Contaminant-stimulated Reactive Oxygen Species Production and Oxidative Damage in Aquatic Organisms
Introduction
An increasing variety of industrial, agricultural and other chemicals is entering the aquatic environment and being taken up into the tissues of invertebrates and vertebrates (Walker and Livingstone, 1992, Porte and Albaigés, 1993, Khan et al., 1995, Van der Oost et al., 1996, Walsh and O'Halloran, 1998, Stecko and Bendell-Young, 2000, Solé et al., 2000). The contaminants comprise chemicals of both long standing and more recent concern, including polynuclear aromatic hydrocarbons (PAHs) (Varanasi, 1989, Baumard et al., 1998); organochlorine pesticides (DDT, dieldrin) and industrial products (chlorophenols, polychlorobiphenyls (PCBs), hexachlorohexanes, hexachlorobenzenes) (Walker and Livingstone, 1992); polychlorinated dibenzo-p-dioxins and dibenzofurans (Cooper, 1989); nitroaromatic and other heterocyclic compounds (Balch et al., 1995, Hetherington et al., 1996); organometallic compounds (Fent, 1996); organophosphate fertilizers (Van der Oost et al., 1996); estrogenic compounds such as alkylphenol ethoxylate surfactants (Routledge and Sumpter, 1996); and many metals including cadmium (Cd), chromium (Cr), copper (Cu), iron (Fe), mercury (Hg), zinc (Zn), lead and silver (Livingstone and Pipe, 1992, Walsh and O'Halloran, 1998). The uptake of these contaminants can occur from sediments, suspended particulate material, water-column and food-sources; and the major routes of input will depend on the particular dietary and ecological lifestyles of the organisms (Van Veld, 1990, Livingstone, 1991, Livingstone, 1998). Such a diverse array of chemicals can have many different mechanisms of toxicity, and several mechanisms may exist for a single contaminant, each contributing to various degrees to the final overall deleterious effect (Livingstone, 1991, Rand, 1995, Walker et al., 1996, Livingstone et al., 2000a).
Since the discovery of the importance of radical reactions in normal biological processes, and in the mechanisms of toxicity of many foreign compounds (xenobiotics), there has been an explosion of research into pro-oxidant and antioxidant processes, principally in mammalian systems (Kehrer, 1993, Halliwell and Gutteridge, 1999). Of more recent interest has been evidence to indicate that contaminant-stimulated `reactive oxygen species' (ROS) production and resulting oxidative damage may be a mechanism of toxicity in aquatic organisms exposed to pollution (for reviews see Di Giulio et al., 1989, Livingstone, 1991, Livingstone et al., 1990, Livingstone et al., 1994, Winston and Di Giulio, 1991, Lemaire and Livingstone, 1993, Di Giulio et al., 1995). The main aims of this short review are to briefly summarize current knowledge and recent advances in the understanding of such processes in aquatic organisms, and to assess these findings in relation to the key question of whether contaminant-stimulated ROS production and oxidative damage pose a threat to animal health and fitness in the aquatic environment.
Section snippets
Origin, Types and Sources of ROS
The normal fate of most of the molecular oxygen consumed by animals is tetravalent reduction to water coupled to the oxidation of food and the production of energy. Partial reduction results in the formation of what have been variously collectively termed as ROS, `oxygen-derived species', oxyradicals, or other descriptors, and comprise both radical and non-radical species. The former include superoxide anion radical (O2−), hydroxyl radical (OH), peroxyl radical RO2), alkoxyl radical (RO) and
ROS Production in Aquatic Organisms – in vitro Studies
Using subcellular fractions, studies have focussed on both endogenous (Winston et al., 1990, Lemaire et al., 1993) and contaminant-stimulated ROS production. Measurements have principally been of NAD(P)H-dependent iron/EDTA-mediated ROS production (detected as oxidation of the scavenging agent 2-keto-4-methiolbutyric acid (KMBA) by OH to yield ethylene; this is a measure of the sum of O2− and H2O2, both of which are converted to OH by Fe/EDTA, and directly produced OH), but also of
ROS Production in Aquatic Organisms – Laboratory and Field in vivo Studies
Very few studies have directly addressed the question of the production of ROS in vivo, either in the absence or presence of xenobiotics, in aquatic organisms, mainly because of the technical difficulties of such measurements. Enhanced OH production (measured as the oxidation of dimethylsulphoxide (to which the animals were exposed in the water-column) to methane sulphinic acid) was seen in the cnidarian Anthopleura elegantissima and its endosymbiotic zooxanthellae algae (Dykens et al., 1992).
Antioxidant Defences
ROS produced in biological systems are detoxified and purportedly held in check by antioxidant defences, which are generally ubiquitous in animal species and different tissue-types. They are found widely in aquatic organisms and their presence, properties and other characteristics have been extensively reviewed (Livingstone, 1991, Winston and Di Giulio, 1991, Lemaire and Livingstone, 1993, Di Giulio et al., 1995). The antioxidant systems principally examined to date in aquatic organisms
Oxidative Damage – Laboratory and Field Studies
In the normal situation, the production of ROS and other reactive species is thought to be held in check by antioxidant defence systems, i.e. a balance exists between pro-oxidant and antioxidant processes. However, the balance is not perfect such that some oxidative damage to key molecules like DNA, protein and lipid occurs continuously, necessitating their repair or replacement (Halliwell and Gutteridge, 1999). In the aquatic situation, it is postulated that despite the presence of basal or
Oxidative Stress, Disease and Animal Fitness
Although the terms are not rigourously defined, even in the mammalian literature, increased oxidative damage leads to a condition known as oxidative stress. The latter has been described as `in essence a serious imbalance between production of ROS/RNS and antioxidant defence' (Halliwell and Gutteridge, 1999), and `a disturbance in the prooxidant– antioxidant balance in favour of the former, leading to potential damage' (Sies, 1991). The condition of oxidative stress can arise through a
Conclusions and Unknowns
Major reasons for studying pro-oxidant and other radical processes in humans are the understanding and treatment of disease, and the understanding of the action of toxins (Halliwell and Gutteridge, 1999). Similar considerations may apply to aquatic organisms, but it is the latter that is of most relevance, particularly in the context of environmental management. Specifically, knowledge of normal and contaminant-related pro-oxidant and antioxidant processes in aquatic animals is needed for: (i)
Acknowledgements
The paper was presented as part of a workshop on marine pollution organized by Professor J.O. Grimalt from CSIC, Barcelona and held during 29 September–1 October 1999 Barcelona, Spain. The author gratefully acknowledges the invitation to participate and the funding provided by the organizers of the workshop.
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