Oxidative effects of the harmful algal blooms on primary organisms of the food web
Degraded water quality from nutrient pollution, physical, biological, and other chemical factors contributes to the development and persistence of many harmful algal blooms (Habs) the complex dynamics of the Habs is a challenge to marine ecosystems for the toxic effects reported. the consequences include fish, bird, and mammal mortality, respiratory or digestive tract problems, memory loss, seizures, lesions and skin irritation in many organisms. This review is intended to briefly summarize the recent reported information on harmful marine toxin deleterious effects over the primary organisms of the food web, namely algae, zooplankton and invertebrates. Special focus is made on oxidative stress status of cells and tissues. even though in situ field research is less controlled than laboratory studies, in which the organisms are directly exposed to the toxins under consideration, both types of approaches are required to fully understand such a complex scenario. on top of that, the contribution of the increasing water temperatures in the sea, as a consequence of the global climate change, will be addressed as a topic for further studies, to evaluate the effect on regulating algal growth, species composition, trophic structure, metabolic stress and function of aquatic ecosystems. BIOCELL 2019 43(2) 41 50 DOI: 10.32604/biocell.2019.06163 www.techscience.com Introduction In the marine environments, certain microalgae (diatoms, dinophyceae, rhodophyte, dinoflagellates) ciliates and cyanobacteria (Reguera, 2002) species synthetize toxins, among other compounds. These elements are available to other organisms (from plankton to humans) directly from the water or through the trophic transfer, and their cellular metabolism could be altered. These effects could be severe when a high bloom is accomplished in events call harmful algal blooms (HABs) The complex scenario of HABs dynamics is a challenge for the analyses of their toxic effects in situ over marine ecosystems. Heisler et al. (2008) summarized the principal features of HABs appearance and promotion stating that: i) increased nutrient pollution promotes the development, persistence and expansion of many HABs; ii) the nutrient pool composition impacts HABs; iii) the availability of exogenous nutrients is required to maintain high biomass blooms, and iv) HAB progress is promoted by either chronic or episodic changes of nutrient distribution. However, degraded water quality from nutrient pollution is not the only factor implicated in HABs. Physical, biological, and other chemical factors also contribute to Address correspondence to: Susana Puntarulo, susanap@ffyb.uba.ar the growth and persistence of many HABs (Sellner et al. 2003; Vadstein et al. 2004) Moreover, actual changes in environmental conditions, mainly by anthropogenic causes, could potentially lead to yet larger toxic events increasing global occurrence of HAB. The growing human population associated to nutrient pollution promotes variations in coastal nutrient loads from lands runoff (Seitzinger et al. 2010; Bergamaschi et al. 2012) Environmental modifications may also be due to altered abiotic parameters or physical dynamics, such as warmer ocean water sand stratification that are caused by climatic changes (Glibert et al. 2011; Wells et al. 2015) In this regard, the microalgae community was reported to be changed when they were exposed in situ to higher temperatures. Hernando et al. (2015) Li et al. (2009) observed that the proportion of small phytoplankton cells increased while larger ones decreased under meltwater conditions and episodic inputs of large river runoff, either in Antarctic or Arctic waters, respectively. Since temperature, oxygen (O2) consumption, availability of food, endogenous rhythms and HABs fluctuate seasonally, these factors might be potential stressors for aquatic organisms. The most severe consequences of HAB include effects on fish, bird, and mammal mortalities, respiratory or digestive tract problems, memory loss, seizures, lesions and skin irritation (Sellner et al. 2003) This review is intended to briefly summarize the recent published information on harmful marine toxin deleterious effects over the primary organisms of the food 42 Joaquin Cabrera et al. web, such as algae, zooplankton and larger invertebrates. Special focus will be made on oxidative stress status on cells and tissues. Even though in situ field research is less controlled than laboratory studies in which the organisms are directly exposed to the toxins under consideration, both types of approaches are required to fully understand such a complex scenario. Fig. 1 was designed to connect the interaction between the external factors (biotic and abiotic) that regulate the HAB, and the objective of this work in terms of analyzing the effect of the marine toxins on oxidative metabolism in marine organisms. Briefly Overview on Oxidative Metabolism