches to Reduce Toxin Content in Toxic Cyanobacterial Biomasses

“…For this study, two toxin-producing cyanobacterial strains from the Blue Biotechnology and Ecotoxicology Culture Collection (LEGE-CC) [28] were used. The cyanobacteria M. aeruginosa (LEGE 91094) and C. ovalisporum (LEGE X-001) were grown in sterilized Z8 medium at 26 ± 1 • C, with a photoperiod of 14 h/10 h (light/dark) and a light intensity of 20 µmol m −2 s −1 [29]. After growing for 45 days in 20 L vessels, the cyanobacteria were collected by centrifugation, frozen at −80 • C, and lyophilized for posterior use.…”