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Oxidative stress responses in the respiratory tree and the body wall of sea cucumber Apostichopus japonicus (Selenka) to high temperature

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Abstract

Sea cucumber Apostichopus japonicas (Selenka) is one of the important aquaculture species distributed in northern China. In recent years, global warming caused frequent high temperature weather in summer in northern China, resulting in dramatic losses of the sea cucumber aquaculture industry. In the present study, we focused on the effect of oxidative stress in Apostichopus japonicus (Selenka) subjected to high temperature stress. Sea cumbers were exposed to the control (16 °C), and high temperature treatments (20 °C, 24 °C, and 28 °C) for 7 days. Then, reactive oxygen species (ROS) level, superoxide dismutase (SOD) activity, catalase (CAT) activity, peroxidase (POD) activity, reduced glutathione (GSH) content, malondialdehyde (MDA) content and 8-hydroxy-2′-deoxyguanosine (8-OHdG) level in the respiratory tree and body wall were detected, respectively. Results showed that 24 °C and 28 °C acute exposure induced the elevation of ROS level, SOD, CAT, POD activities, GSH content, MDA content and 8-OHdG level in the respiratory tree of sea cucumber. In contrast, no significant changes were observed for ROS and 8-OHdG levels in the body wall of sea cucumber, while the antioxidants including SOD, CAT, POD, and GSH decreased to some extent. Moreover, MDA content exhibited a noticeable increase in the body wall, similarly to that in the respiratory tree, indicating that high temperature could induce severe lipid peroxidation in two tissues. Considering the differences in various biomarkers measured in two tissues, respiratory tree might be more susceptible to the high temperature changes compared to the body wall. Our findings may help understand the oxidative stress response to high temperature in the respiratory tree and the body wall in A. japonicus.

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References

  • Abele D, Puntarulo S (2004) Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comp Biochem Physiol A Mol Integr Physiol 138:405–415

    Article  Google Scholar 

  • Almroth BC, de Souza KB, Jonsson E, Sturve J (2019) Oxidative stress and biomarker responses in the Atlantic halibut after long term exposure to elevated CO2 and a range of temperatures. Comp Biochem Physiol B Biochem Mol Biol 238:8

    Google Scholar 

  • An ZH, Dong YW, Dong SL (2009) A high-performance temperature-control scheme: growth of sea cucumber Apostichopus japonicus with different modes of diel temperature fluctuation. Aquacult Int 17:459–467

    Article  Google Scholar 

  • Anderson ME (1985) Determination of glutathione and glutathione disulfide in biological samples. In Methods in Enzymology, vol 113. Academic Press, New York, pp 548–555

  • Bai YC, Chen Y, Pan Y, Zhang LB, Liu SL, Ru XS, **ng LL, Zhang T, Yang HS, Li J (2018) Effect of temperature on growth, energy budget, and physiological performance of green, white, and purple color morphs of sea cucumber, Apostichopus japonicus. J World Aquacult Soc 49:625–637

    Article  CAS  Google Scholar 

  • Becker D, Brinkmann BF, Zeis B, Paul RJ (2011) Acute changes in temperature or oxygen availability induce ROS fluctuations in Daphnia magna linked with fluctuations of reduced and oxidized glutathione, catalase activity and gene (haemoglobin) expression. Biol Cell 103:351–363

    Article  CAS  Google Scholar 

  • Bindoff NL, Cheung WW, Kairo JG, Arstegui J, Guinder VA, Hallberg R, Hilmi N, Jiao N, Karim M, Levin L (2019) Changing ocean, marine ecosystems, and dependent communities: IPCC Special Report on the Ocean and Cryosphere in a Changing Climate. Intergovernmental Panel on Climate Change, Switzerland, pp 477–587

  • Chen JX, Lovatelli A, Conand C, Purcell S, Uthicke S, Hamel J, Mercier A (2004) Present status and prospects of sea cucumber industry in China. Ile 1:25–38

    Google Scholar 

  • Cheng CH, Guo ZX, Luo SW, Wang AL (2018) Effects of high temperature on biochemical parameters, oxidative stress, DNA damage and apoptosis of pufferfish (Takifugu obscurus). Ecotoxicol Environ Saf 150:190–198

    Article  CAS  Google Scholar 

  • Ding Y, Pan L, Lin W (2016) Effect of temperature on immune and antioxidant parameters of Apostichopus japonicus. Trans Oceanol Limnol 3:91–99

