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Effects of glyphosate-based herbicide on primary production and physiological fitness of the macroalgae Ulva lactuca

Publication . Carvalho, Ricardo Cruz de; Feijão, Eduardo; Matos, Ana Rita; Cabrita, Maria Teresa; Utkin, Andrei B.; Novais, Sara C.; Lemos, Marco F.L.; Caçador, Isabel; Marques, João Carlos; Reis-Santos, Patrick; Fonseca, Vanessa F.; Duarte, Bernardo

The use of glyphosate-based herbicides (GBHs) worldwide has increased exponentially over the last two decades increasing the environmental risk to marine and coastal habitats. The present study investigated the effects of GBHs at environmentally relevant concentrations (0, 10, 50, 100, 250, and 500 ug.L-1) on the physiology and biochemistry (photosynthesis, pigment, and lipid composition, antioxidative systems and energy balance) of Ulva lactuca, a cosmopolitan marine macroalgae species. Although GBHs cause deleterious effects such as the inhibition of photosynthetic activity, particularly at 250 ug.L-1, due to the impairment of the electron transport in the chloroplasts, these changes are almost completely reverted at the highest concentration (500 ug.L-1). This could be related to the induction of tolerance mechanisms at a certain threshold or tipping point. While no changes occurred in the energy balance, an increase in the pigment antheraxanthin is observed jointly with an increase in ascorbate peroxidase activity. These mechanisms might have contributed to protecting thylakoids against excess radiation and the increase in reactive oxygen species, associated with stress conditions, as no increase in lipid peroxidation products was observed. Furthermore, changes in the fatty acids profile, usually attributed to the induction of plant stress response mechanisms, demonstrated the high resilience of this macroalgae. Notably, the application of bio-optical tools in ecotoxicology, such as pulse amplitude modulated (PAM) fluorometry and laser-induced fluorescence (LIF), allowed separation of the control samples and those treated by GBHs in different concentrations with a high degree of accuracy, with PAM more accurate in identifying the different treatments.

2022Journal article

Open access

Fluoxetine arrests growth of the model diatom Phaeodactylum tricornutum by increasing oxidative stress and altering energetic and lipid metabolism

Publication . Feijão, Eduardo; Carvalho, Ricardo Cruz de; Duarte, Irina A.; Matos, Ana Rita; Cabrita, Maria Teresa; Novais, Sara C.; Lemos, Marco F.L.; Caçador, Isabel; Marques, João Carlos; Reis-Santos, Patrick; Fonseca, Vanessa F.; Duarte, Bernardo

Pharmaceutical residues impose a new and emerging threat to aquatic environments and its biota. One of the most commonly prescribed pharmaceuticals is the antidepressant fluoxetine, a selective serotonin re-uptake inhibitor that has been frequently detected, in concentrations up to 40 ug L-1, in aquatic ecosystems. The present study aims to investigate the ecotoxicity of fluoxetine at environmentally relevant concentrations (0.3, 0.6, 20, 40, and 80 ug L-1) on cell energy and lipid metabolism, as well as oxidative stress biomarkers in the model diatom Phaeodactylum tricornutum. Exposure to higher concentrations of fluoxetine negatively affected cell density and photosynthesis through a decrease in the active PSII reaction centers. Stress response mechanisms, like b-carotene (b-car) production and antioxidant enzymes [superoxide dismutase (SOD) and ascorbate peroxidase (APX)] up-regulation were triggered, likely as a positive feedback mechanism toward formation of fluoxetine-induced reactive oxygen species. Lipid peroxidation products increased greatly at the highest fluoxetine concentration whereas no variation in the relative amounts of long chain polyunsaturated fatty acids (LC-PUFAs) was observed. However, monogalactosyldiacylglycerol-characteristic fatty acids such as C16:2 and C16:3 increased, suggesting an interaction between light harvesting pigments, lipid environment, and photosynthesis stabilization. Using a canonical multivariate analysis, it was possible to evaluate the efficiency of the application of bio-optical and biochemical techniques as potential fluoxetine exposure biomarkers in P. tricornutum. An overall classification efficiency to the different levels of fluoxetine exposure of 61.1 and 88.9% were obtained for bio-optical and fatty acids profiles, respectively, with different resolution degrees highlighting these parameters as potential efficient biomarkers. Additionally, the negative impact of this pharmaceutical molecule on the primary productivity is also evident alongside with an increase in respiratory oxygen consumption. From the ecological point of view, reduction in diatom biomass due to continued exposure to fluoxetine may severely impact estuarine and coastal trophic webs, by both a reduction in oxygen primary productivity and reduced availability of key fatty acids to the dependent heterotrophic upper levels.