Molecular O2, that represents 21% of the composition of the atmosphere, is essential to life, but it is also toxic because reactive O2 species (ROS) are constantly formed as respiration by products and by other pathways. Even more, ROS formation is a well established event in aerobic cells. The term ROS include free radicals, such as superoxide anion (O2 and hydroxyl radical (OH) and non radical reactive species such as hydrogen peroxide (H2O2) and singlet O2 O2) (Boveris, 1998) When O2 accepts one electron (e the primary product is O2 The reception of the second e leads to the formation of H2O2, and with the incorporation of another e the molecule decomposes to generate OH. The subcellular structures such as, the mitochondria, the endoplasmic reticulum, the peroxisomes, the plasma membrane, and several enzyme activities are responsible for ROS generation by partial reduction of O2 (Robello et al. 2016) Nevertheless, as nature has been exposed to ROS for two billion years, selected mechanisms have been developed to allow biological systems, not only to live but also to use them, in multiple functions. Thus, ROS toxicity depends on their steady state concentration and the cellular scenario in which they are produced (Nunn, 1985) To be able to regulate hazardous reactive species at low steady state concentrations, the presence of an antioxidant system and radicals scavenging biochemical reactions are required. The antioxidants might be enzymatic (e.g. catalase, CAT; superoxide dismutase, SOD; glutathione S transferase, GST; glutathione peroxidase, GPx; etc. or non enzymatic, such as hydrophilic (e.g. ascorbic acid, AH) and lipophilic (e.g. a tocopherol, a T) compounds. On the other hand, nitrogen (N2) represents 79% of the composition of atmospheric air. The radical nitric oxide (NO) is formed when N2 combines with O2 and the a NO reacts with the O2 producing peroxynitrite (ONOO) a radical potencially more oxidative than the first one. Reactive N2 species (RNS) as well, could lead to cellular damage by nitration, nitrosylation and finally to lipid peroxidation (Robello et al. 2016) Thus, ROS and RNS were known for decades to play important roles in mediating cytotoxicity through alterations in protein, lipid, and nucleic acid structure and function with resultant disruption of cellular homeostatic mechanisms. These noxious consequences are often due to markedly elevated (orders of magnitude) steady state concentrations or rates of production of reactive species. In addition, recently it has become apparent that more subtle changes in rates of production of reactive species may critically impact cellular homeostasis and may serve physiological roles in initiating signaling cascades. Fig. 2 shows the actual understanding of the role of the magnitude of the steady state concentration of ROS and RNS in relation to cellular damage/protection status in marine organisms. Detection of ROS and RNS in biological systems is often problematic. Sensitive, specific, and reliable methods to detect changes in reactive species are essential to the understanding of the roles of these substances. Low intracellular steadystate concentrations of these species occur as a result of the balance between the basal rates of generation, scavenging, and the extracellular release of small proportions of the intracellularly formed molecules. However, oxidative stress ratios (damage/protection) such as ascorbyl radical (A) AH content and lipid radical (LR)/a T content were proved to provide a useful tool for stress diagnosis (Puntarulo et al. 2004; Gonzalez et al. 2013) The possibility of marine toxins to induce toxicological effects through an oxidative and/ or a nitrosative pathway was assessed for several researches worldwide at different taxonomic levels. FIGURE 1. Schematic synopsis of the aspects to be analyzed on the light of the main biotic and abiotic factors which promote HAB subsequently af fect ing oxidative metabolism in marine organisms. OxIDATIVE EFFECTS OF THE HARMFuL ALGAL BLOOMS ON PRIMARy ORGANISMS 43 Oxidative Stress Generation in Algae by Exposure to Marine Biotoxins Even though physiological and ecological roles for some marine toxins produced during HAB were postulated, the matter has not yet been fully elucidated. Dring (2006) suggested that instant responses of marine plants to adverse environmental conditions involve excess production of ROS. Phytoplankton is the most significant primary producer (50% of global primary production; Falkowski and Raven, 2007) in the ocean sustaining the pelagic food chains in the aquatic ecosystems. Phytoplankton is also responsible for the substantial sink for CO2 in marine ecosystems. Then, if these organisms are adversely affected, then the surrounding ecosystem may also feel the effects, either directly or indirectly, from the lack of a food source (Wang and Zheng, 2008) The oxidative stress and damage induced by saxitoxin (STx) in the green phytoplankton alga Chlamydomonas reinhardtii was reported by