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Effects of Propranolol on Growth, Lipids and Energy Metabolism and Oxidative Stress Response of Phaeodactylum tricornutum

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MARE—Marine and Environmental Sciences Centre, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisbon, Portugal
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Departamento de Biologia Vegetal, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisbon, Portugal
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cE3c, Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, Campo Grande, Edifício C2, Piso 5, 1749-016 Lisbon, Portugal
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BioISI—Biosystems and Integrative Sciences Institute, Plant Functional Genomics Group, Departamento de Biologia Vegetal, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisbon, Portugal
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Centro de Estudos Geográficos (CEG), Instituto de Geografia e Ordenamento do Território (IGOT), Universidade de Lisboa, Rua Branca Edmée Marques, 1600-276 Lisbon, Portugal
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MARE—Marine and Environmental Sciences Centre, ESTM, Politécnico de Leiria, 2520-641 Peniche, Portugal
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MARE—Marine and Environmental Sciences Centre, Department of Life Sciences, University of Coimbra, 3000 Coimbra, Portugal
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Southern Seas Ecology Laboratories, School of Biological Sciences, The University of Adelaide, Aldeide, SA 5005, Australia
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Author to whom correspondence should be addressed.
Biology 2020, 9(12), 478; https://doi.org/10.3390/biology9120478
Received: 6 November 2020 / Revised: 8 December 2020 / Accepted: 11 December 2020 / Published: 18 December 2020
(This article belongs to the Section Marine Biology)
In the past two decades, increasing attention has been directed to investigate the incidence and consequences of pharmaceuticals in the aquatic environment. Propranolol is a non-selective β-adrenoceptor blocker used in large quantities worldwide to treat cardiovascular conditions. Diatoms (model organism) exposed to this compound showed evident signs of oxidative stress, a significant reduction of the autotrophic O2 production and an increase in the heterotrophic mitochondrial respiration. Additionally, diatoms exposed to propranolol showed a consumption of its storage lipids. In ecological terms this will have cascading impacts in the marine trophic webs, where these organisms are key elements, through a reduction of the water column oxygenation and essential fatty acid availability to the heterotrophic organisms that depend on these primary producers. In ecotoxicological terms, diatoms photochemical and fatty acid traits showed to be potential good biomarkers for toxicity assessment of diatoms exposed to this widespread pharmaceutical compound.
Present demographic trends suggest a rise in the contributions of human pharmaceuticals into coastal ecosystems, underpinning an increasing demand to evaluate the ecotoxicological effects and implications of drug residues in marine risk assessments. Propranolol, a non-selective β-adrenoceptor blocker, is used worldwide to treat high blood pressure conditions and other related cardiovascular conditions. Although diatoms lack β-adrenoceptors, this microalgal group presents receptor-like kinases and proteins with a functional analogy to the animal receptors and that can be targeted by propranolol. In the present work, the authors evaluated the effect of this non-selective β-adrenoceptor blocker in diatom cells using P. tricornutum as a model organism, to evaluate the potential effect of this compound in cell physiology (growth, lipids and energy metabolism and oxidative stress) and its potential relevance for marine ecosystems. Propranolol exposure leads to a significant reduction in diatom cell growth, more evident in the highest concentrations tested. This is likely due to the observed impairment of the main primary photochemistry processes and the enhancement of the mitochondrial respiratory activity. More specifically, propranolol decreased the energy transduction from photosystem II (PSII) to the electron transport chain, leading to an increase in oxidative stress levels. Cells exposed to propranolol also exhibited high-dissipated energy flux, indicating that this excessive energy is efficiently diverted, to some extent, from the photosystems, acting to prevent irreversible photoinhibition. As energy production is impaired at the PSII donor side, preventing energy production through the electron transport chain, diatoms appear to be consuming storage lipids as an energy backup system, to maintain essential cellular functions. This consumption will be attained by an increase in respiratory activity. Considering the primary oxygen production and consumption pathways, propranolol showed a significant reduction of the autotrophic O2 production and an increase in the heterotrophic mitochondrial respiration. Both mechanisms can have negative effects on marine trophic webs, due to a decrease in the energetic input from marine primary producers and a simultaneous oxygen production decrease for heterotrophic species. In ecotoxicological terms, bio-optical and fatty acid data appear as highly efficient tools for ecotoxicity assessment, with an overall high degree of classification when these traits are used to build a toxicological profile, instead of individually assessed. View Full-Text
Keywords: energy metabolism; pharmatoxicology; photobiology; primary producers; toxicophenomics energy metabolism; pharmatoxicology; photobiology; primary producers; toxicophenomics
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MDPI and ACS Style

Duarte, B.; Feijão, E.; Cruz de Carvalho, R.; Duarte, I.A.; Silva, M.; Matos, A.R.; Cabrita, M.T.; Novais, S.C.; Lemos, M.F.L.; Marques, J.C.; Caçador, I.; Reis-Santos, P.; Fonseca, V.F. Effects of Propranolol on Growth, Lipids and Energy Metabolism and Oxidative Stress Response of Phaeodactylum tricornutum. Biology 2020, 9, 478. https://doi.org/10.3390/biology9120478

AMA Style

Duarte B, Feijão E, Cruz de Carvalho R, Duarte IA, Silva M, Matos AR, Cabrita MT, Novais SC, Lemos MFL, Marques JC, Caçador I, Reis-Santos P, Fonseca VF. Effects of Propranolol on Growth, Lipids and Energy Metabolism and Oxidative Stress Response of Phaeodactylum tricornutum. Biology. 2020; 9(12):478. https://doi.org/10.3390/biology9120478

Chicago/Turabian Style

Duarte, Bernardo, Eduardo Feijão, Ricardo Cruz de Carvalho, Irina A. Duarte, Marisa Silva, Ana R. Matos, Maria T. Cabrita, Sara C. Novais, Marco F.L. Lemos, João C. Marques, Isabel Caçador, Patrick Reis-Santos, and Vanessa F. Fonseca 2020. "Effects of Propranolol on Growth, Lipids and Energy Metabolism and Oxidative Stress Response of Phaeodactylum tricornutum" Biology 9, no. 12: 478. https://doi.org/10.3390/biology9120478

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