Selenium nanoparticles enhanced thermal tolerance and maintain cellular stress protection of Pangasius hypophthalmus reared under lead and high temperature

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Highlights

  • The dietary Se-NPs enhance thermal tolerance of Pangasius hypophthalmus reared under Pb and elevated temperature.

  • The CTmin and LTmin were significantly enhanced in P. hypophthalmus fed with Se-NPs and reared under lead and temperature.

  • The CTmax and LTmax were also significantly enhanced in P. hypophthalmus fed with Se-NPs.

  • Dietary Se-NPs also protect against antioxidative and cellular metabolic stress reared under lead and temperature.

Abstract

There is strong relation between nutrition and thermal tolerance of fish in terms of improved critical temperature minima (CTmin), lethal temperature minima (LTmin), critical temperature maxima (CTmax), and lethal temperature maxima (LTmax). Fishes act as quantifying indicators of the climate change due to their critical thermal limits in nature and ability to adjust thermal sensitivity to maintain their homeostasis. In the present study, biologically synthesised selenium nanoparticles (Se-NPs) from fisheries waste (fish gill) were used to evaluate its efficacy for enhancement of thermal tolerance of Pangasius hypophthalmus reared under lead (Pb) and high temperature (34 °C) for 72 days. At the end of the experimental period, CTmin, LTmin, and CTmax, LTmax and cellular metabolic stress were evaluated. The CTmin, LTmin were noticeably (p < 0.01) reduced and CTmax, LTmax were enhanced in treatment groups fed with dietary Se-NPs. It was also observed that CTmax and LTmax were increased with acclimation temperature. The positive correlation was perceived between CTmin, LTmin (Y = −0.45 + 11.05x, R2, 0.768) and CTmax, LTmax (Y = −0.78 + 8.17x, R2, 0.858) fed with Se-NPs supplemented diet and exposed to Pb and high temperature. Significant improvements in the oxidative and metabolic enzymes were noticed post thermal tolerance experiment. Overall results indicated that incorporation of Se-NPs @ 1 mg/ kg in diet can confer protection against Pb and thermal stress in P. hypophthalmus.

Introduction

The fifth report of the IPCC revealed that, extinction of large number of organism in fresh and marine water species is mediated due to climate change, as it interacts with other stressors such as inorganic and organic contamination (IPCC, 2014). Extinction of species will be driven by several climate-associated drivers such as warming, variations in precipitation, reduced river flows, ocean acidification and lowered ocean oxygen levels and the interactions among these drivers and their interaction with simultaneous habitat modification, over-exploitation of stocks, water pollution, eutrophication and invasive species (IPCC, 2014). Rising temperature has enhanced contamination in the aquatic water bodies (Kumar et al., 2017a, Kumar et al., 2014a, Kumar et al., 2016a) resulting in reduction of the thermal tolerance of the aquatic organism especially fishes. Temperature is the key factor that can bring drastic physiological affects on living systems and may directly influence the thermal limits of the toxic substances in the aquatic biota (Olsvik et al., 2016). Therefore, it is absolutely imperative to conduct intensive research on this aspects, so that, solution would be ready for implementation at any certain time period. Fishes are poikilothermic animals hence alterations in the water temperature would have a marked serious impact on many of the key physiological processes and behavioural activities (Jonassen et al., 1999). Furthermore, change in body with rising temperature of the environment will not only affect on all the physiological and biochemical reactions but also the stability of biological molecules of fish will be affected (Hochachka and Somero, 2002). Due to high temperature and contamination, anaerobic metabolic pathways gets accelerated resulting into drastic changes on cellular and biochemical levels (Portner, 2002, Portner and Knust, 2007), impaired circulatory and ventilatory performance, mitochondrial dysfunctioning and impaired oxygen-carrying capacities that may contribute to thermally induced limitation of oxygen (Melzner et al., 2007). In addition, concurrent exposure to metal stress and elevated temperature will result in rapid onset of tissue hypoxemia and aerobic energy deficiency. Metal exposure have also deleterious effects on the metabolic physiology of ectothermic animals and it interferes with cellular process such as ion homeostasis, protein stability and mitochondrial efficiency, leading to elevated costs for maintenance and detoxification (Sokolova and Lannig, 2008).

