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Biomarkers as ecological indices in monitoring the status of market fish

Biomarkers as ecological indices in monitoring the status of market fish Background Environmental contamination has become a major concern over the past few decades, drawing the attention of numerous researchers from both developed and developing nations. The aquatic system serves as the primary sink for the disposal of garbage, which has a negative impact on the aquatic environment and biota. The real- ity is that heavy metals cannot be totally removed from the ecosystem because they can bioaccumulate and grow in strength as they move up the food chain. Particularly heavy metals can build up in the tissues of aquatic animals, and as a result, tissue concentrations of heavy metals may be harmful to both human and animal health. Our study aimed to elucidate the possible use of biomarkers in monitoring and assessing the heavy metals contaminants among fresh water fish. Results From the present study, we conclude that glutathione peroxidase can be used as the bioindicator for nickel and iron contamination. Ultimately, these studies focus on measuring levels of pollution that may induce irreversible ecological changes to aquatic ecosystems. Till now the level of toxicity was moderate, and it was progressing toward the danger. Eor ff ts can be made to control the activities that release pollutants unnaturally into the environment from both public and government so that the clean and clear environment can be maintained. Conclusions The work concludes that a multiparameter analysis is needed to assess and monitor the ecological status of the aquatic environment. Keywords Antioxidant enzymes, Bioindicator, Environmental management, Heavy metal, Pollution (Prüss-Ustün et  al., 2011). It was reported that the two Background biggest crises all over the earth are contamination and Over the last three decades there has been increasing massive disposal of waste in aquatic environment (Anh global concern over environmental awareness over water et al., 2010; Arkoosh et al., 2010). pollution. Water forms a basis for transfer of nutrients Environmental pollutants represent a risk factor for in all ecosystem, which ultimately threatens aquatic life human and animals in all areas of occurrence in the and ends in human via the food chain (Afshan et  al., form of gas, solid and liquid forms as a single or syner- 2014; Garg et  al., 2009; Nagarani et  al., 2020). About a gistic action (Kovacik, 2017). The normal prevalence of quarter of the diseases facing humankind today occur heavy metals is not harmful to the environment, but their due to prolonged exposure to environmental pollution presence at higher concentrations becomes toxic, and pollution in relation to their toxicity to aquatic organ- isms affects the ultimate well-being of humans. Such *Correspondence: N. Nagarani occurrence of high level of pollutants, i.e., heavy met- nagaranikannan@yahoo.co.in als, is known to inhibit biochemical and physiological Department of Zoology, Fatima College (Autonomous), Mary Land, mechanisms vital for fish metabolism (Nagarani et  al., Madurai, Tamil Nadu 625 018, India 2020; Shuhaimi-Othman et  al., 2013). Bioaccumulation © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Nagarani et al. The Journal of Basic and Applied Zoology (2023) 84:2 Page 2 of 6 of any metal above its threshold level results in irrevers- red colored gill, muscle smooth without mucus (indicate ible physiological conditions (Zhang et al., 2010). Despite the presence of microbes or pathogens) and chemical the large scale of natural source for heavy metals, previ- smell free. Collected samples were immediately stored in ous report reveals that the higher contribution toward ice-cold conditions (4 °C). For each analysis three individ- heavy metals pollution is by anthropogenic source, espe- uals per species were used. Fish were washed thoroughly cially for Pb, Hg, Cd, Zn and Cu than natural release, via., with sterilized distilled water and oven-dried for metal anthropogenic and industrial effluents into fresh water analysis. The concentrations of metals were determined and marine resources (Bhattacharyya et al., 2021). according to the standard double acid digestion methods Heavy metals inhibit the functions of structural pro- analyzed using an atomic absorption spectrometer. Stand- teins, enzymes and nucleic acids by