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- Stress-physiological reactions of the green alga Scenedesmus opoliensis to water pollution with herbicides

Even micromolar concentrations of herbicides that enter the aquatic ecosystems from surrounding agricultural fields, exert specific actions on physiological processes of algae and trigger easily detectable antistress reactions that may be useful in an early detection of effects of environmental pollution on living organisms. For example, herbicides that induce oxidative damage of membranes cause a significant increase in lipid peroxidation. This is the reason why methylviologen, a compound which in illuminated algal cells deturns energized electrons from photosystem I during the light phase of photosynthesis, enhances the formation of superoxide radicals and of hydrogen peroxide, two dangerous reactive oxygen species that damage the membrane structures of different cell compartments. As a consequence of this oxidative stress, toxic products of lipid peroxidation (thiobarbituric acid reactive substances) accumulate in the algal cells exposed to methylviologen. Glufosinate, a herbicide known to inhibit glutamine synthase and to induce overaccumulation of ammonia, also induces formation of some reactive oxygen species (most probably of hydrogen peroxide related to disturbance of photorespiration), and this may explain the enhancement of lipid peroxidation caused by this herbicide in the alga Scenedesmus opoliensis. Oxidative damage caused by methylviologen in plants is relatively well documented [5, 20], but as far as we know, there are no data about the influence of glufosinate on membrane lipid peroxidation. Our results show that diuron does not interfere with membrane lipids and does not generate reactive oxygen species that would increase the formation of malondialdehyde and related toxic compounds. Instead, this herbicide that is known to inhibit electron transport on the acceptor side of photosystem II in the illuminated chloroplasts, reduces drastically the oxygen production of algae, probably because the disturbance in the function of photosystem II implies a disfunction of the water-splitting complex associated with its lumenal donor side, where the oxygen molecules are evolved from [7, 14]. Impairment of photochemical reactions by diuron results in an overall deficit in the energetic balance of the algal cells, related to the lower biomass production and decreased cell division rate registered in the algal populations exposed to this herbicide. Other algae were also found to react to the presence of herbicides in water by reducing growth and reproduction rate, and a change of chemical composition of their biomass was also reported [13, 19, 24, 29].

Whenever oxidative stress occurs by generation of reactive oxygen species under adverse environmental conditions, a crucial component of tolerance is the induction of an efficient antioxidative protection system with both enzymatic and non-enzymatic components. Many external stress factors cause the formation and accumulation of reactive oxygen species (singlet oxygen, superoxide radical, hydrogen-peroxide and hydroxyl radical), triggering the synthesis of reducing compound (mainly ascorbate, tocopherol, glutathione and specific xanthophylls), and the enhancement of catalytic activity of antioxidative enzymes (such as catalase, ascorbate peroxidase, superoxide dismutase, peroxiredoxins, glutathione reductase etc.). 10 μM methylviologen increased the amount of ascorbate and decreased the catalase activity in the alga Scenedesmus opoliensis. These results indicate that the algal cells react by accumulation of the protective molecules of ascorbate in order to counteract the oxidative stress imposed by this herbicide, but the synthesis and/or the activity of catalase is inhibited by methylviologen, in consequence the enzyme cannot perform an efficient scavenging of the accumulated hydrogen peroxide. This reduced enzymatic protection is partly compensated by the higher amount of ascorbic acid, which is also involved in decomposition of hydrogen peroxide through the Halliwell-Asada-Foyer redox chain, with participation of glutathione reductase and ascorbate peroxidase [14, 20]. Similar antioxidative responses were reported for green algae exposed to water pollution with chromium ions, and significant differences between tolerant and sensitive algae could be established concerning changes in the antioxidative protective components [15]. In contrast with methylviologen, glufosinate triggered a different antistress reponse, without any significant increase in the ascorbate content of the algal cells, but with an obvious enhancement of catalase activity. In the case of this herbicide, the enzymatic component of antioxidative system seems to play a more important protective role than the non-enzymatic one. This may be considered another new finding of our experiments, suggesting that more components of the antioxidative system have to be investigated in order to get a more accurate image of how the same organism reacts to similar oxidative stress situations imposed by different chemical pollutants.

Considering the influence of herbicides on growth and reproduction of the alga Scenedesmus opoliensis, one can observe that methylviologen exerted the strongest inhibitory effect both on cell division rate and on dry biomass production. Glufosinate had the mildest influence on these parameters, indicating that this is the mostly tolerated herbicide among the three types used in the experiments. Growth of both cell number and cell size was significantly impaired by the long-term exposure of the algal populations to 10 μM of herbicides, indicating that mainly all the physiological processes that ensure survival of individuals and of the species are endangered by the presence of these organic pollutants in the aquatic habitats.

The rate of net photosynthetic oxygen production is also a good functional indicator of algal condition in the presence of herbicides, and it is a suitable parameter for distinguishing between the actions of different herbicides. The net oxygen production of algae in the presence of a constant photon flux density is the result of photosynthetic water-splitting process in the thylakoids, of chlororespiratory oxygen consumption in the chloroplasts, of photorespiratory oxygen consumption in the chloroplast stroma and in the peroxisomes, and of the oxygen demand of mitochondrial respiration, the latter being very reduced due to the Kok-effect in the photosynthesizing algal cells [8, 16, 21]. Different herbicides may interact directly or indirectly with all of these processes involved in the overall oxygen budget of the algal cells. Diuron decreases oxygen production mainly by inhibiting water-splitting related to the photochemical processes in photosystem II. Methylviologen induces the consumption of extra amounts of oxygen for the generation of superoxide radicals and hydrogen peroxide, and this may be the main cause of its inhibitory effect on net oxygen release from algal cells. Glufosinate impairs the metabolic pathway of photorespiration because of disturbances in the endogenic nitrogen cycle of the algal cells. This reduces photorespiratory oxygen consumption and results in an increased net oxygen accumulation. Changes in oxygen production of algae were also observed under the influence of other polluting agents [27, 29, 31].

As a conclusion of the above presented results, one can notice that: 1. methylviologen increases lipid peroxidation in algal cells, inhibits catalase activity, induces accumulation of ascorbate, impairs cell divisions, reduces dry biomass production and lowers net oxygen production; 2. diuron inhibits photosynthetic oxygen production, growth and development of algal populations; 3. glufosinate increases catalase activity, lipid peroxidation and net oxygen production in Scenedesmus opoliensis, but it moderately reduces cell density and biomass production.

High amounts of products of lipid peroxidation and of ascorbate are sensitive molecular indicators of oxidative stress conditions imposed by the presence of methylviologen in the aquatic environment, and these parameters may be suitable for detection of various pollutants that generate reactive oxygen species in algae. Net oxygen production, dry biomass accumulation and the rate of cell divisions are efficient functional indicators of the presence of all the three herbicides used in these experiments to study reactions of the alga to water pollution with organic xenobiotics. The green alga Scenedesmus opoliensis proves to be a promising test organism for bioindication of the effects of environmental stress factors on aquatic ecosystems. Studies on the impact of chemicals on aquatic organisms involve standardized single-species test systems evaluated under controlled laboratory conditions, but in order to achieve a more realistic knowledge of what happens in the complex natural ecosystems, these studies have to be continued with field experiments which take into account multilevel interactions among abiotic and biotic environmental factors [5, 15, 21].

Acknowledgements. This research was supported by grant MENER PC-D06-PT25-293.

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