Abstract
The current study demonstrates oxidative damage and associated neurotoxicity following pH stress in two freshwater carp Labeo rohita and Cirrhinus cirrhosus. Carp (n = 6, 3 replicates) were exposed to four different pH (5.5, 6, 7.5, and 8) against control (pH 6.8 ± 0.05) for 7 days. After completion of treatment, levels of enzymatic (superoxide dismutase [SOD], catalase [CAT], glutathione reductase [GRd]) and non-enzymatic antioxidants (malondialdehyde [MDA], glutathione [GSH]), brain neurological parameters (Na+-K+ATPase, acetylcholinesterase [AcHE], monoamine oxidase [MAO], and nitric oxide [NO]), xanthine oxidase (XO), heat shock proteins (HSP70 and HSP90), and transcription factor NFkB were measured in carp brain. Variation in the pH caused a significant alteration in the glutathione system (glutathione and glutathione reductase), SOD-CAT system, and stress marker malondialdehyde (MDA). Xanthine oxidase was also induced significantly after pH exposure. Brain neurological parameters (MAO, NO, AChE, and Na+-K+ATPase) were significantly reduced at each pH-treated carp group though inhibition was highest at lower acidic pH (5.5). Cirrhinus cirrhosus was more affected than that of Labeo rohita. Molecular chaperon HSP70 expression was induced in all pH-treated groups though such induction was more in acid-stressed fish. HSP90 was found to increase only in acid-stressed carp brain. Expression of NFkB was elevated significantly at each treatment group except for pH 7.5. Finally, both acidic and alkaline pH in the aquatic system was found to disturb oxidative balance in carp brain which ultimately affects the neurological activity in carp. However, acidic environment in the aquatic system was more detrimental than the alkaline system regarding oxidative damage and subsequent neurotoxicity in carp brain.
Similar content being viewed by others
References
Agrahari S, Gopal K (2008) Inhibition of Na+-K+-ATPase in different tissues of freshwater fish Channa punctatus (Bloch) exposed to monocrotophos. Pestic Biochem Physiol 92:57–60
Ahn KS, Aggarwal BB (2005) Transcription factor NF-κB: a sensor for smoke and stress signals. Ann N Y Acad Sci 1056:218–233
Aksoy Y, Balk M, Ögüs IH, Özer N (2004) The mechanism of inhibition of human erythrocyte catalase by azide. Turk J Biol 28:65–70
Ali F, Sultana S (2012) Repeated short-term stress synergizes the ROS signalling through up regulation of NFkB and iNOS expression induced due to combined exposure of trichloroethylene and UVB rays. Mol Cell Biochem 360:133–145
Banaee M (2013) Physiological dysfunction in fish after insecticides exposure. In: Trdan S (ed) Agricultural and biological sciences insecticides, development of safer and more effective technologies. In Tech, Croatia, pp 103–143
Chandanshive NE (2015) Inhibition of Acetylcholin esterase activities by detergents in the nervous system of Mystus montanus. Int J Environ Res 4:48–54
Charrier JG, McFall AS, Richards-Henderson NK, Anastasio C (2014) Hydrogen peroxide formation in a surrogate lung fluid by transition metals and quinones present in particulate matter. Environ Sci Technol 48:7010–7017
Christensen VG, Larson JH, Maki RP, Sandheinrich MB, Brigham ME, Kissane C, Le Duc JF (2017) Lake levels and water quality in comparison to fish mercury body burdens, Voyageurs National Park, Minnesota, 2013–15 (No. 2016-5175). US Geological Survey (2017)
Das D, Moniruzzaman M, Sarbajna A, Chakraborty SB (2017) Effect of heavy metals on tissue-specific antioxidant response in Indian major carps. Environ Sci Pollut Res 24:18010–18024
Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–90
Eroglu A, Dogan Z, Kanak EG, Atli G, Canli M (2015) Effects of heavy metals (Cd, Cu, Cr, Pb, Zn) on fish glutathione metabolism. Environ Sci Pollut Res 22:3229–3237
Fernandes MA, Custódio JB, Santos MS, Moreno AJ, Vicente JA (2006) Tetrandrine concentrations not affecting oxidative phosphorylation protect rat liver mitochondria from oxidative stress. Mitochondrion 6:176–185
