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- DNA damage and lipid peroxidation vs. protection responses in the gill of Dicentrarchus labrax L. from a contaminated coastal lagoon (Ria de Aveiro, Portugal)Publication . Ahmad, I.; Maria, Vera L.; Oliveira, M.; Serafim, Angela; Bebianno, Maria João; Pacheco, M.; Santos, M.A.The present research work aimed to investigate the damage vs. protection responses in gill of European sea bass (Dicentrarchus labrax) captured at a polluted coastal lagoon, Ria de Aveiro (Portugal), as a tool to evaluate the human impacts on environmental health. Damage was assessed as DNA strand breakage and lipid peroxidation (LPO) whereas protection was evaluated by measuring catalase (CAT), glutathione peroxidase (GPX), glutathione reductase (GR), glutathione S-transferase (GST), total glutathione (GSHt), thiols and metallothioneins (MT). Fish were caught at five locations: Gafanha (GAF), Rio Novo do Príncipe (RIO), Laranjo (LAR) and Vagos (VAG) presenting each a different recognized source of contamination, and Torreira (TOR), assumed as reference site. Among the surveyed sites, gill damage was observed only at GAF, as measured by DNA integrity loss and LPO increase. An overall induction in enzymatic antioxidant protection was perceptible in fish from GAF and VAG, expressed as higher GPX, GR and GST activities. In addition, LAR fish showed elevated GST and CAT activities. Thiols content was higher in all study sites irrespective to the pollution spectrum, whereas GSHt increase was only observed at GAF and VAG. The highest MT level was detected in fish from VAG and the lowest level from RIO suggesting a low contamination degree on this particular site. Globally, the results expressed site-specific response patterns, signalling two critical areas - GAF and VAG. Additionally, a joint analysis (damage vs. protection) allowed the following ordering of surveyed sites according to the contamination degree and risk to fish health; GAF>VAG>LAR>RIO>TOR. D. labrax gill responses demonstrated their efficacy as early warning signals of the contaminants presence. Moreover, the adopted approach, considering simultaneously protection responses and damaging effects, also revealed its usefulness on the pollution extent assessment.
- Comparative petroleum hydrocarbons levels and biochemical responses in mussels from hydrothermal vents (Bathymodiolus azoricus) and coastal environments (Mytilus galloprovincialis)Publication . Serafim, Angela; Lopes, Belisandra; Company, Rui; Ferreira, A. M.; Bebianno, Maria JoãoAliphatic hydrocarbons and PAHs in the whole soft tissues of Bathymodiolus azoricus from three Mid-Atlantic Ridge hydrothermal vents (Menez-Gwen, Lucky Strike and Rainbow), and Mytilus galloprovincialis from three contaminated coastal sites in South Portugal were analysed, and its effects on the digestive gland microsomes mixed-function oxygenase system (MFO) were assessed. Aliphatic hydrocarbons levels were present in the same magnitude in both coastal and hydrothermal environments, while the UCM (unresolved complex mixture) for coastal mussels were higher than in vent mussels. In general, significantly higher PAHs concentrations were found in coastal mussels, compared to B. azoricus where low molecular weight PAHs (2-3 rings) represented the majority of PAHs contrarily to what was observed in M. galloprovincialis. The MFO components were present in both mussel species, and were detected in vent mussels for the first time. However this system seems to have different roles in species from these contrasting environments. In coastal mussels MFO responded to hydrocarbon contamination while response in hydrothermal organisms appeared to be related mainly to endogenous factors.
- A multibiomarker approach in Mytilus galloprovincialis to assess environmental qualityPublication . Cravo, Alexandra; Lopes, Belisandra; Serafim, M.A.; Company, Rui; Barreira, Luísa; Gomes, Tânia; Bebianno, Maria JoãoA multibiomarker approach was carried out for the first time in the South Portuguese Coast using Mytilus galloprovincialis, to assess environmental quality, establish if there are adverse biological responses associated to different sources of anthropogenic contamination and to determine spatial and seasonal trends. For this purpose the battery of biomarkers selected was: superoxide dismutase (SOD), catalase (CAT), glutathione peroxidases (GPx total and Se dependent), Cytochrome P450 component system, Glutathione-S-transferase (GST) and acetylcholinesterase (AChE), metallothionein (MT) and lead-delta-aminolevulinic acid dehydratase (ALAD), lipid peroxidation (LPO) and Condition Index (CI) along with the determination of PAHs and metals (Cd, Cu, Ni, Pb and Zn). Results show that despite the levels of both organic and metallic contaminants in these eight spots in the South Coast of Portugal not being particularly high compared with other contaminated/polluted sites worldwide, the selected battery of biomarkers responded efficiently to the environmental changes and allowed an environmental assessment between seasons and sites. Different spatial and seasonal responses were evident along the South Coast of Portugal, meaning that the contamination is not homogeneous. This does not only reflect different competition, origin and intensity of contamination, but also different environmental conditions (e.g. temperature, salinity). Along the South Portuguese Coast site 8 was the most contaminated, while site 2 was considered the least contaminated. Despite environmental factors possibly causing difficulties in the general interpretation of biomarker data, those that better responded to environmental contamination were CYP450, SOD-mit and T-GPx for the summation SigmaPAHs, MT (digestive gland) for metals (especially Cu), ALAD for Pb and LPO for both organic and metallic contamination. These biomarkers were also positively correlated with temperature in summer, revealing this as a more stressful/critical season. In future environmental contamination assessments there is no need to analyse the components b5, P418, NADH and NADPH of phase I MFO system, and MT in the gills, since their responses are not evident.
