Toxicity Evaluation, Oxidative, and Immune Responses of Mercury on Nile Tilapia: Modulatory Role of Dietary Nannochloropsis oculata

Biological Trace Element Research https://doi.org/10.1007/s12011-023-03771-4 RESEARCH Toxicity Evaluation, Oxidative, and Immune Responses of Mercury on Nile Tilapia: Modulatory Role of Dietary Nannochloropsis oculata Eman Zahran1 · Fatma Ahmed2 Mahmoud G. El Sebaei7,8 · Zeinab Hassan3 · Iman Ibrahim4 · Asmaa A. Khaled5 · Dušan Palić6 · Received: 18 April 2023 / Accepted: 9 July 2023 © The Author(s) 2023 Abstract The current study evaluated the potential ameliorative effect of a dietary immune modulator, Nannochloropsis oculata microalga, on the mercuric chloride (HgCl2)-induced toxicity of Nile tilapia. Nile tilapia (45–50 g) were fed a control diet or exposed to ¼ LC50 of H gCl2 (0.3 mg/L) and fed on a medicated feed supplemented with N. oculata (5% and 10% (50 or 100 g/kg dry feed)) for 21 days. Growth and somatic indices, Hg2+ bioaccumulation in muscles, and serum acetylcholinesterase (AChE) activity were investigated. Antioxidant and stress-related gene expression analyses were carried out in gills and intestines. Histopathological examinations of gills and intestines were performed to monitor the traits associated with Hg2+ toxicity or refer to detoxification. H g2+ toxicity led to significant musculature bioaccumulation, inhibited AChE activity, downregulated genes related to antioxidants and stress, and elicited histopathological changes in the gills and intestine. Supplementation with N. oculata at 10% was able to upregulate the anti-oxidative-related genes while downregulated the stress apoptotic genes in gills and intestines compared to the unexposed group. In addition, minor to no histopathological traits were detected in the gills and intestines of the N. oculata-supplemented diets. Our data showed the benefit of dietary N. oculata in suppressing Hg2+ toxicity, which might support its efficacy as therapeutic/preventive agent to overcome environmental heavy metal pollution in aquatic habitats. Keywords Acetylcholinesterase activity · Environmental pollutants · Mercury toxication · Microalgae · Oreochromis niloticus Introduction Fish environmental diseases are caused by numerous ecological contaminants, including heavy metals [1]. Aquatic contamination by heavy metals might happen from atmospheric deposition or industrial activities; therefore, their bioaccumulation was frequently reported in different aquatic * Eman Zahran 1 Department of Aquatic Animal Medicine, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt 2 Department of Zoology, Faculty of Science, Sohag University, Sohag 82524, Egypt 3 Fish Disease Department, Faculty of Veterinary Medicine, Aswan University, Aswan 81528, Egypt 4 Pathology Department, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt ecosystems worldwide [2–4]. Several anthropogenic activities, such as fossil fuel and coal combustions or agricultural and industrial consumptions, release heavy metals causing severe contamination of the adjacent aquatic habitats. These metals are dangerous for aquatic organisms as they could persist in their environment and accumulate in their organs, negatively affecting their health, growth, meat quality, and 5 Animal and Fish Production Department, Faculty of Agriculture Saba Basha, Alexandria University, Alexandria, Egypt 6 Chair for Fish Diseases and Fisheries Biology, Ludwig-Maximilians-University Munich, Munich 80539, Germany 7 Department of Biomedical Sciences, College of Veterinary Medicine, King Faisal University, Al‑Ahsa 31982, Saudi Arabia 8 Department of Biochemistry and Molecular Biology, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt 13 Vol.:(0123456789) E. Zahran et al. reproduction and leading to death or extended harm to their offspring [5–7]. Furthermore, the damage of such elements extends to the human consumers of fish and seafood [8–10] or through agricultural product consumption [11]. Mercury (Hg) is one of the toxic heavy metals that spread out in aquatic habitats mainly from agricultural waste containing pesticides, in addition to occurring naturally in the atmosphere and could be deposited via weathering [6]. It is considered the third most dangerous environmentally heavy metal pollutant after arsenic and lead, found in the environment in three different forms elementary (Hg0), organic (methylmercury “MeHg”), and inorganic (chloride mercury “HgCl2”). Although MeHg is the most toxic form [12], HgCl2 is the most common and harmful form since it can pass across biological membranes and interact with amino acids forming organo-mercury complexes [13]. The reported Hg2+ toxicity for fish is in the form of brain oxidative stress, inhibition of hepatic biotransformation enzymes, genotoxicity in blood, and reproductive alterations [14–16]. Several factors can cause Hg2+ accumulation in fish tissues. Environmental factors such as pH of the water, dissolved organic carbon, and other biological factors including fish age, size, foraging habitat, and primary productivity can all influence bioaccumulation [6, 17]. Low primary productivity leads to high Hg2+ concentrations because of the algal bio-dilution, which increases the accumulated MeHg levels [6]. Additionally, H g2+ concentrations increased with fish size, and higher concentrations were reported in the bottom (demersal) than in the surface (pelagic) fish and concerning percent floodable area rather than the hydromorphic soils, which did not influence fish Hg level [6]. The inorganic mercury compounds suppress the antioxidant defense system in host bodies and induce apoptosis. Chelating agents are used in medicine to treat mercury toxicity by forming chelation compounds with toxic metal ions that are easily excreted through the excretory system [13]. On the other hand, natural antioxidants are preferable because drugs are ineffective at repairing tissue damage and may cause toxic side effects. Using the biological systems for mercury absorption reported augmentation of H g2+ accumulation in the aquatic organisms’ organs [18]. Several natural antioxidant products have recently been used as potential non-toxic therapies against heavy metals and microalgae toxicity. Microalgae are essential metabolites for food and medicine [19] and have gained high importance in the aquaculture industry [20] since they were frequently used as feed and food additives, in addition to being live feed in aquaculture [21]. Furthermore, surfaces of algal cells possess several kinds of functional groups responsible for heavy metals’ chelation from contaminated water [22]. Microalgae, including N. oculata, rapidly respond to changes in element availability; therefore, they can be used to evaluate contaminated areas and predict the ecological effects of pollution. 13 The current study focuses on Hg2+ toxicity because it is a ubiquitous heavy metal; MeHg and HgCl2 naturally occur in the water and cause ultimate public health problems [23]. Besides, t (...truncated)