Bioaccumulation of persistent organic pollutants (POPs) and biomarkers of pollution in Mediterranean deep-sea organisms / Bioacumulación de contaminantes orgánicos persistentes (COPs) y biomarcadores en organismos del mar Mediterráneo profundo

Abstract

[eng] The deep-sea has long been considered the last region one Earth to be untouched from anthropogenic disturbances. However, studies have shown that the deep-sea is not as pristine as once assumed and it has been suggested that it may actually act as a sink for persistent organic pollutants (POPs). POPs are ubiquitous in the environment and of particular concern due to their high persistence, toxicity, bioaccumulation potential and long-range transport. Although POPs have been detected in a range of deep-sea organisms from around the world, little is known on the potential impact anthropogenic contamination may have on deep-sea ecosystems. Thus, the present thesis aimed to investigate the bioaccumulation of POPs and potential adverse effects in deep-sea organisms resulting from exposure to these contaminants. To this end, a range of different contaminants, including legacy (e.g. polychlorinated biphenyls [PCBs], dichlorodiphenyltrichloroethane [DDTs], hexachlorocyclohexanes [HCHs]) and emergent (e.g. polybrominated diphenyl ethers [PBDEs]) POPs, as well as other contaminant classes such as polycyclic aromatic hydrocarbons (PAHs), alkylphenols (APs) and mercury (Hg) were determined in different Mediterranean deep-sea organisms. Results showed that Mediterranean deep-sea organisms are potentially exposed to a wide range of contaminants, some of them potentially causing a risk for the deep-sea ecosystem as well as for human health. In this context, the present work presents one of the few studies and the first in the Mediterranean to simultaneously determine the bioaccumulation of legacy POPs and emergent PBDEs in deep-sea organisms. Moreover, the presence of APs in deep-sea fauna has not been previously investigated and this thesis thus provides novel information on the presence of these contaminants in remote marine environment. Also, Hg contamination could be of particular concern for deep-sea environments as levels appeared to increase with increasing habitat depth of the analyzed species. Furthermore, almost all species, including the commercially exploited fish Mora moro and the highly valuable red shrimp Aristeus antennatus, exhibited Hg levels exceeding the recommended consumption value of 0.5 μg/g wet weight and thus potentially pose a risk for human health.

In addition to chemical analyses, biomarkers of pollution including enzymatic activities and gene expression profiles were used to determine the potential negative effects contaminant exposure may have on deep-sea biota. The biomarkers applied include enzymes involved in the xenobiotic metabolism such as the cytochrome P450 enzymes (CYPs), carboxylesterase (CbE) and glutathione-S-transferase (GST) as well as antioxidant responses such as catalase (CAT), glutathione peroxidase (GPX), glutathione reductase (GR) and superoxide dismutase (SOD). The present work has shown that despite the lack of seasonal fluctuations of abiotic factors such as temperature and salinity in the Mediterranean deep-sea, organisms exhibit significant seasonal variability in enzymatic responses related to reproductive processes and food availability. Additional findings of the present work include the differential accumulation of POPs among fish species and compared to the crustacean Aristeus antennatus. Apart from factors such as habitat and feeding strategies, results indicated that differential CYP-mediated xenobiotic metabolism capacities between fish and crustacea may influence the variations in bioaccumulation patterns of POPs such as PCBs. Furthermore, novel biomarkers such as the gene expression of vitellogenin as indicator of endocrine disruption in male fish was applied for the first time to a deep-sea fish species, namely Alepocephalus rostratus. Furthermore, a major objective of this work was to investigate the particular case of submarine canyons, which are thought to act as natural conduits for particles and associated contaminants from surface waters to the deep ocean. In this sense, the present study showed that deep-sea organisms dwelling within the head of Blanes canyon, NW Mediterranean, might be particularly at risk from experiencing detrimental effects from exposure to anthropogenic pollutants.

[spa] Durante mucho tiempo, el mar profundo se consideraba como el único medio exento de impacto antropogénico. Sin embargo, en las últimas décadas varios estudios han demostrado que el mar profundo no es tan prístino como se había pensado y que podría de hecho actuar como sumidero para contaminantes persistentes. Esta tesis tiene como objetivo de estudiar la bioacumulación de contaminantes orgánicos persistentes (COPs) en organismos del mar Mediterráneo profundo y los posibles efectos adversos que les pueden ocasionar. Con este fin, se determinaron los niveles de COPs legados como los bifenilos policlorados (PCBs), diclodifeniltricloroetano (DDTs), hexaclorociclohexanos (HCHs), y el penta- y hexaclorobenzeno (PeCB, HCB) y también de COPs emergentes como los polibromodifenil éteres (PBDEs). Además, se analizaron otros tipos de contaminantes como el mercurio (Hg) en musculatura y los metabolitos de hidrocarburos aromáticos policíclicos (PAHs) y alquilfenoles (APs) en bilis. Los posibles efectos negativos asociados con la exposición a estos contaminantes se determinaron mediante biomarcadores enzimáticos y de expresión génica, incluyendo enzimas de citocromo P450 (CYPs), glutatión-S-transferasa (GST), carboxilesterasa (CbE), glutatión peroxidasa (GPX), glutatión reductasa (GR) y catalasa (CAT). Los resultados obtenidos indicaron que los organismos de las zonas profundas del Mediterráneo están potencialmente expuestos a múltiples tipos de contaminantes de los cuales algunos pueden causar efectos adversos. En este contexto, este estudio es el primero en investigar los niveles de COPs legados y los emergentes PBDEs en organismos de gran profundidad del Mediterráneo. Además, se analizó por primera vez la presencia de metabolitos de APs en una especie abisal aportando información relevante respeto a la presencia y destino de estos contaminantes en el medio marino. Un objetivo importante de esta tesis consistía en investigar la contaminación del cañón de Blanes, ya que los cañones submarinos podrían actuar como vía de transporte preferencial de contaminantes asociados a partículas debido a su proximidad de la costa y su estructura geomorfológica. En este sentido, los resultados sugirieron que los organismos que habitan la zona de la cabecera del cañón de Blanes presentan un riesgo mayor de sufrir efectos adversos asociados a la exposición a COPs.