forming metal com- ards were made using certified solutions (Merck, UK) plexes (Jaishankar et al., 2014). In addition it also induces acidified with H NO to the same pH as the samples. Fresh structural or morphological alterations, chromosomal samples were stored at − 80 °C for further enzymatic stud- aberrations, and ultimately results in impairment in the ies. The whole samples were homogenized in trichloro immune system (Coen et  al., 2012). The nature of heavy acidic acid (TCA) for lipid peroxidation analysis and in metal toxicity in fish primarily depends on various phys - phosphate buffer (pH 7) for reduced glutathione analyses. ico-chemical parameters including its solubility, hard- ness, pH and ecosystem complexity via gills, food and Determination of non‑enzymatic biomarkers skin (Tao et  al., 2001). Fishes are one of the main nutri- Lipid peroxidation in fish liver, gill, microsomes (pooled tional components consumed by humans. Besides, this sample mixture) was evaluated by the thiobarbituric acid fish was at apex in aquatic food chain; hence, they can be (TBA) method (Buege and Aust, 1978). The reaction mix - a best bioindicators for aquatic pollution. Fish have the ture, 8.1% sodium dodecyl sulfate (0.2 ml) and thiobarbi- ability to uptake and concentrate metals directly from the turic acid 20% in trichloroacidic acid (2 ml) were heated surrounding water or indirectly from other organisms for 1  h in boiling water bath. After cooling, n-butanol: such as small fish, invertebrates and aquatic vegetation. pyridine (15:1) mixture solution was added and centri- Fish accumulate pollutants preferentially in their fatty fuged to obtain n-butanol: pyridine layer. The absorb - tissues like liver the end of the aquatic food chain and ance of the sample was estimated at 532 nm. The level of may accumulate metals and pass them to human beings lipid peroxide was expressed as malondialdehyde (MDA) through food causing chronic or acute diseases (AL-You- nmol/mg protein using the extinction coefficient for the −1 −1 suf et al., 2000). MDA = 1.55 M cm . Heavy metals are known to induce oxidative stress The concentration, c, from the equation and/or carcinogenesis by mediating free radicals/reac- tive oxygen species (Javed et al., 2015). Redox active met- = , the light path, l, is 1 cm. εxl als (Fe, Cu, Cr, Hg, Pb, Cd, Ni) produced ROS through redox cycling which disturbs the thiol groups containing Reduced glutathione (GSH) was assayed by the method antioxidants and enzymes (Jomova et  al., 2010; Kurtuas, of Boyne and Ellman (Boyne & Ellman, 1942). Briefly, 2015; Stohs & Bagchi, 1995) and damage the fish at vari - One milliliter of homogenate (PBS, pH 7.4) was centrifu- ous level including DNA, gills, membrane lipids and pro- gation at 8000 rpm for 15 min at 4 °C. The assay mixture teins. Each oxidative stress parameter is specific for some contained 0.1  ml filtered aliquot and 2.7  ml phosphate of the heavy metals. Based on this information, selection buffer (0.1  M, pH 7.4) in a total volume of 3.0  ml. After of specific oxidative biomarkers has to be done for accu - centrifugation, 2.0  ml of the protein-free supernatant rate analysis. With the backdrop of this information the was mixed with 0.2  ml of 0.4  M Na HPO4 and 1.0  ml present study was conducted to test the environmental of DTNB (5,5- dithio-bis-(2-nitrobenzoic acid)) reagent risk assessment in market fish. (40  mg DTNB in 100  ml of aqueous 1% trisodium cit- rate). The yellow color developed was read immediately Methods at 412  nm in a spectrophotometer. GSH concentration Sample collection and preservation was expressed as nmol/mg. The healthy fresh fish were procured during early morn - ing at 5.30 am from the local fish market at Narimedu Post‑mitochondrial supernatant preparation (PMS) (9.9372°  N, 78.1258°  E), Madurai, Tamilnadu, India. The Tissues were perfused with ice-cold saline (0.9% sodium study was conducted during the period of January–April chloride) and homogenized in chilled potassium chlo- 2019. The samples used in the study were selected by ride (1.17%) using a homogenizer. The homogenates were physical observation based on the criteria such as grown centrifuged at 3000 rpm for 5 min at 4 °C to separate the fish (fingerlings were avoided), fresh without rotten smell, Nagar ani et al. The Journal of Basic and Applied Zoology (2023) 84:2 Page 3 of 6 nuclear debris. The supernatant so obtained was centri - Results