- Effect of cadmium, copper and mercury on antioxidant enzyme activities and lipid peroxidation in the gills of the hydrothermal vent mussel Bathymodiolus azoricusPublication . Company, Rui; Serafim, Angela; Bebianno, Maria João; Cosson, R.; Shillito, B.; Fiala-Médioni, A.Metals are known to influence lipid peroxidation and oxidative status of marine organisms. Hydrothermal vent mussels Bathymodiolus azoricus live in deep-sea environments with anomalous conditions, including high metal concentrations. Although B. azoricus are aerobic organisms they possess abundant methano and thioautotrophic symbiotic bacteria in the gills. The enzymatic defences (superoxide dismutase (SOD), catalase (CAT), total glutathione peroxidase (Total GPx) and selenium-dependent glutathione peroxidase (Se-GPx)) and lipid peroxidation were determined in the gills of B. azoricus exposed to Cd (0.9 microM), Cu (0.4 microM) and Hg (0.1 microM) with different times of exposure. The experiments were performed in pressurized containers at 9+/-1 degrees C and 85 bars. Results show that vent mussels possess antioxidant enzymatic protection in the gills. Cd and Cu had an inhibitory effect in the enzymatic defence system, contrarily to Hg. These enzymatic systems are not completely understood in the B. azoricus, since reactive oxygen species might be produced through other processes than natural redox cycling, due to hydrogen sulphide and oxygen content present. Also the symbiotic bacteria may play an important contribution in the antioxidant protection of the gills.
- Variation of metal and metallothionein concentrations in a natural population of ruditapes decussatusPublication . Bebianno, Maria João; Serafim, A.The spatial and seasonal variation of total and subcellular distribution of Cd, Cu, and Zn was followed in different tissues (gills, digestive gland, and remaining tissues) of the clam Ruditapes decussatus collected along a metal contamination gradient in the Ria Formosa lagoon (southern Portugal) and compared with metallothionein (MT) concentrations.Total metal concentrations decreased according to the sequence digestive gland > gills > remaining tissues for Cd, digestive gland approximately gills > remaining tissues for Cu and gills > digestive gland > remaining tissues for Zn. MT concentrations in these tissues decreased according to the same sequence observed for Cd. In all the tissues, the highest subcellular concentration was in the cytosol for Cd and Cu and in the pellet for Zn. Among the three metals, Cd concentrations showed the most evident spatial variation. In all tissues, total and subcellular Cd concentrations decreased from the inner parts of the lagoon toward the ocean. However, no significant spatial or seasonal variation occurred in clam tissues for the other two metals, though marginal elevated Cu concentrations were observed in the inner parts of the lagoon. Therefore, Cu subcellular distribution in clam tissues was not significantly altered by Cu changes in the lagoon and are the baseline levels for normal metabolism of this clam population. The fact that total Zn concentrations remained unchanged both spatial and seasonal suggested that these clams regulate Zn in their tissues. In the three tissues, MT bind most significantly to Cd and Cu, while Zn, although binding to MT, is preferably bound to other ligands. MT concentrations showed the same spatial and seasonal variation of Cd and were significantly related with total and heat-treated cytosolic Cd in all tissues. For Cu a significant relationship between MT and total or cytosolic Cu was only observed in the remaining tissues. No relationship was observed between MT and total or cytosolic Zn concentrations. Metals and MT concentrations increased with the increase in the condition index for the gills and the digestive gland and decreased from the remaining tissues.Cd concentrations in the gills increased only in the heat-treated cytosolic fraction while Zn in this fraction decreased. Thus Cd concentrations in this tissue displaced Zn from the MT-fraction, leading to a modification of the soluble/insoluble Zn ratio once total Zn concentrations remained unchanged. This modification reflects a perturbation in the normal metabolism in this tissue due to the excess of Cd present. With the exception of the gills, Zn subcellular distribution in the other two tissues was similar among sites and season. The model that describes the relationship between MT, metals, and weight in the gills, digestive gland and remaining tissues also indicates that Cd was the only metal that influence MT synthesis significantly in all the tissues. The induced and/or existent MT was sufficient to bind free Cd ions present in the cells, preventing any damage to cellular metabolism in this clam population. Therefore, MT in the gills and digestive gland of R. decussatus can be used as an early warning signal for Cd exposure and are a useful biomarker to assess the toxicological status of this population in the Ria Formosa lagoon.
