Abstract
The aim of this study was to compare low-temperature tolerances in different strains of large yellow croaker. Dai Qu (DQ), Min-Yue Dong (MY), and Quan Zhou (NZ) strains of large yellow croaker were subjected to cold stress (8.6 °C) for 12 h, 24 h, 48 h, and 96 h. Survival rate, histological observation, and antioxidant and energy metabolism indicators were determined. The results showed that compared with the DQ group and MY group, NZ group aggravated hepatic structure, enhanced ROS, lactate, and anaerobic metabolism (PK gene expression and activity), while inhibited ATP, GSH, antioxidant enzymes (mRNA levels and activities of SOD, GPx, and CAT), and aerobic metabolism enzymes (mRNA levels and activities of F-ATPase, SDH, and MDH), indicating the reduction of cold tolerance in the NZ group was closely correlated with the decrement of antioxidative capacity and energy metabolism efficiency. Nrf2 and AMPK gene expressions were correlated with antioxidant and energy metabolism mRNA levels, respectively, suggesting Nrf2 and AMPK might participate in the modulation of target genes during the cold-stress adaptation. In conclusion, low temperature tolerance of fish depended on the antioxidant defense and energy metabolism efficiency, which contributes to understanding the underlying mechanisms of cold adaptation in large yellow croaker.
Similar content being viewed by others
Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Aebi H (1984) [13] Catalase in vitro. Methods Enzymol 105:121–126
Bizuayehu TT, Johansen SD, Puvanendran V, Toften H, Babiak I (2015) Temperature during early development has long-term effects on microRNA expression in Atlantic cod. BMC Genomics 16:1–12
Cao L, Tang R, Huang W, Wang Y (2021) Seasonal variability and dynamics of coastal sea surface temperature fronts in the East China Sea. Ocean Dynam 71:237–249
Dodson M, Redmann M, Rajasekaran NS, Darley-Usmar V, Zhang J (2015) KEAP1-NRF2 signalling and autophagy in protection against oxidative and reductive proteotoxicity. Biochem J 469:347–355
Drotar A, Phelps P, Fall R (1985) Evidence for glutathione peroxidase activities in cultured plant cells. Plant Sci 42:35–40
Fedoseeva IV, Pyatrikas DV, Stepanov AV, Fedyaeva AV, Varakina NN, Rusaleva TM, Borovskii GB, Rikhvanov EG (2017) The role of flavin-containing enzymes in mitochondrial membrane hyperpolarization and ROS production in respiring Saccharomyces cerevisiae cells under heat-shock conditions. Sci Rep 7:2586
Foster GD, Moon TW (1986) Enzyme activities in the Atlantic hagfish, Myxine glutinosa: changes with captivity and food deprivation. Can J Zool 64:1080–1085
Han S, Wei S, Chen R, Ni M, Chen L (2022) Tissue-specific and differential cold responses in the domesticated cold tolerant fugu. Fishes 7:159
Huang D, Liang H, Zhu J, Ren M, Ge X (2022) Transcriptome reveals insights into hepatic nutritional metabolism and gill immune responses adapted to cold stress in genetically improved farmed tilapia (GIFT: Oreochromis niloticus). Aquacult Rep 26:101297
Huang D, Ni X, Tang Q, Zhu X, Xu D (2012) Spatial and temporal variability of sea surface temperature in the Yellow Sea and East China Sea over the past 141 years. Mod Climatol 7:213–234
Ighodaro OM, Akinloye OA (2017) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alex J Med 54:287–293
Jerez-Cepa I, Marín-Rincón A, Martínez-Rodríguez G, Ruiz-Jarabo I, Mancera JM (2020) A natural additive in the diet to improve growth and reduce energy expenditure of gilthead seabream (Sparus aurata L.): attenuation of high stocking density stress responses. Aquaculture 524:735263
Kahn BB, Alquier T, Carling D, Hardie DG (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 1:15–25
Kon T, Pei L, Ichikawa R, Chen C, Wang P, Takemura I, Ye Y, Yan X, Guo B, Li W (2021) Whole-genome resequencing of large yellow croaker (Larimichthys crocea) reveals the population structure and signatures of environmental adaptation. Sci Rep 11:11235
Liu M, Zhou Y, Guo X, Wei W, Li Z, Zhou L, Wang Z, Gui J (2022) Comparative transcriptomes and metabolomes reveal different tolerance mechanisms to cold stress in two different catfish species. Aquaculture 560:738543
