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- Impact of heat and cold events on the energetic metabolism of the C3 halophyte Halimione portulacoidesPublication . Duarte, Bernardo; Santos, D.; Marques, J. C.; Caçador, IsabelAccording to the newest predictions, it is expected that the Mediterranean systems experience more frequent and longer heat and cold treatments events. Salt marshes will be no exception. Halimione portulacoides is a widely distributed halophyte highly adapted to harsh environments. Plants exposed to heat stress showed a reduction in the maximum electron transport rates and increase in the rate of RC closure, as indicated by the increase in M0. Alongside there was also a reduction in the quinone pool size while compared to the plants maintained in the control condition. In contrast plants exposed to low temperatures didn't show any signs of damage on the ETC. Heat-exposed individuals experienced a reduction of connectivity between the PS II antennae with simultaneous inhibition of the electron transport. This was more evident in the donor side of the PS II, Being this a consequence of the damages in the oxygen-evolving complex. Also if both PS I and PS II energy fluxes are observed, there are evident differences in the thermal tolerance of both photosystems. While compared to the control group, cold exposed plants showed an increased PS I efficiency (δR0) indicating a tolerance of this photosystem to low temperatures. Nevertheless, the excessive redox potential generated by light harvesting and inefficient processing was not dissipated correctly and consequently causing a oxidative stress situation. In the present study only heat exposed plants showed a significant activation of the xanthophyll cycle. Alongside with this mechanism and similarly to what was observed for cold treated plants, it could be observed an increase in auroxanthin content, an efficient energy quencher under stress conditions. The coupled activation of the xanthophyll cycle along with a higher auroxanthin synthesis suggests that heat-treated individuals had higher needs to dissipate excessive energy than the cells exposed to cold treatment. In both cases appears to exist an efficient ROS scavenging mechanism. According to our data, heat and cold treatment events can have serious impacts on H. portulacoides photobiology reducing its primary productivity. At the ecosystem level, these climatic events could pose a serious threat to the survival of this species in the new climatic reality that our planet is facing.
- Zostera noltii development probing using chlorophyll a transient analysis (JIP-test) under field conditions: Integrating physiological insights into a photochemical stress indexPublication . Duarte, Bernardo; Pedro, Sílvia; Marques, J. C.; Adão, Helena; Caçador, IsabelBeyond their undeniable role, nowadays we also must look to seagrass beds as endangered environmentswith urgent monitoring and conservation needs. In the present study Z. noltii photochemical performanceof under different stages of development/recovery was assessed and its results applied in the develop-ment of a photochemical stress index (PSI) to classify and efficiently assess the physiological conditionof seagrass beds. In order to investigate deeper into this metabolic network the JIP-test was applied,allowing to identify the reasons underlying the first signs of stress. Less developed beds low connectiv-ity between PS II antennae leading inevitably to an impairment of the energetic transport. Associatedto this also the quinone pool showed severe depletion both in number and function. Alongside the K-step presence in the Kautsky curve points to severe damage at donor side of the PS II, where the OxygenEvolving Complexes (OECs) are located. All these negative impacts increase the quantum yield of the non-photochemical reactions in stressed/less developed seagrass beds. In sum, more developed beds showproportionally higher light use efficiencies promoted by a higher number of oxidized reaction centrescoupled with an enhanced capacity in using the generated electron potential and relatively lower energydissipations. Coupling all the photochemical into an Integrated Biomarker Response (IBR) approach, aphotochemical stress index (PSI) was produced. The PSI showed that more developed sites present lowerphotochemical stress values with inverse significant correlation with biomass coverage, reinforcing theapplicability of this non-invasive index as a reflex of the seagrass bed development stage.