fuged at 10,000  rpm for 20  min at 4  °C to get the post- The work was carried out to assess the environmental mitochondrial supernatant which was used to assay stress in the marine fish at local market. This study also biomarker enzymes. The antioxidant enzyme response measures the bioaccumulation of pollutants and its effect was measured using a double-beam UV spectrometer during transport. The list of fish samples collected from (Model 2201; Systronics). the local market is given in Table 1. One unit of enzymes is equal to 50% inhibition. The malondialdehyde (MDA), an intermediate of the oxidation of polyunsaturated fatty acids, is considered as Blank − Sample a useful index of general lipid peroxidation. Malondial- Inhibition(%) = × 100 Blank dehyde (MDA) forms an adduct with thiobarbituric acid which can be quantified by spectrophotometer at 532 nm. In practice, TBARS is expressed in terms of malondialde- Biomarker enzyme analysis hyde (MDA) equivalent which is depicted in Fig.  1. The The enzyme biomarkers were quantified by standard pro - TBARS in the sample is 2 to 200  µM MDA. Among the tocol. Superoxide dismutase (SOD) activity was assayed order Periciformes Alectis indica showed lower MDA by the method of Kono et  al., 2000; catalase activity formation. The non-antioxidant compounds glutathione, (Matsumura et al., 2002); acetyl choline esterase enzyme a part of glutathione peroxidase, and glutathione reduc- (AChE) activity was measured by using spectrophotom- tase enzymes were measured in the reduced form. The eter based on Ellman’s method (1961), and glutathione glutathione content was found to be varying from 5 to peroxidase (GPx) activity in the homogenate was evalu- 39 µM in the species under study, as shown in Fig. 2. ated by the NADPH (nicotinamide adenine dinucleotide phosphate) method with minor modification (Rotruck et al., 1973). One unit of enzymes is equal to 50% inhibition. Blank − Sample Inhibition(%) = × 100 Blank Statistical analysis All the experiments were performed thrice to get the concordant values. All statistical tests are performed using GraphPad Prism (version 8). Data are reported as Mean ± SD, and statistical difference will be accepted at P < 0.05. Fig. 1 Level of MDA formation in the collected fish Table 1 List of fish collated to study the environmental risk assessment S. no Vernacular name Scientific name Class Order 1 Emperor Long Face emperor bream Lethrinus olivaceus Actinopterygii Perciformes 2 Indian goat fish (Nagarai Meen) Parupeneus indicus Actinopterygii Perciformes 3 Malabar Trevally/Jack Fish—Paarai Meen Carangoides malabaricus Actinopterygii Perciformes 4 Blue Fin Travelly Alectis indica Actinopterygii Perciformes 5 Silver Pomfret Pampus argenteus Actinopterygii Scombriformes 6 Chaalai or Sardine Sardinella longiceps Actinopterygii Clupeiformes 7 Ailai/Dolphin Coryphaena hippurus (Linnaeus, 1758) Actinopterygii Perciformes 8 Mural, Needle fish, Viraal, Gar fish Hemiramphus far (Forsskal, 1775) Actinopterygii Beloniformes 9 Barracuda (ooli) Sphyraena forsteri (Cuvier, 1829) Actinopterygii Scombriformes 10 Kilanga, Lady Fish Elops machnata (Forskal, 1775) Actinopterygii Elopiformes 11 Crab Portunus pelagicus Malacostraca Decapoda Nagarani et al. The Journal of Basic and Applied Zoology (2023) 84:2 Page 4 of 6 Fig. 2 Level of reduced glutathione in the collected fish Fig. 5 Glutathione peroxidase activity Fig. 3 Superoxide dismutase activity Fig. 6 Catalase activity Fig. 4 Acetylcholine esterase activity Fig. 7 Heavy metal studies in the collected fish samples Enzymes play an important role during the metal toxicity in eliminating and converting the free radical observed to have higher concentration of acetyl choline into stable molecule and thus prevent cellular damage. esterase enzyme activity than other species (Fig. 4). Cory- The biochemical markers of environmental stress are phaena hippurus was observed to have higher concentra- depicted Figs.  3, 4, 5 and 6. Coryphaena hippurus  was tion of GPx (Fig. 5). The catalase activity was noted to be observed to have higher concentration of superoxide moderate among all fish species and ranges between 0.1 dismutase enzymes than other species. Silver Pomfret and 1.2 units and is depicted in Fig. 6. and Sphyraena forsteri of order Sconmrifoemes were Nagar ani et al. The Journal of Basic and Applied Zoology (2023) 84:2 Page 5 of 6 The concentration of metals in the muscle tissues biomarker