Flynn EE, Bjelde BE, Miller NA, Todgham AE (2015) Ocean acidification exerts negative effects during warming conditions in a developing Antarctic fish. Conserv Physiol 3:033
Heuer RM, Grosell M (2014) Physiological impacts of elevated carbon dioxide and ocean acidification on fish. Am J Physiol Regul Integr Comp Physiol ajpregu-00064
Huang L, Mivechi NF, Moskophidis D (2001) Insights into regulation and function of the major stress-induced hsp70 molecular chaperone in vivo: analysis of mice with targeted gene disruption of the hsp70.1 or hsp70.3 gene. Mol Cell Biol 21:8575–8591
John S, Kale M, Rathore N, Bhatnagar D (2001) Protective effect of vitamin E in dimethoate and malathion induced oxidative stress in rat erythrocytes. J Nutr Biochem 12:500–504
Kaplowitz N (1996) Oxidative stress and liver disease. Prog Liver Dis 14:131–159
Kavitha P, Rao JV (2009) Sub-lethal effects of profenofos on tissue-specific antioxidative responses in a euryhyaline fish, Oreochromis mossambicus. Ecotoxicol Environ Saf 72:1727–1733
Keppler D, Leier I, Jedlitschky G (1997) Transport of glutathione conjugates and glucuronides by the multidrug resistance proteins MRP1 and MRP2. Biol Chem 378:787–791
Klanian MG, Preciat MT (2017) Effect of pH on temperature controlled degradation of reactive oxygen species, heat shock protein expression, and mucosal immunity in the sea cucumber Isostichopus badionotus. PLoS One 12:e0175812
Koo JW, Russo SJ, Ferguson D, Nestler EJ, Duman RS (2010) Nuclear factor-κB is a critical mediator of stress-impaired neurogenesis and depressive behavior. Proc Natl Acad Sci 107:2669–2674
Kumar S, Moniruzzaman M, Mukherjee M, Debjit D, Chakraborty SB (2016) Mucuna seed extract treatment alleviates SDS-induced oxidative stress and neuronal damage in carp brain. IJPPR 8:1669–1674
Li ZH, Li P, Shi ZC (2015) Chronic exposure to tributyltin induces brain functional damage in juvenile common carp (Cyprinus carpio). PLoS One 10:e0123091
Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666
Madeira D, Narciso L, Cabral HN, Vinagre C (2012) Thermal tolerance and potential impacts of climate change on coastal and estuarine organisms. J Sea Res 70:32–41
Moniruzzaman M, Hasan KN, Maitra SK (2016) Melatonin actions on ovaprim (synthetic GnRH and domperidone)-induced oocyte maturation in carp. Reproduction 151:285–296
Moniruzzaman M, Midday P, Dhara A, Das D, Ghosal I, Mukherjee D, Chakraborty SB (2017) Change in redox state and heat shock protein expression in an Indian major carp Cirrhinus cirrhosus exposed to zinc and lead. J Toxicol Sci 42:731–740
Morgan JD, Iwama GK (1991) Effects of salinity on growth, metabolism, and ion regulation in juvenile rainbow and steelhead trout (Oncorhynchus mykiss) and fall chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci 48:2083–2094
Morgan MJ, Liu ZG (2011) Crosstalk of reactive oxygen species and NF-κB signaling. Cell Res 21:103–115
Mourente G, Dıaz-Salvago E, Bell JG, Tocher DR (2002) Increased activities of hepatic antioxidant defence enzymes in juvenile gilthead sea bream (Sparus aurata L.) fed dietary oxidised oil: attenuation by dietary vitamin E. Aquaculture 214:343–361
Mukherjee M, Moniruzzaman M, Kumar S, Das D, Chakraborty SB (2017a) Neuronal and oxidative damage in the catfish brain alleviated after mucuna seed extract treatment. IJPPR 9:52–57
Mukherjee J, Moniruzzaman M, Chakraborty SB, Lek S, Ray S (2017b) Towards a physiological response of fishes under variable environmental conditions: an approach through neural network. Ecol Indic 78:381e394
Niklitschek EJ, Secor DH (2009) Dissolved oxygen, temperature and salinity effects on the ecophysiology and survival of juvenile Atlantic sturgeon in estuarine waters: I. Laboratory results. J Exp Mar Biol Ecol 381:150–160
Padmini E, Tharani J (2015) Differential expression of heat shock proteins in fish hepatocytes under hypoxic condition. Int J Fish Aquat Stud 3:447–455