- Halophyte fatty acids as biomarkers of anthropogenic-driven contamination in Mediterranean marshes: Sentinel species survey and development of an integrated biomarker response (IBR) indexPublication . Duarte, Bernardo; Carreiras, João; Pérez-Romero, Jesús Alberto; Mateos-Naranjo, Enrique; Redondo-Gómez, Susana; Matos, Ana Rita; Marques, J. C.; Caçador, IsabelEstuarine environments are extremely affected by anthropogenic-driven contamination, namely heavy metals. In the recent years, several organisms have been studied to be used as sentinel species providing a wide range of biomarkers for estuarine contamination. Only recently non-traditional biomarkers, such as fatty acids, were included in animal ecotoxicology and impact assessment studies. Nevertheless, there is a wide lack of knowledge regarding to its application in estuarine plants. Considering this the present work aimed to evaluate the application of fatty acid profiling in Mediterranean halophytic species chronically exposed to different degrees of metal contamination, while incorporating these fatty acid biomarkers into an unifying index. From the fatty acids analysis two different types of sentinel halophytes could be identified: the contamination sensitive Halimione portulacoides (sea purslane), Sarcocornia fruticosa (glasswort) and Spartina patens (saltmeadow cordgrass), and the contamination-tolerant Spartina maritima (small cordgrass). In sensitive species the most evident changes in the fatty acid profiles were the decrease in the 18:3 and the increase in the 16:0 fatty acid relative concentrations, while the inverse trend was recorded in the tolerant S. maritima under chronic contamination. Beyond the evident physiological importance, these shifts in the halophyte fatty acid profiles provide some understanding on their use as biomarkers of metal contamination. After application of an integrated biomarker response (IBR) index it was possible to conclude that in sensitive halophytes (H. portulacoides, S. fruticosa and S. patens) the samples collected from the contaminated site produce had higher IBR values than the tolerant species S. maritima being these lower values linked with an adaptation mechanism towards contamination. Furthermore, the fatty acid-based IBR index was intrinsically connected with the bioavailable metals concentrations in the rhizosediments, which make that it could be used in future impact assessment and/or ecotoxicology studies. In summary, the data showed that two of the most abundant halophytes in the Mediterranean eco-region (S. fruticose and H. portulacoides) are potential sentinel species of metal contamination, whereas its fatty acid profile is an efficient biomarker of the degree of environmental contamination.
- Marine angiosperm indices used to assess ecological status within the Water Framework Directive and South African National Water Act: Learning from differences and common issuesPublication . Duarte, Bernardo; Neto, João; Marques, J. C.; Adams, Janine B.; Caçador, IsabelThis paper reviews and discusses the methods and metrics used for the assessment of the ecological status of marine angiosperms comparing the European with the South African situation. In Europe salt marsh and seagrasses are an important biological element for establishing the ecological quality status of transitional waters and in South Africa changes over time in the salt marsh and submerged macrophyte habitats (species richness, abundance and community composition) is used nationally to assess the health of estuaries. In Europe several studies have developed metrics that include salt marsh species composition and community structure to assess the ecological quality status. Deviation of taxonomic composition and abundance from a reference situation is investigated. Multi-metric approaches have been shown to provide a more holistic view of the ecological status of the ecosystem. Many indices are highly dependent on historical data to assess the deviation from reference conditions. Within the WFD spirit one widely used approach for salt marsh assessment, the Best’s method, the baseline can be determined based on the first sampling effort, by the largest previously recorded size of the salt marsh or using the “maximum potential size” of the salt marsh from habitat prediction models. In South Africa all habitat below the 5 m contour line is considered estuary habitat and any land occupied here by agricultural or other developments is considered as a loss of habitat from the reference condition. For seagrasses European metrics are based on attributes from the community (e.g., taxonomic composition, epiphytes), the population (e.g., bed extent, shoots density), but also quantified at individual species (e.g., leaves length) or physiological levels (e.g., stable isotopic signatures). Seagrass habitats in South African estuaries are highly dynamic in response to floods and an understanding of this is needed before present ecological status can be assessed.
- DNA Sequencing as a Tool to Monitor Marine Ecological StatusPublication . Goodwin, Kelly D.; Thompson, Luke R.; Duarte, Bernardo; Kahlke, Tim; Thompson, Andrew R.; Marques, J. C.; Caçador, IsabelMany ocean policies mandate integrated, ecosystem-based approaches to marine monitoring, driving a global need for efficient, low-cost bioindicators of marine ecological quality. Most traditional methods to assess biological quality rely on specialized expertise to provide visual identification of a limited set of specific taxonomic groups, a time-consuming process that can provide a narrow view of ecological status. In addition, microbial assemblages drive food webs but are not amenable to visual inspection and thus are largely excluded from detailed inventory. Molecular-based assessments of biodiversity and ecosystem function offer advantages over traditional methods and are increasingly being generated for a suite of taxa using a “microbes to mammals” or “barcodes to biomes” approach. Progress in these efforts coupled with continued improvements in high-throughput sequencing and bioinformatics pave the way for sequence data to be employed in formal integrated ecosystem evaluation, including food web assessments, as called for in the European Union Marine Strategy Framework Directive. DNA sequencing of bioindicators, both traditional (e.g., benthic macroinvertebrates, ichthyoplankton) and emerging (e.g., microbial assemblages, fish via eDNA), promises to improve assessment of marine biological quality by increasing the breadth, depth, and throughput of information and by reducing costs and reliance on specialized taxonomic expertise.