responses in fish from highly polluted areas is depicted in Fig.  7. The level of metals was below the close to a point source is quite challenging since response permissible limit; hence, the less or no environmen- to toxicants may also differ between areas and fish spe - tal risk was found in the collected species (FAO, 1984). cies (Balk et al., 2011). The order of accumulation of metals in the fish was Fe > Mn > Zn > Cu > Ni irrespectively to the species. Fe Conclusions was low in crab when compared with fish due to the role There is a growing concern that the elements through the of iron in hemoglobin formation, followed by manganese, natural cycling process are being disturbed by anthro- zinc and copper which participate as cofactors in SOD pogenic activities, especially the growth of industrial, formation; on the other hand, Ni was found to be low domestic and urban discharge of its effluents. From the since Ni was one of the non-essential metals. present study, we conclude that glutathione peroxidize can be used as the biomarkers for Ni, Fe contamina- tion. Ultimately, these studies must focus on measuring Discussion levels of pollution that may induce irreversible ecologi- Compared to the order Perciformes the other two order cal changes to aquatic ecosystems. Till now the levels of Beloniformes and Scombriformes have higher levels of toxicity were moderate, and it was progressing toward reduced glutathione. Usually animals encounter oxidative the danger. Efforts can be made to maintain and control stress upon exposure to pollutants or heavy metals. This the activities that release pollutants unnaturally into the disturbs their cellular ionic homeostasis through their environment from both public and government so that oxidative defense mechanisms such as enzyme, chelation the clean and clear environment can be maintained. (Nagarani et  al., 2009). The reduced glutathione (GSH) was found to increase since GSH has a vital role in pro- tein metabolism. The increase in the reduced glutathione Abbreviations AChE Acetyl choline esterase enzyme level in the present study may also be due to the synthe- CAT Catalase sis of metal chelator (Nagarani et al., 2012). The increase DTNB-5,5 Dithio-bis-(2-nitrobenzoic acid) in the levels of MDA may be due to external physiologi- GPx Glutathione peroxidase GSH Reduced glutathione cal stress. Fish exhibit many of the same defenses against MDA Malondialdehyde oxidative stress as do mammals. These defenses include NADPH Nicotinamide adenine dinucleotide phosphate both low molecular weight free radical scavengers such PMS Post-mitochondrial suspension SOD Superoxide dismutase as GSH and ascorbic acid, as well as enzymatic defense TBA Thiobarbituric acid such as SOD, Ach E, CAT and GPx. The high concentra - TCA Trichloro acidic acid tion of SOD with reference to the level of Cu indicates Acknowledgements the role of Cu as cofactor ions in the formation Cu-SOD Authors acknowledge all laboratory assistants at Fatima College for their in fish. contributions during this study. Copper are bonded with many cytoplasmic and mem- Author contributions brane proteins like ferritin, which in turn would release All authors were involved for sampling, field work, laboratory activities, data and increase the metal ions in the tissues. These free ions collection and statistical analysis. The authors GK, DD, KGM, MAJ, PVM and were able to catalyze the breakdown of hydrogen perox- RS involved in data collection and laboratory works. The manuscript was prepared by GK, while edited by NN. All authors have read and approved the ide into water molecules through the Fenton reaction. manuscript. The level of CAT and SOD activity in animals usually reflects the face of environmental pollutants (Dautrem - Funding Not funded. epuits et  al., 2004), since SOD-CAT was the first line of defense against oxidative stress. The CAT activity was Availability of data and materials noted to decrease; this may be due to the flux of superox - We declare that the data generated from this study are readily available as well as the materials used. ide ion formation which in turn decreases the formation of hydrogen peroxide and inhibit CAT activity (Pandey Declarations et al., 2003). The low level of CAT also confirms that the sample is pathogen free. 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Biomarkers as ecological indices in monitoring the status of market fish