  • Dolmatov IY, Frolova LT, Zakharova EA, Ginanova TT (2011) Development of respiratory trees in the holothurian Apostichopus japonicus (Aspidochirotida: Holothuroidea). Cell Tissue Res 346:327–338

    Article  Google Scholar 

  • Dong YW, Dong SL (2006) Growth and oxygen consumption of the juvenile sea cucumber Apostichopus japonicus (Selenka) at constant and fluctuating water temperatures. Aquac Res 37:1327–1333

    Article  Google Scholar 

  • Dong YW, Ji TT, Dong SL (2007) Stress responses to rapid temperature changes of the juvenile sea cucumber (Apostichopus japonicus Selenka). J Ocean Univ China 6:275–280

    Article  CAS  Google Scholar 

  • Dong YW, Yu SS, Wang QL, Dong SL (2011) Physiological responses in a variable environment: relationships between metabolism, hsp and thermotolerance in an intertidal-subtidal species. PLoS One 6:6

    Article  Google Scholar 

  • Duan YF, Zhang Y, Dong HBA, Wang Y, Zhang JS (2017) Effect of the dietary probiotic Clostridium butyricum on growth, intestine antioxidant capacity and resistance to high temperature stress in kuruma shrimp Marsupenaeus japonicus. J Therm Biol 66:93–100

    Article  CAS  Google Scholar 

  • Duran EG, Cuaya MP, Gutierrez MV, Leon JA (2018) Effects of temperature and pH on the oxidative stress of benthic marine invertebrates. Biol Bull 45:610–616

    Article  Google Scholar 

  • Forman HJ, Zhang H, Rinna A (2009) Glutathione: overview of its protective roles, measurement, and biosynthesis. Mol Aspects Med 30:1–12

    Article  CAS  Google Scholar 

  • Freire CA, Welker AF, Storey JM, Storey KB, Hermes-Lima M (1999) Oxidative stress in estuarine and intertidal environments (temperate and tropical). Oxidative Stress in Aquatic Ecosystems. Wiley-Blackwell, New Jersey, pp 41–57

  • Gao F, Yang HS, Xu Q, Wang FY, Liu GB (2009) Effect of water temperature on digestive enzyme activity and gut mass in sea cucumber Apostichopus japonicus (Selenka), with special reference to aestivation. Chin J Oceanol Limnol 27:714–722

    Article  CAS  Google Scholar 

  • Gismondi E, Beisel JN, Cossu-Leguille C (2012) Influence of gender and season on reduced glutathione concentration and energy reserves of Gammarus roeseli. Environ Res 118:47–52

    Article  CAS  Google Scholar 

  • Góth L (1991) A simple method for determination of serum catalase activity and revision of reference range. Clin Chim Acta 196:143–151

    Article  Google Scholar 

  • Hayes JD, McLellan LI (1999) Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radic Res 31:273–300

  • Hellou J, Ross NW, Moon TW (2012) Glutathione, glutathione S-transferase, and glutathione conjugates, complementary markers of oxidative stress in aquatic biota. Environ Sci Pollut Res 19:2007–2023

    Article  CAS  Google Scholar 

  • Huo D, Sun LN, Ru XS, Zhang LB, Lin CG, Liu SL, **n XK, Yang HS (2018) Impact of hypoxia stress on the physiological responses of sea cucumber Apostichopus japonicus: respiration, digestion, immunity and oxidative damage. PeerJ 6:24

    Article  Google Scholar 

  • Huo D, Sun L, Sun JC, Zhang LB, Liu SL, Su F, Yang HS (2021) Sea cucumbers in a high temperature and low dissolved oxygen world: roles of miRNAs in the regulation of environmental stresses. Environ Pollut 268:9

    Article  Google Scholar 

  • Ji TT, Dong YW, Dong SL (2008) Growth and physiological responses in the sea cucumber, Apostichopus japonicus Selenka: aestivation and temperature. Aquaculture 283:180–187

    Article  CAS  Google Scholar 

  • Kamyab E, Kuhnhold H, Novais SC, Alves LM, Indriana L, Kunzmann A, Slater M, Lemos MF (2017) Effects of thermal stress on the immune and oxidative stress responses of juvenile sea cucumber Holothuria scabra. J Comp Physiol B 187:51–61