- A tale of two spartinas: Climatic, photobiological and isotopic insights on the fitness of non-indigenous versus native speciesPublication . Duarte, Bernardo; Baeta, Alexandra; Rousseau-Gueutin, M.; Ainouche, M.; Marques, J. C.; Caçador, IsabelSalt marshes are facing a new threat: the invasion by non-indigenous species (NIS), Although its introduction time is not established yet, in 1999 Spartina versicolor was already identified as a NIS in the Mediterranean marshes, significantly spreading its area of colonization. Using the Mediterranean native Spartina maritima as a reference, the present research studied the ecophysiological fitness of this NIS in its new environment, as a tool to understand its potential invasiveness. It was found that Spartina versicolor had a stable photobiological pattern, with only minor fluctuations during an annual cycle, and lower efficiencies comparated to S. maritima. The NIS seems to be rather insensitive to the observed abiotic factors fluctuations (salinity and pH of the sediment), and thus contrasts with the native S. maritima, known to be salinity dependent with higher productivity values in higher salinity environments. Most of the differences observed between the photobiology of these species could be explained by their nitrogen nutrition (here evaluated by the δ15N stable isotope) and directly related with the Mediterranean climate. Enhanced by a higher N availability during winter, the primary production of S. maritima which lead to dilution of the foliar δ15N concentration in the newly formed biomass, similarly to what is observed along a rainfall gradient. On the other hand, S. versicolor showed an increased δ15N in its tissues along the annual rainfall gradient, probably due to a δ15N concentration effect during low biomass production periods (winter and autumn). Together with the photobiological traits, these isotopic data point out to a climatic misfit of S. versicolor to the Mediterranean climate compared to the native S. maritima. This appears to be the major constrain shaping the ecophysiological fitness of this NIS, its primary production and consequently, its spreading rate along the Mediterranean marshes.
- Ecotoxicity of the lipid-lowering drug bezafibrate on the bioenergetics and lipid metabolism of the diatom Phaeodactylum tricornutumPublication . Duarte, Bernardo; Prata, Diogo; Matos, Ana Rita; Cabrita, Maria Teresa; Caçador, Isabel; Marques, J. C.; Cabral, Henrique; Reis Santos, Patrick; Fonseca, VanessaPharmaceutical residues impose a new and emerging threat to the marine environment and its biota. In most countries, ecotoxicity tests are not required for all pharmaceutical residues classes and, even when mandatory, these tests are not performed using marine primary producers such as diatoms. These microalgae are among the most abundant class of primary producers in the marine realm and key players in the marine trophic web. Blood-lipid-lowering agents such as bezafibrate and its derivatives are among the most prescribed drugs and most frequently found human pharmaceuticals in aquatic environments. The present study aims to investigate the bezafibrate ecotoxicity and its effects on primary productivity and lipid metabolism, at environmentally relevant concentrations, using the model diatom Phaeodactylum tricornutum. Under controlled conditions, diatom cultures were exposed to bezafibrate at 0, 3, 6, 30 and 60 μg L-1, representing concentrations that can be found in the vicinity of discharges of wastewater treatment plants. High bezafibrate concentrations increased cell density and are suggested to promote a shift from autotrophic to mixotrophic metabolism, with diatoms using light energy generated redox potential to breakdown bezafibrate as carbon source. This was supported by an evident increase in cell density coupled with an impairment of the thylakoid electron transport and consequent photosynthetic activity reduction. In agreement, the concentrations of plastidial marker fatty acids showed negative correlations and Canonical Analysis of Principal coordinates of the relative abundances of fatty acid and photochemical data allowed the separation of controls and cells exposed to bezafibrate with high classification efficiency, namely for photochemical traits, suggesting their validity as suitable biomarkers of bezafibrate exposure. Further evaluations of the occurrence of a metabolic shift in diatoms due to exposure to bezafibrate is paramount, as ultimately it may reduce O2 generation and CO2 fixation in aquatic ecosystems with ensuing consequences for neighboring heterotrophic organisms.
- Phytoplankton community-level bio-optical assessment in a naturally mercury contaminated Antarctic ecosystem (Deception Island)Publication . Duarte, Bernardo; Cabrita, Maria Teresa; Vidal, Tânia; Pereira, Joana Luísa; Pacheco, Mário; Pereira, Patrícia; Canário, João; Gonçalves, Fernando J.M.; Matos, Ana Rita; Rosa, Rui; Marques, J. C.; Caçador, Isabel; Gameiro, C.Mercury naturally contaminated environments, like Deception Island (Antarctica), are field labs to study the physiological consequences of chronic Hg-exposure at the community level. Deception Island volcanic vents lead to a continuous chronic exposure of the phytoplanktonic communities to potentially toxic Hg concentrations. Comparing Hg-contaminated areas (Fumarolas Bay - FB, Gabriel de Castilla station - GdC station), no significant differences in chlorophyll a concentrations were detected, indicating that biomass production was not impaired by Hg-exposure despite the high Hg levels found in the cells. Moreover, the electron transport energy, responsible for energy production, also presented rather similar values in phytoplankton from both locations. Regarding FB communities, although the cells absorbed and trapped lower amounts of energy, the effect of Hg was not relevant in the photochemical work produced by the electronic transport chain. This might be due to the activation of alternative internal electron donors, as counteractive measure to the energy accumulated inside the cells. In fact, this alternative electron pathway, may have allowed FB communities to have similar electron transport energy fluxes without using respiration as photoprotective measure towards excessive energy. Hg-exposed cells also showed a shift from the energy flux towards the PS I (photosystem I), alleviating the excessive energy accumulation at the PS II (photosystem II) and preventing an oxidative burst. Our findings suggest a higher energy use efficiency in the communities exposed to volcanic Hg, which is not observable in cultured phytoplankton species grown under Hg exposure. This may constitute a metabolic adaptation, driven from chronic exposure allowing the maintenance of high levels of primary productivity under the assumingly unfavourable conditions of Deception Island.