- Contamination assessment of a coastal lagoon (Ria de Aveiro, Portugal) using defence and damage biochemical indicators in gill of Liza aurata – An integrated biomarker approachPublication . Oliveira, M.; Maria, Vera L.; Ahmad, I.; Serafim, Angela; Bebianno, Maria João; Pacheco, M.; Santos, M. A.Fish gill importance in toxicants uptake, bioconcentration and excretion allied to meagre knowledge on branchial damage/protection responses substantiate this study. Five critical sites in Ria de Aveiro (Portugal) were assessed in comparison with a reference site (Torreira), focusing on Liza aurata gill antioxidant defences versus damage (oxidative and genetic). Only in Barra fish displayed damage (lipid peroxidation) though no differences were found in antioxidants. In all other sites, except Rio, antioxidant alterations were found. Thus, fish from Gafanha, Laranjo and Vagos showed higher total glutathione, glutathione peroxidase and catalase. Higher glutathione reductase and glutathione S-transferase activity was also found in the first and the last sites, respectively. In Laranjo, metallothionein levels were higher though lower in Gafanha and Vagos. In general, damage was not accompanied by defences weakening confirming that predicting damage based on antioxidants depletion is not straightforward. The integrated biomarker response index ranked sites as: Gafanha>Barra>Laranjo>Vagos>Rio>Torreira.
- Biomarkers in Ruditapes decussatus: a potential bioindicator speciesPublication . Bebianno, Maria João; Géret, F.; Hoarau, P.; Serafim, Angela; Coelho, M. R.; Gnassia-barelli, M.; Roméo, M.The clam Ruditapes decussatus is distributed worldwide and due to its ecological and economical interest has been proposed as a bioindicator in areas where mussels are not available. The accumulation of several anthropogenic compounds in their tissues suggests that they possess mechanisms that allow them to cope with the toxic effects of these contaminants. Besides pollutant uptake, the use of biomarkers is pointed out in this paper since it is a promising approach to monitor the effect of these contaminants in the marine environment. Biomarkers complement the information of the direct chemical characterization of different types of contaminants. Therefore, the aim of this paper is to review the role of several biomarkers: (metallothioneins (MT), superoxide dismutase (SOD), catalase (CAT), glutathione peroxidases (GPx) (total and selenium-dependent), lipid peroxidation (measured as MDA, one of the final products of lipid peroxidation), glutathione S-transferase (GST) and acetylcholinesterase (AChE), measured in different tissues of the clam R. decussatus, in laboratory conditions and under various environmental stresses, in two ecosystems (Ria Formosa lagoon- Portugal) and Bizerta lagoon (Tunisia) in a perspective of a multibiomarker approach to assess environmental changes. Experiment and field studies are in good agreement since MT levels, especially in the gills, the first target tissue of these contaminants, can be used as biomarker of exposure to Cd. GPx and MDA may also be determined in this respect. AChE activity is inhibited by pesticide and, to a less extent, by metal exposure in the gills and whole soft body of clams. However, the induction of GST isoforms experimentally demonstrated is not observed in the field because only global GST activity was determined. The whole set of results opens new research perspectives for the use of this species to assess the effect of mixtures of pollutants in the aquatic environment.
- Involvement of metallothionein in Zn accumulation and elimination strategies in Ruditapes decussatusPublication . Serafim, Angela; Bebianno, Maria JoãoThe aim of this study was to identify the involvement of metallothionein (MT) in Zn accumulation and elimination strategies in different tissues (gills, digestive gland, and remaining tissues) of Ruditapes decussatus. Clams were exposed to two Zn concentrations (100 and 1000 microg/L) for 40 days, followed by a depuration period of 50 days. The accumulation and elimination processes were complemented by subcellular Zn distribution, to determine the affinity of this element for the different cellular partitions. Subsequently, the involvement of MT was followed. Zinc concentrations in the tissues of R. decussatus exposed to 100 microg/L was partially regulated, whereas in those exposed to 1000 microg/L, Zn was accumulated (exponentially and linearly) throughout the exposure period. The greatest amount of Zn is associated to the insoluble fraction; however, in the highest Zn exposure, approximately 30% is in the thermostable fraction, where MT occurs. Gel filtration chromatography confirmed that the Zn ions accumulated in this fraction were bound to MT. This protein is actively involved in the elimination of this metal, through the rapid degradation of the Zn-MT complex because MT and Zn are turning over simultaneously. Therefore, MT participates in Zn homeostasis in R. decussatus when Zn exposure is low. When Zn accumulation increases, the role of this protein changes from a constitutive function to the detoxification of the excess of Zn ions.