    Article  CAS  Google Scholar 

  • Kim JH, Park HJ, Kim KW, Hwang IK, Kim DH, Oh CW, Lee JS, Kang JC (2017) Growth performance, oxidative stress, and non-specific immune responses in juvenile sablefish, Anoplopoma fimbria, by changes of water temperature and salinity. Fish Physiol Biochem 43:1421–1431

    Article  CAS  Google Scholar 

  • Kurutas EB (2016) The importance of antioxidants which play the role in cellular response against oxidative/nitrosative stress: current state. Nutr J 15:22

    Google Scholar 

  • LeBel CP, Ischiropoulos H, Bondy SC (1992) Evaluation of the probe 2’,7’-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 5:227–231

    Article  CAS  Google Scholar 

  • Li C, Fang H, Xu D (2019a) Effect of seasonal high temperature on the immune response in Apostichopus japonicus by transcriptome analysis. Fish Shellfish Immunol 92:765–771

    Article  CAS  Google Scholar 

  • Li L, Chen MY, Storey KB (2019b) Metabolic response of longitudinal muscles to acute hypoxia in sea cucumber Apostichopus japonicus (Selenka): A metabolome integrated analysis. Comp Biochem Physiol D Genomics Proteomics 29:235–244

    Article  CAS  Google Scholar 

  • Li XS, Liao GX, Ju ZL, Wang CY, Li N, **ong DQ, Zhang YL (2020) Antioxidant response and oxidative stress in the respiratory tree of sea cucumber (Apostichopus japonicus) following exposure to crude oil and chemical dispersant. J Mar Sci Eng 8:547

    Article  Google Scholar 

  • Li XS, Wang CY, Li N, Gao YL, Ju ZL, Liao GX, **ong DQ (2021) Combined effects of elevated temperature and crude oil pollution on oxidative stress and apoptosis in sea cucumber (Apostichopus japonicus, Selenka). Int J Environ Res Public Health 18:801

    Article  CAS  Google Scholar 

  • Liu S, Zhang S, Ru X, Sun L, Li J, Zhou Y, Yang H (2016) Effect of high temperature stress on the fertility of male and female gametes of the sea cucumber Apostichopus japonicus. Aquac Res 47:3127–3135

    Article  Google Scholar 

  • Lundquist I, Josefsson JO (1971) Sensitive method for determination of peroxidase activity in tissue by means of coupled oxidation reaction. Anal Biochem 41:567–577

    Article  CAS  Google Scholar 

  • Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30

    Article  CAS  Google Scholar 

  • Madeira C, Leal MC, Diniz MS, Cabral HN, Vinagre C (2018) Thermal stress and energy metabolism in two circumtropical decapod crustaceans: responses to acute temperature events. Mar Environ Res 141:148–158

    Article  CAS  Google Scholar 

  • Madkour LH (2020) Consequences of oxidative stress and ROS-mediated pathways cellular signaling stress response. RETRACTED BOOK Nanoparticles Induce Oxidative and Endoplasmic. Springer, Cham, pp 193–260

  • Yu XJ, Xu LJ, Wu FX (2020) China fishery statistical yearbook. Chinese Agricultural Press, Bei**g, pp 28

  • Masella R, Di Benedetto R, Varì R, Filesi C, Giovannini C (2005) Novel mechanisms of natural antioxidant compounds in biological systems: involvement of glutathione and glutathione-related enzymes. J Nutr Biochem 16:577–586

    Article  CAS  Google Scholar 

  • Okun MR, Edelstein LM, Or N, Hamada G, Donnellan B, Lever WF (1970) Histochemical differentiation of peroxidase-mediated from tyrosinase-mediated melanin formation in mammalian tissues. Histochemie 23:295–309

    Article  CAS  Google Scholar 

  • Rabeh I, Telahigue K, Bejaoui S, Hajji T, Chouba L, El Cafsi M, Soudani N (2019) Effects of mercury graded doses on redox status, metallothionein levels and genotoxicity in the intestine of sea cucumber Holothuria forskali. Chem Ecol 35:204–218

    Article  CAS  Google Scholar 

  • Ray PD, Huang B, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24:981–990

    Article  CAS  Google Scholar 

  • Sanchez W, Burgeot T, Porcher JM (2013) A novel “Integrated Biomarker Response” calculation based on reference deviation concept. Environ Sci Pollut Res 20:2721–2725