Pal A, He Y, Jekel M, Reinhard M, Gin KYH (2014) Emerging contaminants of public health significance as water quality indicator compounds in the urban water cycle. Environ Int 71:46–62
Peng J, Jones GL, Watson K (2000) Stress proteins as biomarkers of oxidative stress: effects of antioxidant supplements. Free Radic Biol Med 28:1598–1606
Pörtner HO (2010) Oxygen-and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213:881–893
Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97
Rahal A, Kumar A, Singh V, Yadav B, Tiwari R, Chakraborty S, Dhama K (2014) Oxidative stress, prooxidants, and antioxidants: the interplay. Biomed Res Int 2014:1–19
Rajan DS (2015) An evaluation of the effect of a detergent on dissolved oxygen consumption rate of Anabas testudineus. IJFAS 2:46–48
Reddy GR, Devi BC, Chetty CS (2007) Developmental lead neurotoxicity: alterations in brain cholinergic system. Neurotoxicology 28:402–407
Richert DA, Edwards S, Westerfeld WW (1949) On the determination of liver xanthine oxidase and the respiration of rat liver homogenates. J Biol Chem 181:255–271
Roessig JM, Woodley CM, Cech JJ, Hansen LJ (2004) Effects of global climate change on marine and estuarine fishes and fisheries. Rev Fish Biol Fish 14:251–275
Sarada S, Himadri P, Mishra C, Geetali P, Ram MS, Ilavazhagan G (2008) Role of oxidative stress and NFkB in hypoxia-induced pulmonary edema. Exp Biol Med 233:1088–1098
Sessa WC, Pritchard K, Seyedi N, Wang J, Hintze TH (1994) Chronic exercise in dogs increases coronary vascular nitric oxide production and endothelial cell nitric oxide synthase; gene expression. Circ Res 74:349–353
Sies H (1985) Hydroperoxides and thiol oxidants in the study of oxidative stress in intact cells and organs. Oxidative Stress 73–90
Solaini G, Baracca A, Lenaz G, Sgarbi G (2010) Hypoxia and mitochondrial oxidative metabolism. Biochim Biophys Acta 1797:1171–1177
Tabakoff B, Alivisatos SGA (1972) Modified method for spectrophotometric determination of monoamine oxidase activity. Anal Chem 44:427–428
Traystman RJ, Kirsch JR, Koehler RC (1991) Oxygen radical mechanisms of brain injury following ischemia and reperfusion. J Appl Physiol 71:1185–1195
Tseng YC, Chen RD, Lucassen M, Schmidt MM, Dringen R, Abele D, Hwang PP (2011) Exploring uncoupling proteins and antioxidant mechanisms under acute cold exposure in brains of fish. PLoS One 6:e18180
Zhang J, Zuo Z, Chen R, Chen Y, Wang C (2008) Tributyltin exposure causes brain damage in Sebastiscus marmoratus. Chemosphere 73:337–343
Acknowledgments
The authors thankfully acknowledge Mr. Ramkrishna Das for his assistance during the course of the experimental setup and maintenance of experimental fish.
Funding
This study was financially supported by DST-NPDF (PDF/2017/001308) and DBT Research Associateship Programme, Govt. of India, IISC, Bangalore.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The investigation conforms to the Guide for the Care and Use of Laboratory Animals published by the US National Institute of Health (NIH Publication No. 85-23, revised 1996) and was also approved by the Institutional Animal Ethics Committee, University of Calcutta (Registration #885/ac/05/CPCSEA), registered under the “Committee for the Purpose of Control and Supervision of Experiments on Laboratory Animals” (CPCSEA), Ministry of Environment and Forests, Government of India.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible editor: Thomas Braunbeck
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 15 kb)
Rights and permissions
About this article
Cite this article
Mukherjee, A., Bhowmick, A.R., Mukherjee, J. et al. Physiological response of fish under variable acidic conditions: a molecular approach through the assessment of an eco-physiological marker in the brain. Environ Sci Pollut Res 26, 23442–23452 (2019). https://doi.org/10.1007/s11356-019-05602-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-05602-3