Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria <i>Microcystis aeruginosa</i> and <i>Chrysosporum ovalisporum</i>

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...

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Main Authors: Flavio Oliveira, Leticia Diez-Quijada, Maria V. Turkina, João Morais, Aldo Barreiro Felpeto, Joana Azevedo, Angeles Jos, Ana M. Camean, Vitor Vasconcelos, José Carlos Martins, Alexandre Campos
Format: Article
Language:English
Published: MDPI AG 2020-03-01
Series:Toxins
Subjects:
Online Access:https://www.mdpi.com/2072-6651/12/3/196
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language English
format Article
sources DOAJ
author Flavio Oliveira
Leticia Diez-Quijada
Maria V. Turkina
João Morais
Aldo Barreiro Felpeto
Joana Azevedo
Angeles Jos
Ana M. Camean
Vitor Vasconcelos
José Carlos Martins
Alexandre Campos
spellingShingle Flavio Oliveira
Leticia Diez-Quijada
Maria V. Turkina
João Morais
Aldo Barreiro Felpeto
Joana Azevedo
Angeles Jos
Ana M. Camean
Vitor Vasconcelos
José Carlos Martins
Alexandre Campos
Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria <i>Microcystis aeruginosa</i> and <i>Chrysosporum ovalisporum</i>
Toxins
<i>mytilus galloprovincialis</i>
toxic cyanobacteria
microcystin
cylindrospermopsin
ecotoxicology
shotgun proteomics
author_facet Flavio Oliveira
Leticia Diez-Quijada
Maria V. Turkina
João Morais
Aldo Barreiro Felpeto
Joana Azevedo
Angeles Jos
Ana M. Camean
Vitor Vasconcelos
José Carlos Martins
Alexandre Campos
author_sort Flavio Oliveira
title Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria <i>Microcystis aeruginosa</i> and <i>Chrysosporum ovalisporum</i>
title_short Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria <i>Microcystis aeruginosa</i> and <i>Chrysosporum ovalisporum</i>
title_full Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria <i>Microcystis aeruginosa</i> and <i>Chrysosporum ovalisporum</i>
title_fullStr Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria <i>Microcystis aeruginosa</i> and <i>Chrysosporum ovalisporum</i>
title_full_unstemmed Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria <i>Microcystis aeruginosa</i> and <i>Chrysosporum ovalisporum</i>
title_sort physiological and metabolic responses of marine mussels exposed to toxic cyanobacteria <i>microcystis aeruginosa</i> and <i>chrysosporum ovalisporum</i>
publisher MDPI AG
series Toxins
issn 2072-6651
publishDate 2020-03-01
description 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 <i>Mytilus galloprovincialis</i> 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, <i>Microcystis aeruginosa</i> and <i>Chrysosporum ovalisporum</i> at 1 &#215; 10<sup>5</sup> cells/mL, resembling a natural cyanobacteria bloom. The estimated amount of toxins produced by <i>M. aeruginosa</i> and <i>C. ovalisporum</i> 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 <i>Parachlorella kessleri</i>. The results showed that the marine mussel is able to filter toxic cyanobacteria at a rate equal or higher than the non-toxic microalga <i>P. kessleri</i>. Filtration rates observed after 15 days of feeding toxic microalgae were 1773.04 mL/ind.h (for <i>M. aeruginosa</i>), 2151.83 mL/ind.h (for <i>C. ovalisporum</i>), 1673.29 mL/ind.h (for the mixture of the 2 cyanobacteria) and 2539.25 mL/ind.h (for the non-toxic <i>P. kessleri</i>). 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.
topic <i>mytilus galloprovincialis</i>
toxic cyanobacteria
microcystin
cylindrospermopsin
ecotoxicology
shotgun proteomics
url https://www.mdpi.com/2072-6651/12/3/196
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spelling doaj-f5c1044ece144862b960b0bf4349aec32020-11-25T03:11:37ZengMDPI AGToxins2072-66512020-03-0112319610.3390/toxins12030196toxins12030196Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria <i>Microcystis aeruginosa</i> and <i>Chrysosporum ovalisporum</i>Flavio Oliveira0Leticia Diez-Quijada1Maria V. Turkina2João Morais3Aldo Barreiro Felpeto4Joana Azevedo5Angeles Jos6Ana M. Camean7Vitor Vasconcelos8José Carlos Martins9Alexandre Campos10CIIMAR- 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, PortugalArea of Toxicology, Faculty of Pharmacy, Universidad de Sevilla, Profesor García González n2, 41012 Seville, SpainDepartment of Biomedical and Clinical Sciences, Faculty of Medicine and Clinical Sciences, Linköping University, 581 83 Linköping, SwedenCIIMAR- 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, PortugalCIIMAR- 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, PortugalCIIMAR- 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, PortugalArea of Toxicology, Faculty of Pharmacy, Universidad de Sevilla, Profesor García González n2, 41012 Seville, SpainArea of Toxicology, Faculty of Pharmacy, Universidad de Sevilla, Profesor García González n2, 41012 Seville, SpainCIIMAR- 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, PortugalCIIMAR- 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, PortugalCIIMAR- 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, PortugalToxic 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 <i>Mytilus galloprovincialis</i> 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, <i>Microcystis aeruginosa</i> and <i>Chrysosporum ovalisporum</i> at 1 &#215; 10<sup>5</sup> cells/mL, resembling a natural cyanobacteria bloom. The estimated amount of toxins produced by <i>M. aeruginosa</i> and <i>C. ovalisporum</i> 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 <i>Parachlorella kessleri</i>. The results showed that the marine mussel is able to filter toxic cyanobacteria at a rate equal or higher than the non-toxic microalga <i>P. kessleri</i>. Filtration rates observed after 15 days of feeding toxic microalgae were 1773.04 mL/ind.h (for <i>M. aeruginosa</i>), 2151.83 mL/ind.h (for <i>C. ovalisporum</i>), 1673.29 mL/ind.h (for the mixture of the 2 cyanobacteria) and 2539.25 mL/ind.h (for the non-toxic <i>P. kessleri</i>). 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.https://www.mdpi.com/2072-6651/12/3/196<i>mytilus galloprovincialis</i>toxic cyanobacteriamicrocystincylindrospermopsinecotoxicologyshotgun proteomics