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Abstract

Background Environmental contamination has become a major concern over the past few decades, drawing the attention of numerous researchers from both developed and developing nations. The aquatic system serves as the primary sink for the disposal of garbage, which has a negative impact on the aquatic environment and biota. The real- ity is that heavy metals cannot be totally removed from the ecosystem because they can bioaccumulate and grow in strength as they move up the food chain. Particularly heavy metals can build up in the tissues of aquatic animals, and as a result, tissue concentrations of heavy metals may be harmful to both human and animal health. Our study aimed to elucidate the possible use of biomarkers in monitoring and assessing the heavy metals contaminants among fresh water fish. Results From the present study, we conclude that glutathione peroxidase can be used as the bioindicator for nickel and iron contamination. Ultimately, these studies focus on measuring levels of pollution that may induce irreversible ecological changes to aquatic ecosystems. Till now the level of toxicity was moderate, and it was progressing toward the danger. Eor ff ts can be made to control the activities that release pollutants unnaturally into the environment from both public and government so that the clean and clear environment can be maintained. Conclusions The work concludes that a multiparameter analysis is needed to assess and monitor the ecological status of the aquatic environment. Keywords Antioxidant enzymes, Bioindicator, Environmental management, Heavy metal, Pollution (Prüss-Ustün et  al., 2011). It was reported that the two Background biggest crises all over the earth are contamination and Over the last three decades there has been increasing massive disposal of waste in aquatic environment (Anh global concern over environmental awareness over water et al., 2010; Arkoosh et al., 2010). pollution. Water forms a basis for transfer of nutrients Environmental pollutants represent a risk factor for in all ecosystem, which ultimately threatens aquatic life human and animals in all areas of occurrence in the and ends in human via the food chain (Afshan et  al., form of gas, solid and liquid forms as a single or syner- 2014; Garg et  al., 2009; Nagarani et  al., 2020). About a gistic action (Kovacik, 2017). The normal prevalence of quarter of the diseases facing humankind today occur heavy metals is not harmful to the environment, but their due to prolonged exposure to environmental pollution presence at higher concentrations becomes toxic, and pollution in relation to their toxicity to aquatic organ- isms affects the ultimate well-being of humans. Such *Correspondence: N. Nagarani occurrence of high level of pollutants, i.e., heavy met- nagaranikannan@yahoo.co.in als, is known to inhibit biochemical and physiological Department of Zoology, Fatima College (Autonomous), Mary Land, mechanisms vital for fish metabolism (Nagarani et  al., Madurai, Tamil Nadu 625 018, India 2020; Shuhaimi-Othman et  al., 2013). Bioaccumulation © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Nagarani et al. The Journal of Basic and Applied Zoology (2023) 84:2 Page 2 of 6 of any metal above its threshold level results in irrevers- red colored gill, muscle smooth without mucus (indicate ible physiological conditions (Zhang et al., 2010). Despite the presence of microbes or pathogens) and chemical the large scale of natural source for heavy metals, previ- smell free. Collected samples were immediately stored in ous report reveals that the higher contribution toward ice-cold conditions (4 °C). For each analysis three individ- heavy metals pollution is by anthropogenic source, espe- uals per species were used. Fish were washed thoroughly cially for Pb, Hg, Cd, Zn and Cu than natural release, via., with sterilized distilled water and oven-dried for metal anthropogenic and industrial effluents into fresh water analysis. The concentrations of metals were determined and marine resources (Bhattacharyya et al., 2021). according to the standard double acid digestion methods Heavy metals inhibit the functions of structural pro- analyzed using an atomic absorption spectrometer. Stand- teins, enzymes and nucleic acids by forming metal com- ards were made using certified solutions (Merck, UK) plexes (Jaishankar et al., 2014). In addition it also induces acidified with