- Disentangling the photochemical salinity tolerance in Aster tripolium L.: connecting biophysical traits with changes in fatty acid compositionPublication . Duarte, Bernardo; Cabrita, M. T.; Gameiro, Carla; Matos, A. R.; Godinho, R.; Marques, J. C.; Caçador, IsabelA profound analysis of A. tripolium photochemical traits under salinity exposure is lacking in the literature, with very few references focusing on its fatty acid profile role in photophysiology. To address this, the deep photochemical processes were evaluated by Pulse Amplitude Modulated (PAM) Fluorometry coupled with a discrimination of its leaf fatty acid profile. Plants exposed to 125-250 mm NaCl showed higher photochemical light harvesting efficiencies and lower energy dissipation rates. under higher NaCl exposure, there is evident damage of the oxygen evolving complexes (OECs). On the other hand, Reaction Centre (RC) closure net rate and density increased, improving the energy fluxes entering the PS II, in spite of the high amounts of energy dissipated and the loss of PS II antennae connectivity. Energy dissipation was mainly achieved through the auroxanthin pathway. Total fatty acid content displayed a similar trend, being also higher under 125-250 mm NaCl with high levels of omega-3 and omega-6 fatty acids. The increase in oleic acid and palmitic acid allows the maintenance of the good functioning of the PS II. Also relevant was the high concentration of chloroplastic C16:1t in the individuals subjected to 125-250 mm NaCl, related with a higher electron transport activity and with the organization of the Light Harvesting Complexes (LHC) and thus reducing the activation of energy dissipation mechanisms. All these new insights shed some light not only on the photophysiology of this potential cash-crop, but also highlight its important saline agriculture applications of this species as forage and potential source of essential fatty acids.
- Ecophysiological response of native and invasive Spartina species to extreme temperature events in Mediterranean marshesPublication . Duarte, Bernardo; Marques, J. C.; Caçador, IsabelThe recent IPCC WG2 5th Assessment Report (IPCC 2014), notes an increase in the frequency and duration of extreme climatic events, especially for the Mediterranean region. Together with climate change, the invasion of natural communities by non-indigenous species (NIS) constitutes a serious threat to biodiversity. One of these NIS is the American Spartina patens, now present in Western European marshes. The present study aims to understand the biochemical and photochemical responses of S. patens compared with S. maritima under extreme temperature events. Under normal and extreme heat conditions, S. patens had a higher photosynthetic efficiency (α), compared with cold wave events, where the native S. maritima was far more efficient. This reduced photosynthetic efficiency was mostly due to a decrease in the connectivity between photosystem II (PSII) antennae. This was accompanied by severe damage to the oxygen-evolving complex of PSII. On the other hand, S. patens oxygen evolving complexes (OECs) seem to be temperature insensitive. The light absorption capacity was maintained due to a higher net rate of reaction centre (RC) closure as a counteractive measure of the reduced number of RC, especially in S. maritima. The loss of connectivity between PSII antennae and damage in OECs under heat stress leads to a severe reduction in the maximum yield for photochemistry enhanced by the low probability of each absorbed quanta to produce electronic work. However, while S. maritima presents high energy losses under heat stress, S. patens developed efficient quenching mechanisms under thermal stress, through auroxanthin. In S. patens, cold wave-treated individuals also displayed a very active line of enzymatic defences for reactive oxygen species scavenging. In fact, only cold treated individuals of this species presented higher activities of anti-oxidant enzymes, revealing some degree of adaptation to this new environment. In contrast, in S. maritima the exposure to extreme heat periods led, in most cases, to a decrease in the enzymatic defences, leaving the cell prone to oxidative damage. In summary, S. patens appears to have a higher fitness for the incoming climatic scenarios, being more tolerant to heat stress, while S. maritima will have its photobiological fitness decreased. This will impose a shift in the salt marsh biodiversity, favouring the non-indigenous S. patens expansion.