- Antioxidant systems and lipid peroxidation in from Mid-Atlantic Ridge hydrothermal vent fieldsPublication . Bebianno, Maria João; Company, Rui; Serafim, Angela; Camus, L.; Cosson, R.; Fialamedoni, A.Enzymatic defenses involved in protection from oxygen radical damage were determined in gills and mantle of Bathymodiolus azoricus collected from three contrasting Mid-Atlantic Ridge (MAR) hydrothermal vent fields (Menez-Gwen, Lucky Strike and Rainbow). The activities of superoxide dismutase (SOD), catalase (CAT), glutathione peroxidases (GPx) (total and Se-dependent), and levels of total oxyradical scavenging capacity (TOSC), metallothioneins (MT) and lipid peroxidation (LPO) were determined in B. azoricus tissues and the impact of metal concentrations on these antioxidant systems and lipid peroxidation assessed. SOD, CAT, TOSC, MTs and LPO levels were higher in B. azoricus gills while glutathione peroxidases (total and Se-dependent) were higher in the mantle, and with the exception of CAT, were of the same order of magnitude as in other molluscs. TOSC levels from Menez-Gwen indicate that the vent environment at this site is less stressful and the formation of ROS in mussels is effectively counteracted by the antioxidant defense system. TOSC depletion indicates an elevated ROS production in molluscs at the other two vent sites. Cytosolic SOD, GPx and LPO were more relevant at Lucky Strike (Bairro Alto) where levels of essential (Cu and Zn) and toxic metals (Cd and Ag) were highest in the organisms. CAT activity and LPO were predominant at the Rainbow vent site, where an excess of Fe in mussel tissues and in vent fluids (the highest of all three vent sites) may have contributed to increased LPO. Therefore, three distinct pathways for antioxidant enzyme systems and LPO based on environmental metal speciation of MAR vent fields are proposed for Bathymodiolus gills. At Menez-Gwen, TOSC towards peroxyl and hydroxyl radicals and peroxynitrite are predominant, while at Lucky Strike cytosolic SOD activity and GPx are the main antioxidant mechanisms. Finally at Rainbow, catalase and lipid peroxidation are dominant, suggesting that resistance of mussels to metal toxicity at these vent fields decreases in the sequence Menez-Gwen > Lucky Strike and Rainbow.
- Antioxidant biochemical responses to long-term copper exposure in Bathymodiolus azoricus from Menez-Gwen hydrothermal ventPublication . Company, Rui; Serafim, Angela; Cosson, Richard P.; Fiala-Médioni, Aline; Camus, Lionel; Colaço, Ana; Serrão-Santos, Ricardo; Bebianno, Maria JoãoCopper (Cu) is essential to various physiological processes in marine organisms. However, at high concentrations this redox-active transition metal may enhance the formation of reactive oxygen species (ROS) and subsequently initiate oxidative damage. High concentrations of Cu may increase oxidative damage to lipids, proteins and DNA. Bathymodiolus azoricus is a Mytilid bivalve very common in hydrothermal environments near the Azores Triple Junction continuously exposed to high metal concentrations, including Cu, emanating from the vent fluids. The knowledge of antioxidant defence system and other stress related biomarkers in these organisms is still scarce. The aim of this work was to study the effect of Cu (25 microg l(-1); 24 days exposure; 6 days depuration) on the antioxidant stress biomarkers in the gills and mantle of B. azoricus. The expression of stress related biomarkers was tissue-dependent and results suggest that other factors than metal exposure may influence stress biomarkers, since little variation in antioxidant enzymes activities, MT concentrations, LPO and total oxyradical scavenging capacity (TOSC) occurred in both control and Cu-exposed mussels. Moreover, there is a general tendency for these parameters to increase with time, in both control and Cu-exposed mussels, suggesting that reactive oxygen species (ROS) formation is not metal dependent, and may be related with poor physiological conditions of the animals after long periods in adverse conditions compared to those in hydrothermal environments.