H NO to the same pH as the samples. Fresh structural or morphological alterations, chromosomal samples were stored at − 80 °C for further enzymatic stud- aberrations, and ultimately results in impairment in the ies. The whole samples were homogenized in trichloro immune system (Coen et  al., 2012). The nature of heavy acidic acid (TCA) for lipid peroxidation analysis and in metal toxicity in fish primarily depends on various phys - phosphate buffer (pH 7) for reduced glutathione analyses. ico-chemical parameters including its solubility, hard- ness, pH and ecosystem complexity via gills, food and Determination of non‑enzymatic biomarkers skin (Tao et  al., 2001). Fishes are one of the main nutri- Lipid peroxidation in fish liver, gill, microsomes (pooled tional components consumed by humans. Besides, this sample mixture) was evaluated by the thiobarbituric acid fish was at apex in aquatic food chain; hence, they can be (TBA) method (Buege and Aust, 1978). The reaction mix - a best bioindicators for aquatic pollution. Fish have the ture, 8.1% sodium dodecyl sulfate (0.2 ml) and thiobarbi- ability to uptake and concentrate metals directly from the turic acid 20% in trichloroacidic acid (2 ml) were heated surrounding water or indirectly from other organisms for 1  h in boiling water bath. After cooling, n-butanol: such as small fish, invertebrates and aquatic vegetation. pyridine (15:1) mixture solution was added and centri- Fish accumulate pollutants preferentially in their fatty fuged to obtain n-butanol: pyridine layer. The absorb - tissues like liver the end of the aquatic food chain and ance of the sample was estimated at 532 nm. The level of may accumulate metals and pass them to human beings lipid peroxide was expressed as malondialdehyde (MDA) through food causing chronic or acute diseases (AL-You- nmol/mg protein using the extinction coefficient for the −1 −1 suf et al., 2000). MDA = 1.55 M cm . Heavy metals are known to induce oxidative stress The concentration, c, from the equation and/or carcinogenesis by mediating free radicals/reac- tive oxygen species (Javed et al., 2015). Redox active met- = , the light path, l, is 1 cm. εxl als (Fe, Cu, Cr, Hg, Pb, Cd, Ni) produced ROS through redox cycling which disturbs the thiol groups containing Reduced glutathione (GSH) was assayed by the method antioxidants and enzymes (Jomova et  al., 2010; Kurtuas, of Boyne and Ellman (Boyne & Ellman, 1942). Briefly, 2015; Stohs & Bagchi, 1995) and damage the fish at vari - One milliliter of homogenate (PBS, pH 7.4) was centrifu- ous level including DNA, gills, membrane lipids and pro- gation at 8000 rpm for 15 min at 4 °C. The assay mixture teins. Each oxidative stress parameter is specific for some contained 0.1  ml filtered aliquot and 2.7  ml phosphate of the heavy metals. Based on this information, selection buffer (0.1  M, pH 7.4) in a total volume of 3.0  ml. After of specific oxidative biomarkers has to be done for accu - centrifugation, 2.0  ml of the protein-free supernatant rate analysis. With the backdrop of this information the was mixed with 0.2  ml of 0.4  M Na HPO4 and 1.0  ml present study was conducted to test the environmental of DTNB (5,5- dithio-bis-(2-nitrobenzoic acid)) reagent risk assessment in market fish. (40  mg DTNB in 100  ml of aqueous 1% trisodium cit- rate). The yellow color developed was read immediately Methods at 412  nm in a spectrophotometer. GSH concentration Sample collection and preservation was expressed as nmol/mg. The healthy fresh fish were procured during early morn - ing at 5.30 am from the local fish market at Narimedu Post‑mitochondrial supernatant preparation (PMS) (9.9372°  N, 78.1258°  E), Madurai, Tamilnadu, India. The Tissues were perfused with ice-cold saline (0.9% sodium study was conducted during the period of January–April chloride) and homogenized in chilled potassium chlo- 2019. The samples used in the study were selected by ride (1.17%) using a homogenizer. The homogenates were physical observation based on the criteria such as grown centrifuged at 3000 rpm for 5 min at 4 °C to separate the fish (fingerlings were avoided), fresh without rotten smell, Nagar ani et al. The Journal of Basic and Applied Zoology (2023) 84:2 Page 3 of 6 nuclear debris. The supernatant so obtained was centri - Results fuged at 10,000  rpm for 20  min at 4  °C to get the post- The work was carried out to assess the environmental mitochondrial supernatant which