To counteract the problems of stress such as elevated temperature and or heavy metal, nutritional approaches may offer a viable and sustainable means. In this context, application of nanoparticle based feed formulation is the key pragmatic alternative to cope up the integrative and or multiple stressors. Se is essential nutrient component and have major role as antioxidant and immune enhancer in fish (Huang et al., 2012), therefore application of selenium nanoparticle (Se-NPs) was used in this study. Se plays pivotal role in maintaining various leukocytic effector functions including adherence, migration, phagocytosis, and cytokine secretion. Se deficiency may affects normal physiological health of animal (Ewan, 1976) and in case of excess level in diet/water, the bioaccumulation of Se in various organs of animals could be harmful (Hilton et al., 1980). Nano-selenium (Se-NPs) has lesser toxicity than inorganic selenium (Forootanfar et al., 2014) and is essential for normal functioning of selenoproteins such as selenocysteine and selenomethionine (Rao et al., 2013). The selenoproteins have important role in activation, proliferation, and differentiation of cells that drive innate and adaptive immune responses and are also involved in the immunoregulation in the human and animal body (Huang et al., 2012, Kudva et al., 2015). Se acts as co-factor for glutathione peroxidase and have diverse functions in the antioxidant defense systems and is a central component of the enzyme glutathione peroxidase (Ahsan et al., 2014). The enzymatic and nonenzymatic are two categories for antioxidant defense hence, Se falls under physiological non-enzymatic antioxidant category (Cheung et al., 2004, Mruk et al., 2002, Nogueira et al., 2003). In addition to this, some nonenzymatic antioxidants are the micronutrients, which are derived directly from the diet, while others must be appropriately supplied in order to reach the necessary concentrations in the body (Talas et al., 2008).

Several researchers proved that, modulating the immune response, thorough dietary supplementation can enhance fish tolerance to thermal stress (Kumar et al., 2014a, Kumar et al., 2016a, Tejpal et al., 2014) leading to enhanced fish production. Exposure of fish to Pb and high temperature leads to alteration in antioxidative enzymes, neurotransmitter enzyme, protein and carbohydrate metabolic enzymes, lipid peroxidation, resulting in cell damage to specific organs (Casillas et al., 1983). The catalase, superoxide dismutase and glutathione-s-transferase are important component for antioxidative defence against oxidative damage, protein metabolic enzymes such as alanine aminotransferase (ALT) and aspartate aminotransferase (AST), carbohydrate metabolic enzymes such as lactate dehydrogenase (LDH) and malate dehydrogenase (MDH) and lipid peroxidation (LPO) are important biomarkers of cellular and metabolic stress (Kumar et al., 2011, Kumar et al., 2014b, Kumar et al., 2016b). On this backdrop, the present study was aimed to investigate the possible protective role of dietary selenium nanoparticles (Se-NPs) against thermal tolerance and cellular metabolic stress conconcurrent exposure to lead and elevated temperature (34 °C) in P. hypophthalmus.

Section snippets

Experimental animal

Pangasius hypophthalmus fingerlings were procured from the local fish market (Nil Aquarium, Baramati, Pune India). The fish were treated with a prophylactic dip in salt solution (2%) and then acclimatized to fibre reinforced plastic (FRP) tanks (Circular, 500 L) for one month prior to the experiment. Fish were randomly distributed into 21 plastic tank of 125 L capacity and reared for 72 days. Thirteen fish of uniform size (4.68 ± 0.95 g) per tank were stocked in seven distinct treatment groups in

Thermal tolerance (CTmin, LT min and CTmax, LTmax) of P. hypophthalmus

The effects of Se-NPs on thermal tolerance (CTmin, LTmin and CTmax, LTmax) of P. hypophthalmus exposed and or unexposed to Pb (4 ppm) and high temperature (34 °C) for 72 days are presented in Fig. 2(A–D). The supplementation of Se-NPs exhibited remarkable (p < 0.01) effect on CTmin, LTmin and CTmax, LTmax in different experimental groups. Se-NPs fed groups demonstrated that significantly lowered CTmin and LTmin in compared to control (unexposed), Pb alone as well as concurrent exposed to Pb and high

Discussion

Temperature is one of the most crucial environmental factors for overall development of fish but if temperature rises beyond optimum level, the haemostasis in fish gets disturbed resulting in reduction of growth performance, thermal tolerance, metabolic performance as well as reproductive success of the fish (Fry, 1971). Temperature pre-exposure to fishes facilitate in enhancement of thermal tolerance which is attested by the results of present investigations. Other researchers also reported

Conclusions

Aquatic metal contamination and global warming are serious concerns that hamper the production of aquaculture system. Selenium nanoparticle is the important nutritional components which facilitated in elevated thermal tolerance, improved anti-oxidative status and reduced cellular metabolic stress in P. hypophthalmus @ Se-NPs 1 mg/kg dietary incorporation. To the best of our knowledge, this is the first report on selenium nanoparticles (Se-NPs) as an anti-stress agent in the diet of P.