    Article  CAS  Google Scholar 

  • Sarasamma S, Audira G, Samikannu P, Juniardi S, Siregar P, Hao EW, Chen JR, Hsiao CD (2019) Behavioral impairments and oxidative stress in the brain, muscle, and gill caused by chronic exposure of C70 nanoparticles on adult zebrafish. Int J Mol Sci 20:23

    Article  Google Scholar 

  • Schieber M, Chandel NS (2014) ROS function in redox signaling and oxidative stress. Curr Biol 24:R453–R462

    Article  CAS  Google Scholar 

  • Schmedes A, Hølmer G (1989) A new thiobarbituric acid (TBA) method for determining free malondialdehyde (MDA) and hydroperoxides selectively as a measure of lipid peroxidation. J Am Oil Chem Soc 66:813–817

    Article  CAS  Google Scholar 

  • Sies H (2015) Oxidative stress: a concept in redox biology and medicine. Redox Biol 4:180–183

    Article  CAS  Google Scholar 

  • Sies H (2020) Oxidative stress: concept and some practical aspects. Antioxidants (Basel) 9:6

    Google Scholar 

  • Slimen IB, Najar T, Ghram A, Dabbebi H, Ben Mrad M, Abdrabbah M (2014) Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. A review. Int J Hyperth 30:513–523

    Article  Google Scholar 

  • Snezhkina AV, Kudryavtseva AV, Kardymon OL, Savvateeva MV, Melnikova NV, Krasnov GS, Dmitriev AA (2019) ROS generation and antioxidant defense systems in normal and malignant cells. Oxid Med Cell Longev 2019:17

    Article  Google Scholar 

  • Sokolova IM, Sukhotin AA, Lannig G (1999) Stress effects on metabolism and energy budgets in mollusks, Oxidative Stress in Aquatic Ecosystems. Wiley-Blackwell, New Jersey, pp 261–280

  • Sun HJ, Zhou ZC, Dong Y, Yang AF, Jiang B, Gao S, Chen Z, Guan XY, Wang B, Wang XL (2013) Identification and expression analysis of two Toll-like receptor genes from sea cucumber (Apostichopus japonicus). Fish Shellfish Immunol 34:147–158

    Article  Google Scholar 

  • Telahigue K, Rabeh I, Bejaoui S, Hajji T, Nechi S, Chelbi E, El Cafsi M, Soudani N (2020) Mercury disrupts redox status, up-regulates metallothionein and induces genotoxicity in respiratory tree of sea cucumber (Holothuria forskali). Drug Chem Toxicol 43:287–297

    Article  CAS  Google Scholar 

  • Valavanidis A, Vlachogianni T, Fiotakis C (2009) 8-hydroxy-2′ -deoxyguanosine (8-OHdG): a critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health C 27:120–139

    Article  CAS  Google Scholar 

  • Vinagre C, Madeira D, Narciso L, Cabral HN, Diniz M (2012) Effect of temperature on oxidative stress in fish: lipid peroxidation and catalase activity in the muscle of juvenile seabass, Dicentrarchus labrax. Ecol Ind 23:274–279

    Article  CAS  Google Scholar 

  • Vinagre C, Madeira D, Mendonca V, Dias M, Roma J, Diniz MS (2014) Effect of temperature in multiple biomarkers of oxidative stress in coastal shrimp. J Therm Biol 41:38–42

    Article  CAS  Google Scholar 

  • Wang H, Liu S, Cui J, Li C, Hu Y, Zhou W, Chang Y, Qiu X, Liu Z, Wang X (2015) Identification and characterization of microRNAs from longitudinal muscle and respiratory tree in sea cucumber (Apostichopus japonicus) using high-throughput sequencing. PLoS One 10:e0134899

    Article  Google Scholar 

  • Wang L (2019) Present situation and strategy on development of sea cucumber breeding in Dalian. Inner Mongolia Sci Tech Econ 10:14–15

  • Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ, de Bettignies T, Bennett S, Rousseaux CS (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat Clim Chang 3:78–82

    Article  Google Scholar 

  • Wilhelm D, Tribess T, Gaspari C, Claudio FD, Torres MA, Magalhaes ARM (2001) Seasonal changes in antioxidant defenses of the digestive gland of the brown mussel (Perna perna). Aquaculture 203:149–158