was used to assay stress in the marine fish at local market. This study also biomarker enzymes. The antioxidant enzyme response measures the bioaccumulation of pollutants and its effect was measured using a double-beam UV spectrometer during transport. The list of fish samples collected from (Model 2201; Systronics). the local market is given in Table 1. One unit of enzymes is equal to 50% inhibition. The malondialdehyde (MDA), an intermediate of the oxidation of polyunsaturated fatty acids, is considered as Blank − Sample a useful index of general lipid peroxidation. Malondial- Inhibition(%) = × 100 Blank dehyde (MDA) forms an adduct with thiobarbituric acid which can be quantified by spectrophotometer at 532 nm. In practice, TBARS is expressed in terms of malondialde- Biomarker enzyme analysis hyde (MDA) equivalent which is depicted in Fig.  1. The The enzyme biomarkers were quantified by standard pro - TBARS in the sample is 2 to 200  µM MDA. Among the tocol. Superoxide dismutase (SOD) activity was assayed order Periciformes Alectis indica showed lower MDA by the method of Kono et  al., 2000; catalase activity formation. The non-antioxidant compounds glutathione, (Matsumura et al., 2002); acetyl choline esterase enzyme a part of glutathione peroxidase, and glutathione reduc- (AChE) activity was measured by using spectrophotom- tase enzymes were measured in the reduced form. The eter based on Ellman’s method (1961), and glutathione glutathione content was found to be varying from 5 to peroxidase (GPx) activity in the homogenate was evalu- 39 µM in the species under study, as shown in Fig. 2. ated by the NADPH (nicotinamide adenine dinucleotide phosphate) method with minor modification (Rotruck et al., 1973). One unit of enzymes is equal to 50% inhibition. Blank − Sample Inhibition(%) = × 100 Blank Statistical analysis All the experiments were performed thrice to get the concordant values. All statistical tests are performed using GraphPad Prism (version 8). Data are reported as Mean ± SD, and statistical difference will be accepted at P < 0.05. Fig. 1 Level of MDA formation in the collected fish Table 1 List of fish collated to study the environmental risk assessment S. no Vernacular name Scientific name Class Order 1 Emperor Long Face emperor bream Lethrinus olivaceus Actinopterygii Perciformes 2 Indian goat fish (Nagarai Meen) Parupeneus indicus Actinopterygii Perciformes 3 Malabar Trevally/Jack Fish—Paarai Meen Carangoides malabaricus Actinopterygii Perciformes 4 Blue Fin Travelly Alectis indica Actinopterygii Perciformes 5 Silver Pomfret Pampus argenteus Actinopterygii Scombriformes 6 Chaalai or Sardine Sardinella longiceps Actinopterygii Clupeiformes 7 Ailai/Dolphin Coryphaena hippurus (Linnaeus, 1758) Actinopterygii Perciformes 8 Mural, Needle fish, Viraal, Gar fish Hemiramphus far (Forsskal, 1775) Actinopterygii Beloniformes 9 Barracuda (ooli) Sphyraena forsteri (Cuvier, 1829) Actinopterygii Scombriformes 10 Kilanga, Lady Fish Elops machnata (Forskal, 1775) Actinopterygii Elopiformes 11 Crab Portunus pelagicus Malacostraca Decapoda Nagarani et al. The Journal of Basic and Applied Zoology (2023) 84:2 Page 4 of 6 Fig. 2 Level of reduced glutathione in the collected fish Fig. 5 Glutathione peroxidase activity Fig. 3 Superoxide dismutase activity Fig. 6 Catalase activity Fig. 4 Acetylcholine esterase activity Fig. 7 Heavy metal studies in the collected fish samples Enzymes play an important role during the metal toxicity in eliminating and converting the free radical observed to have higher concentration of acetyl choline into stable molecule and thus prevent cellular damage. esterase enzyme activity than other species (Fig. 4). Cory- The biochemical markers of environmental stress are phaena hippurus was observed to have higher concentra- depicted Figs.  3, 4, 5 and 6. Coryphaena hippurus  was tion of GPx (Fig. 5). The catalase activity was noted to be observed to have higher concentration of superoxide moderate among all fish species and ranges between 0.1 dismutase enzymes than other species. Silver Pomfret and 1.2 units and is depicted in Fig. 6. and Sphyraena forsteri of order Sconmrifoemes were Nagar ani et al. The Journal of Basic and Applied Zoology (2023) 84:2 Page 5 of 6 The concentration of metals in the muscle tissues biomarker responses in fish from highly polluted areas is depicted in Fig.  7. The level of metals was below the close to a point source is quite challenging