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Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria Microcystis aeruginosa and Chrysosporum ovalisporum.
Toxins (Basel). 2020 03 20; 12(3)T

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.

Authors+Show Affiliations

CIIMAR- Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos, s/n, 4450-208 Porto, Portugal.Area of Toxicology, Faculty of Pharmacy, Universidad de Sevilla, Profesor García González n2, 41012 Seville, Spain.Department of Biomedical and Clinical Sciences, Faculty of Medicine and Clinical Sciences, Linköping University, 581 83 Linköping, Sweden.CIIMAR- Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos, s/n, 4450-208 Porto, Portugal.CIIMAR- Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos, s/n, 4450-208 Porto, Portugal.CIIMAR- Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos, s/n, 4450-208 Porto, Portugal.Area of Toxicology, Faculty of Pharmacy, Universidad de Sevilla, Profesor García González n2, 41012 Seville, Spain.Area of Toxicology, Faculty of Pharmacy, Universidad de Sevilla, Profesor García González n2, 41012 Seville, Spain.CIIMAR- Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos, s/n, 4450-208 Porto, Portugal. Biology Department, Faculty of Sciences, University of Porto, Rua do Campo Alegre, s/n, 4169-007 Porto, Portugal.CIIMAR- Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos, s/n, 4450-208 Porto, Portugal.CIIMAR- Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos, s/n, 4450-208 Porto, Portugal.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

32245045

Citation

Oliveira, Flavio, et al. "Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria Microcystis Aeruginosa and Chrysosporum Ovalisporum." Toxins, vol. 12, no. 3, 2020.
Oliveira F, Diez-Quijada L, Turkina MV, et al. Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria Microcystis aeruginosa and Chrysosporum ovalisporum. Toxins (Basel). 2020;12(3).
Oliveira, F., Diez-Quijada, L., Turkina, M. V., Morais, J., Felpeto, A. B., Azevedo, J., Jos, A., Camean, A. M., Vasconcelos, V., Martins, J. C., & Campos, A. (2020). Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria Microcystis aeruginosa and Chrysosporum ovalisporum. Toxins, 12(3). https://doi.org/10.3390/toxins12030196
Oliveira F, et al. Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria Microcystis Aeruginosa and Chrysosporum Ovalisporum. Toxins (Basel). 2020 03 20;12(3) PubMed PMID: 32245045.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria Microcystis aeruginosa and Chrysosporum ovalisporum. AU - Oliveira,Flavio, AU - Diez-Quijada,Leticia, AU - Turkina,Maria V, AU - Morais,João, AU - Felpeto,Aldo Barreiro, AU - Azevedo,Joana, AU - Jos,Angeles, AU - Camean,Ana M, AU - Vasconcelos,Vitor, AU - Martins,José Carlos, AU - Campos,Alexandre, Y1 - 2020/03/20/ PY - 2020/01/21/received PY - 2020/03/14/revised PY - 2020/03/18/accepted PY - 2020/4/5/entrez PY - 2020/4/5/pubmed PY - 2021/3/6/medline KW - Mytilus galloprovincialis KW - cylindrospermopsin KW - ecotoxicology KW - microcystin KW - shotgun proteomics KW - toxic cyanobacteria JF - Toxins JO - Toxins (Basel) VL - 12 IS - 3 N2 - 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. SN - 2072-6651 UR - https://www.unboundmedicine.com/medline/citation/32245045/Physiological_and_Metabolic_Responses_of_Marine_Mussels_Exposed_to_Toxic_Cyanobacteria_Microcystis_aeruginosa_and_Chrysosporum_ovalisporum_ L2 - https://www.mdpi.com/resolver?pii=toxins12030196 DB - PRIME DP - Unbound Medicine ER -