Bioluminescence, the emission of ecologically functional light by living organisms, emerged independently on several occasions, yet the evolutionary origins of most bioluminescent systems remain obscure. We propose that the luminescent substrates of the luminous reactions (luciferins) are the evolutionary core of most systems, while luciferases, the enzymes catalysing the photogenic oxidation of the luciferin, serve to optimise the expression of the endogenous chemiluminescent properties of the luciferin. Coelenterazine, a luciferin occurring in many marine bioluminescent groups, has strong antioxidative properties as it is highly reactive with reactive oxygen species such as the superoxide anion or peroxides. We suggest that the primary function of coelenterazine was originally the detoxification of the deleterious oxygen derivatives. The functional shift from its antioxidative to its light-emitting function might have occurred when the strength of selection for antioxidative defence mechanisms decreased. This might have been made possible when marine organisms began colonising deeper layers of the oceans, where exposure to oxidative stress is considerably reduced because of reduced light irradiance and lower oxygen levels. A reduction in metabolic activity with increasing depth would also have decreased the endogenous production of reactive oxygen species. Therefore, in these organisms, mechanisms for harnessing the chemiluminescence of coelenterazine in specialised organs could have developed, while the beneficial antioxidative properties were maintained in other tissues. The full range of graded irradiance in the mesopelagic zone, where the majority of organisms are bioluminescent, would have provided a continuum for the selection and improvement of proto-bioluminescence. Although the requirement for oxygen or reactive oxygen species observed in bioluminescent systems reflects the high energy required to produce visible light, it may suggest that oxygen-detoxifying mechanisms provided excellent foundations for the emergence of many bioluminescent systems.
Oxygen, while being an obligate fuel for aerobic life, has been shown to be toxic through its deleterious reactive species, which can cause oxidative stress and lead ultimately to cell and organism death. In marine organisms, reactive oxygen species (ROS), such as the superoxide anion and hydrogen peroxide, are generated within respiring cells and tissues and also by photochemical processes in sea water. Considering both the reduced metabolic rate of nektonic organisms thriving in the deep sea and the physico-chemical conditions of this dark, poorly oxygenated environment, the meso- and bathypelagic waters of the oceans might be considered as refuges against oxidative dangers. This hypothesis prompted us to investigate the activities of the three essential enzymes (superoxide dismutase, SOD; catalase, CAT; glutathione peroxidase, GPX) constitutive of the antioxidative arsenal of cells in the tissues of 16 species of meso- and bathypelagic fishes occurring between the surface and a depth of 1300 m. While enzymatic activities were detected in all tissues from all species, the levels of SOD and GPX decreased in parallel with the exponential reduction in the metabolic activity as estimated by citrate synthase activity. In contrast, CAT was affected neither by the metabolic activity nor by the depth of occurrence of the fishes. High levels of metabolic and antioxidative enzymes were detected in the light organs of bioluminescent species. The adjustment of the activity of SOD and GPX to the decreased metabolic activity associated with deep-sea living suggests that these antioxidative defense mechanisms are used primarily against metabolically produced ROS, whereas the maintenance of CAT activity throughout all depths could be indicative of another role. The possible reasons for the occurrence of such a reduced antioxidative arsenal in deep-sea species are discussed.
Oceans function as a sink for organochlorine compounds (OCs) such as PCBs and DDTs. Deep-sea fish bioaccumulate OCs to levels 10 to 100 times higher than shallow-water species. OCs induce the cytochrome P450 (CYP) system, the activity of which may increase reactive oxygen species (ROS) production in liver cells. However, the susceptibility of fish to the oxidative stress likely caused by OCs remains unclear. We analysed whether PCB and DDT contamination of roundnose grenadier Coryphaenoides rupestris was associated with higher ethoxyresorufin-O-deethylase (EROD) activity (CYP1A-related), and activities of antioxidant enzymes such as catalase (CAT), superoxide dismutases (SOD) and glutathione peroxidases (GPX). Biological parameters affecting EROD patterns (e.g. gender, ontogeny) were also investigated. Citrate synthase (CS) was used as a proxy for oxidative metabolism, responsible for basal ROS production and recruitment of antioxidant enzymes in liver cells. Hepatic OC levels were determined in individuals of different sizes (89 to 2016 g) from northern Atlantic slopes (depth range = 1000 to 1900 m). Median PCB and DDT values were 2.39 and 1.48 µg g -1 lipid weight, respectively, while median EROD activity was 15 pmol min -1 mg -1 protein. Gender greatly influenced OC levels (females were less contaminated), whilst weight (linked to ontogeny) positively affected DDT levels. EROD increased with PCB levels, and to some extent SOD and CAT were more influenced by EROD than CS, indicating that PCBs strongly affect the redox balance of roundnose grenadier liver cells through increased CYP1A activity. Therefore, OC-related CYP1A induction may be a major source of cellular ROS in liver of roundnose grenadier.
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