Liu Q, Lin H, Chen J, Ma J, Liu R, Ding S (2020) Genetic variation and population genetic structure of the large yellow croaker (Larimichthys crocea) based on genome-wide single nucleotide polymorphisms in farmed and wild populations. Fish Res 232:105718
Luo C, Wang X, Long J, Liu J (2006) An NADH-tetrazolium-coupled sensitive assay for malate dehydrogenase in mitochondria and crude tissue homogenates. J Biochem Biophys Methods 68:101–111
Miao L, Ming-Yun LI, Chen J, Zhang H (2014) Breeding of fast growth and low temperature tolerance of new variety donghai no.1 large yellow croaker (pseudosciaena crocea). J Agr Biotechnol 22:1314–1320
Martínez-Reyes I, Cuezva JM (2014) The H+-ATP synthase: a gate to ROS-mediated cell death or cell survival. Biochim Biophys Acta 1837:1099–1112
Mateus AP, Costa R, Gisbert E, Pinto PI, Andree KB, Estévez A, Power DM (2017) Thermal imprinting modifies bone homeostasis in cold-challenged sea bream (Sparus aurata). J Exp Biol 220:3442–3454
Morcillo P, Esteban MA, Cuesta A (2016) Heavy metals produce toxicity, oxidative stress and apoptosis in the marine teleost fish SAF-1 cell line. Chemosphere 144:225–233
Morin C, Zini R, Simon N, Tillement JP (2002) Dehydroepiandrosterone and α- estradiol limit the functional alterations of rat brain mitochondria submitted to different experimental stresses. Neuroscience 115:415–424
Nakano M, Kimura H, Hara M, Kuroiwa M, Yoshikawa T (1990) A highly sensitive method for determining both Mn- and Cu-Zn superoxide dismutase activities in tissues and blood cells. Anal Biochem 187:277–280
Nesci S, Trombetti F, Ventrella V, Pagliarani A (2018) From the Ca2+-activated F1FO-ATPase to the mitochondrial permeability transition pore: an overview. Biochimie 152:85–93
Nie M, Hu J, Lu Y, Wu Z, You F (2019) Cold effect analysis and screening of SNPs associated with cold-tolerance in the olive flounder Paralichthys olivaceus. J Appl Ichthyol 35:924–932
Nitzan T, Kokou F, Doron-Faigenboim A, Slosman T, Biran J (2019) Transcriptome analysis reveals common and differential response to low temperature exposure between tolerant and sensitive blue tilapia (Oreochromis aureus). Front Genet 10:100
Omini J, Wojciechowska I, Skirycz A, Moriyama H, Obata T (2021) Association of the malate dehydrogenase-citrate synthase metabolon is modulated by intermediates of the Krebs tricarboxylic acid cycle. Sci Rep 11:1–10
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RTPCR. Nucleic Acids Res 29:e45
Philip GH, Reddy PM, Sridevi G (1995) Cypermethrin-induced in vivo alterations in the carbohydrate metabolism of freshwater fish, Labeo rohita. Ecotoxicol Environ Saf 31:173–178
Sadi G, Bozan D, Yildiz HB (2014) Redox regulation of antioxidant enzymes: post-translational modulation of catalase and glutathione peroxidase activity by resveratrol in diabetic rat liver. Mol Cell Biochem 393:111–122
Schleger IC, Carneiro Pereira DM, Resende AC, Romao S, Herrerias T, Alves Neundorf AK, Sloty AM, Guimaraes IM, Rosa DPDS, Maria Carster GP (2022) Cold and warm waters: energy metabolism and antioxidant defenses of the freshwater fish Astyanax lacustris (Characiformes: Characidae) under thermal stress. J Comp Physiol B 192:77–94
Sokolova I (2021) Bioenergetics in environmental adaptation and stress tolerance of aquatic ectotherms: linking physiology and ecology in a multi-stressor landscape. J Exp Biol 224:jeb236802
Wen X, Chu P, Xu J, Wei X, Yin S (2020) Combined effects of low temperature and salinity on the immune response, antioxidant capacity and lipid metabolism in the pufferfish (Takifugu fasciatus). Aquaculture 531:735866
Wu C, Zhang D, Kan M, Lv Z, Zhu A, Su Y, Zhou D, Zhang J, Zhang Z, Xu M, Jiang L, Guo B, Wang T, Chi C, Mao Y, Zhou J, Yu X, Wang H, Weng X, Jin JG, Ye J, He L, Liu Y (2014) The draft genome of the large yellow croaker reveals well-developed innate immunity. Nat Commun 5:5227
Wu Z, Wu J, Zhao Q, Fu S, Jin J (2020) Emerging roles of aerobic glycolysis in breast cancer. Clin Transl Oncol 22:631–646