Acknowledgement

The authors express sincere gratitude to the Director, ICAR-National Institute of abiotic Stress Management, Baramati, Pune for providing all the facilities to conduct the present work. The financial assistance has been provided by Indian Council of Agricultural Research (ICAR), New Delhi, India as institutional project (#IXX09673) is highly acknowledged. I also place a record of thanks to, Mrs. Yogita, and Mr. Yuvraj Sanas for their technical assistance.

References (73)

  • F.E.J. Fry

    the effect of environmental factors on the physiology of the fish

  • S.K. Gupta et al.

    Dietary microbial levan enhances tolerance of Labeo rohita (Hamilton) juveniles to thermal stress

    Aquaculture

    (2010)
  • S. Hestrin

    The reaction of acetyl choline esters and other carboxylic acid derivatives with hydroxylamine and its analytical application

    J. Biol. Chem.

    (1949)
  • J.W. Hilton et al.

    Slinger, The requirement and toxicity of selenium in rainbow trout (Salmo gairdneri)

    J. Nutr.

    (1980)
  • N. Kumar et al.

    Dietary lecithin potentiates thermal tolerance and cellular ctress protection of milk fish (Chanos chanos) reared under low dose endosulfan induced stress

    J. Therm. Biol.

    (2014)
  • N. Kumar et al.

    Dietary pyridoxine potentiates thermal tolerance, heat shock protein and protect against cellular stress of milk fish (Chanos chanos) under endosulfan-induced stress

    Fish Shellfish Immunol.

    (2016)
  • N. Kumar et al.

    Acute toxicity, biochemical and histopathological responses of endosulfan in Chanos chanos

    Ecotoxicol. Environ. Saf.

    (2016)
  • N. Kumar et al.

    Dietary zinc promotes immuno-biochemical plasticity and protects fish against multiple stresses

    Fish Shellfish Immunol.

    (2017)
  • N. Kumar et al.

    Oxidative and cellular metabolic stress of Oreochromis mossambicus as biomarkers indicators of trace element contaminants

    Chemosphere

    (2017)
  • N. Kumar et al.

    Cellular stress and histopathological tools used as biomarkers in Oreochromis mossambicus for assessing metal contamination

    Environ. Toxicol. Pharmacol.

    (2017)
  • O.H. Lowry et al.

    Protein measurement with the folin phenol reagent

    J. Biol. Chem.

    (1951)
  • H.P. Misra et al.

    The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase

    J. Biol. Chem.

    (1972)
  • D.D. Mruk et al.

    Antioxidant superoxide dismutase- a review: its function, regulation in the testis, and role in male fertility

    Contraception

    (2002)
  • K. Nakano et al.

    The 70-kD a heat shock protein response in two intertidal sculpins, Oligocottus maculosus and O. snyderi: relationship of hsp70 and thermal tolerance

    Comp. Biochem. Physiol. A

    (2002)
  • P.A. Olsvik et al.

    Fish pre-acclimation temperature only modestly affects cadmium toxicity in Atlantic salmon hepatocytes

    J. Therm. Biol.

    (2016)
  • H.O. Portner

    Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals

    Comp. Biochem. Physiol. A

    (2002)
  • S.A. Sakr et al.

    Effect of selenium on carbimazole-induced testicular damage and oxidative stress in albino rats

    J. Trace Elem. Med. Biol.

    (2011)
  • C.S. Tejpal et al.

    Effect of dietary supplementation of l-tryptophan on thermal tolerance and oxygen consumption rate in Cirrhinus mrigala fingerlings under varied stocking density

    J. Therm. Biol.

    (2014)
  • APHA-AWWA-WEF
  • S.C. Baker et al.

    Upper lethal temperature of fingerling black crappie

    J. Fish Biol.

    (1996)
  • T.L. Beitinger et al.

    Temperature tolerances of North American freshwater fishes exposed to dynamic changes in temperature

    Environ. Biol. Fish

    (2000)
  • A.E. Favier

    Nutritional and clinical factors affecting the bioavailability of trace elements in humans

  • S. Gawel et al.

    Malondialdehyde (MDA) as a lipid peroxidation marker

    Wiad. Lek.

    (2004)
  • V.N. Gladyshev et al.

    Selenocysteine-containing proteins in mammals

    J. Biomed. Sci.

    (1999)
  • W.H. Habing et al.

    Glutathione-S- Transferase, the first enzymatic step in mercatpopunc acid formation

    J. Biol. Chem.

    (1974)
  • X. Hao et al.

    Effects of dietary selenium on the pathological changes and oxidative stress in loach (Paramisgurnus dabryanus)

    Fish Physiol. Biochem.

    (2014)
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