since response permissible limit; hence, the less or no environmen- to toxicants may also differ between areas and fish spe - tal risk was found in the collected species (FAO, 1984). cies (Balk et al., 2011). The order of accumulation of metals in the fish was Fe > Mn > Zn > Cu > Ni irrespectively to the species. Fe Conclusions was low in crab when compared with fish due to the role There is a growing concern that the elements through the of iron in hemoglobin formation, followed by manganese, natural cycling process are being disturbed by anthro- zinc and copper which participate as cofactors in SOD pogenic activities, especially the growth of industrial, formation; on the other hand, Ni was found to be low domestic and urban discharge of its effluents. From the since Ni was one of the non-essential metals. present study, we conclude that glutathione peroxidize can be used as the biomarkers for Ni, Fe contamina- tion. Ultimately, these studies must focus on measuring Discussion levels of pollution that may induce irreversible ecologi- Compared to the order Perciformes the other two order cal changes to aquatic ecosystems. Till now the levels of Beloniformes and Scombriformes have higher levels of toxicity were moderate, and it was progressing toward reduced glutathione. Usually animals encounter oxidative the danger. Efforts can be made to maintain and control stress upon exposure to pollutants or heavy metals. This the activities that release pollutants unnaturally into the disturbs their cellular ionic homeostasis through their environment from both public and government so that oxidative defense mechanisms such as enzyme, chelation the clean and clear environment can be maintained. (Nagarani et  al., 2009). The reduced glutathione (GSH) was found to increase since GSH has a vital role in pro- tein metabolism. The increase in the reduced glutathione Abbreviations AChE Acetyl choline esterase enzyme level in the present study may also be due to the synthe- CAT Catalase sis of metal chelator (Nagarani et al., 2012). The increase DTNB-5,5 Dithio-bis-(2-nitrobenzoic acid) in the levels of MDA may be due to external physiologi- GPx Glutathione peroxidase GSH Reduced glutathione cal stress. Fish exhibit many of the same defenses against MDA Malondialdehyde oxidative stress as do mammals. These defenses include NADPH Nicotinamide adenine dinucleotide phosphate both low molecular weight free radical scavengers such PMS Post-mitochondrial suspension SOD Superoxide dismutase as GSH and ascorbic acid, as well as enzymatic defense TBA Thiobarbituric acid such as SOD, Ach E, CAT and GPx. The high concentra - TCA Trichloro acidic acid tion of SOD with reference to the level of Cu indicates Acknowledgements the role of Cu as cofactor ions in the formation Cu-SOD Authors acknowledge all laboratory assistants at Fatima College for their in fish. contributions during this study. Copper are bonded with many cytoplasmic and mem- Author contributions brane proteins like ferritin, which in turn would release All authors were involved for sampling, field work, laboratory activities, data and increase the metal ions in the tissues. These free ions collection and statistical analysis. The authors GK, DD, KGM, MAJ, PVM and were able to catalyze the breakdown of hydrogen perox- RS involved in data collection and laboratory works. The manuscript was prepared by GK, while edited by NN. All authors have read and approved the ide into water molecules through the Fenton reaction. manuscript. The level of CAT and SOD activity in animals usually reflects the face of environmental pollutants (Dautrem - Funding Not funded. epuits et  al., 2004), since SOD-CAT was the first line of defense against oxidative stress. The CAT activity was Availability of data and materials noted to decrease; this may be due to the flux of superox - We declare that the data generated from this study are readily available as well as the materials used. ide ion formation which in turn decreases the formation of hydrogen peroxide and inhibit CAT activity (Pandey Declarations et al., 2003). The low level of CAT also confirms that the sample is pathogen free. 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The Journal of Basic and Applied Zoology – Springer Journals

Published: Jan 10, 2023

Keywords: Antioxidant enzymes; Bioindicator; Environmental management; Heavy metal; Pollution

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