2020Journal article

Open access

Evaluation of multivariate biomarker indexes application in ecotoxicity tests with marine diatoms exposed to emerging contaminants

Publication . Pires, Vanessa; Novais, Sara C.; Lemos, Marco F.L.; Fonseca, Vanessa; Duarte, Bernardo

Worldwide anthropogenic activities result in the production and release of potentially damaging toxic pollutants into ecosystems, thereby jeopardizing their health and continuity. Research studies and biomonitoring programs attend to this emerging problematic by applying and developing statistically relevant indexes that integrate complex biomarker response data to provide a holistic approach, reflecting toxically induced alterations at the organism or population level. Ultimately, indexes allow simple result communications, enhancing policy makers understanding, and contributing to better resource and environmental managing policies. In this study three indexes, the integrated biomarker response index (IBR), the bioeffects assessment index (BAI) and principal components analysis (PCA), were evaluated for their sensitivity in revealing toxically induced stress patterns in cells of the diatom Phaeodactylum tricornutum under contaminant exposure. The set of biomarkers selected for index construction comprised the anti-oxidant enzymes APX, CAT and SOD, and the lipid peroxidation marker TBARS. Several significant correlations with the applied concentration gradients were noticed for all indexes, although IBR excelled for its reliability in delivering statistically significant dose-response patterns for four out of the five tested compounds.

2021Journal article

Open access

Glyphosate-based herbicide toxicophenomics in marine diatoms: impacts on primary production and physiological fitness

Publication . Carvalho, Ricardo Cruz de; Feijão, Eduardo; Matos, Ana Rita; Cabrita, Maria Teresa; Novais, Sara C.; Lemos, Marco F.L.; Caçador, Isabel; Marques, João Carlos; Reis-Santos, Patrick; Fonseca, Vanessa F.; Duarte, Bernardo

Glyphosate is the main active component of the commercial formulation Roundup®, the most widely used chemical herbicide worldwide. However, its potential high toxicity to the environment and throughout trophic webs has come under increasing scrutiny. The present study aims to investigate the application of bio-optical techniques and their correlation to physiological and biochemical processes, including primary productivity, oxidative stress, energy balance, and alterations in pigment and lipid composition in Phaeodactylum tricornutum, a representative species of marine diatoms, using the case study of its response to the herbicide glyphosate-based Roundup® formulation, at environmentally relevant concentrations. Cultures were exposed to the herbicide formulation representing effective glyphosate concentrations of 0, 10, 50, 100, 250, and 500 ug L-1. Results showed that high concentrations decreased cell density; furthermore, the inhibition of photosynthetic activity was not only caused by the impairment of electron transport in the thylakoids, but also by a decrease of antioxidant capacity and increased lipid peroxidation. Nevertheless, concentrations of one of the plastidial marker fatty acids had a positive correlation with the highest concentration as well as an increase in total protein. Cell energy allocation also increased with concentration, relative to control and the lowest concentration, although culture growth was inhibited. Pigment composition and fatty acid profiles proved to be efficient biomarkers for the highest glyphosate-based herbicide concentrations, while bio-optical data separated controls from intermediate concentrations and high concentrations.

2020Journal article

Open access

Effect biomarkers of the widespread antimicrobial triclosan in a marine model diatom

Publication . Duarte, Bernardo; Feijão, Eduardo; Carvalho, Ricardo Cruz de; Matos, Ana Rita; Cabrita, Maria Teresa; Novais, Sara C.; Moutinho, Ariana; Lemos, Marco F.L.; Marques, João Carlos; Caçador, Isabel; Reis-Santos, Patrick; Fonseca, Vanessa

The present-day COVID-19 pandemic has led to the increasing daily use of antimicrobials worldwide. Triclosan is a manmade disinfectant chemical used in several consumer healthcare products, and thus frequently detected in surface waters. In the present work, we aimed to evaluate the effect of triclosan on diatom cell photophysiology, fatty acid profiles, and oxidative stress biomarkers, using the diatom Phaeodactylum tricornutum as a model organism. Several photochemical effects were observed, such as the lower ability of the photosystems to efficiently trap light energy. A severe depletion of fucoxanthin under triclosan application was also evident, pointing to potential use of carotenoid as reactive oxygen species scavengers. It was also observed an evident favouring of the peroxidase activity to detriment of the SOD activity, indicating that superoxide anion is not efficiently metabolized. High triclosan exposure induced high cellular energy allocation, directly linked with an increase in the energy assigned to vital functions, enabling cells to maintain the growth rates upon triclosan exposure. Oxidative stress traits were found to be the most efficient biomarkers as promising tools for triclosan ecotoxicological assessments. Overall, the increasing use of triclosan will lead to significant effects on the diatom photochemical and oxidative stress levels, compromising key roles of diatoms in the marine system.

2022Journal article

Open access