Xu H, Zhang DL, Yu DH, Lv CH, Luo HY, Wang ZY (2015) Molecular cloning and expression analysis of scd1 gene from large yellow croaker Larimichthys crocea under cold stress. Gene 568:100–108
Yu Y, Zhang HR, Jin J, Wang Y (2019) Trends of sea surface temperature and sea surface temperature fronts in the South China Sea during 2003–2017. Acta Oceanol Sin 38:106–115
Zeng L, Ai CX, Wang YH, Zhang JS, Wu CW (2017) Abrupt salinity stress induces oxidative stress via the Nrf2-Keap1 signaling pathway in large yellow croaker Pseudosciaena crocea. Fish Physiol Biochem 43:955–964
Zeng L, Ai CX, Zhang JS, Li WC (2020) Pre-hypoxia exposure inhibited copper toxicity by improving energy metabolism, antioxidant defence and mitophagy in the liver of the large yellow croaker Larimichthys crocea. Sci Total Environ 708:134961
Zeng L, Ai CX, Zheng JL, Zhang JS, Li WC (2019) Cu pre-exposure alters antioxidant defense and energy metabolism in large yellow croaker Larimichthys crocea in response to severe hypoxia. Sci Total Environ 687:702–711
Zeng L, Li WC, Zhang H, Cao P, Song W (2021) Hypoxic acclimation improves mitochondrial bioenergetic function in large yellow croaker Larimichthys crocea under Cu stress. Ecotoxicol Environ Saf 224:112688
Zeng L, Liu B, Wu CW, Lei JL, Xu MY, Zhu AY, Zhang JS, Hong WS (2016) Molecular characterization and expression analysis of AMPK α subunit isoform genes from Scophthalmus maximus responding to salinity stress. Fish Physiol Biochem 42:1595–1607
Zhang M, Hu J, Zhu J, Wang Y, Zhang Y, Li Y, Xu S, Yan X, Zhang D (2022) Transcriptome, antioxidant enzymes and histological analysis reveal molecular mechanisms responsive to long-term cold stress in silver pomfret (Pampus argenteus). Fish Shellfish Immunol 121:351–361
Zhang QY, Hong WS, Yang SY, Liu M (2011) Discussion on the division of geographic populations for the large yellow croaker (Larimichthys crocea). Mod Fish Inf 2:3–8
Zhang W, Gao J, Lu L, Bold T, Tang J (2021) Intracellular GSH/GST antioxidants system change as an earlier biomarker for toxicity evaluation of iron oxide nanoparticles. NanoImpact 23:100338
Zorov DB, Juhaszova M, Sollott SJ (2006) Mitochondrial ROS induced ROS release: an update and review. BBA-Bioenerg 1757:509–517
Funding
This study was supported by the Natural Science Foundation of Fujian Province (2022J01027), Natural Science Foundation of Zhejiang Province (LY18D060008), and Key research projects of universities of Anhui Education Department (2022AH051923).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Yong-Hong Wang, Hui Zhang, Yu-Cong Huang, and Wei-Guang Zou. The first draft of the manuscript was written by Chun-Xiang Ai, the main manuscript was revised by Lin Zeng, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethical approval
We assured that all experiments, animal care, and protocols followed the ethical guidelines of the Bengbu University for the care and use of laboratory animals, and also followed the ethical guidelines of the Zhejiang Ocean University for the care and use of laboratory animals.
With the submission of this manuscript “Different cold tolerances among three strains of large yellow croaker: related to antioxidant defense and energy metabolism,” I would like to confirm that the above-mentioned manuscript has not been published elsewhere, accepted for publication elsewhere or under editorial review for publication elsewhere; and that my Institutes’ (Bengbu University and Zhejiang Ocean University) representatives are fully aware of this submission.
Consent for publication
All authors agree to submit the manuscript entitled “Different cold tolerances among three strains of large yellow croaker: related to antioxidant defense and energy metabolism” to Fish Physiology and Biochemistry for publication consideration.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zeng, L., Wang, YH., Ai, CX. et al. Different cold tolerances among three strains of large yellow croaker: related to antioxidant defense and energy metabolism. Fish Physiol Biochem 49, 471–486 (2023). https://doi.org/10.1007/s10695-023-01201-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-023-01201-9