    Article  Google Scholar 

  • Wilhelm Filho D, Torres M, Tribess T, Pedrosa R, Soares C (2001) Influence of season and pollution on the antioxidant defenses of the cichlid fish acará (Geophagus brasiliensis). Braz J Med Biol Res 34:719–726

    Article  CAS  Google Scholar 

  • Wu DH, Zheng PP, Zhang YY, Wang CL (2010) Effect of temperature stress on serum non-specific immune factors in swimming crab Portunus trituberculatus. J Dalian Ocean Univ 25:370–375

    CAS  Google Scholar 

  • Yang AF, Zhou ZC, He CB, Hu JJ, Chen Z, Gao XG, Dong Y, Jiang B, Liu WD, Guan XY, Wang XY (2009) Analysis of expressed sequence tags from body wall, intestine and respiratory tree of sea cucumber (Apostichopus japonicus). Aquaculture 296:193–199

    Article  CAS  Google Scholar 

  • Yang H, Wang X, Pei H, Fan D (2019) Cloning a peroxidase cDNA sequence from the oriental armyworm, Mythimna separata walker and its induction to different temperature stress. Chin J Biol Control 35:44–52

  • Yang HS, Yuan XT, Zhou Y, Mao YZ, Zhang T, Liu Y (2005) Effects of body size and water temperature on food consumption and growth in the sea cucumber Apostichopus japonicus (Selenka) with special reference to aestivation. Aquac Res 36:1085–1092

    Article  Google Scholar 

  • Yang HS, Zhou Y, Zhang T, Yuan XT, Li XX, Liu Y, Zhang FS (2006) Metabolic characteristics of sea cucumber Apostichopus japonicus (Selenka) during aestivation. J Exp Mar Biol Ecol 330:505–510

    Article  CAS  Google Scholar 

  • Yuan XT, Yang HS, Wang LL, Zhou Y, Zhang T (2007) Effects of aestivation on energy budget of sea cucumber Apostichopus japonicus (Selenka) (Echinodermata:Holothuroidea). Acta Ecol Sin 27:3155–3161

    Article  Google Scholar 

  • Yuan XT, Yang HS, Wang LL, Zhou Y, Gabr HR (2009) Bioenergetic responses of sub-adult sea cucumber Apostichopus japonicus (Selenka) (Echinodermata: Holothuroidea) to temperature with special discussion regarding its southernmost distribution limit in China. J Therm Biol 34:315–319

    Article  Google Scholar 

  • Zacarias-Soto M, Tec-Tec P, Olvera-Novoa MA (2018) Effect of diet on growth and body biochemical composition of juvenile four-sided sea cucumber Isostichopus badionotus (Selenka, 1867). Aquac Res 49:939–946

    Article  CAS  Google Scholar 

  • Zhang J, Wang X, Vikash YQ, Wu D, Liu Y, Dong W (2016a) ROS and ROS-mediated cellular signaling. Oxid Med Cell Longev 2016:4350965

    Article  Google Scholar 

  • Zhang P, **ng XL, Sun JX, Zhao W (2016b) Advances on heavy metals pollution and its toxicology to sea cucumbers. Mar Environ Sci 35:149–154

    Google Scholar 

  • Zhang XQ, Hu CY, Sun X, Zang XN, Zhang XC, Fang T, Xu NJ (2020) Comparative transcriptome analysis reveals chitooligosaccharides-induced stress tolerance of Gracilariopsis lemaneiformis under high temperature stress. Aquaculture 519:13

    Article  Google Scholar 

  • Zhou J, Wang L, **n Y, Wang WN, He WY, Wang AL, Liu Y (2010) Effect of temperature on antioxidant enzyme gene expression and stress protein response in white shrimp, Litopenaeus vannamei. J Therm Biol 35:284–289

    Article  CAS  Google Scholar 

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Acknowledgements

The authors are grateful to the editor and the anonymous reviewers for their availability to review this work. Their valuable comments and suggestions have improved the quality of the manuscript.

Funding

This research was funded by the National Key Research and Development Program of China, grant number 2018YFD0900606, and the National Natural Science Foundation of China, grant numbers 42076215 and 42076167.

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Authors and Affiliations

  1. School of Environmental Science and Engineering, Dalian Maritime University, Dalian, 116026, China

    Zhonglei Ju, Yulu Zhang, Nan Li, **shan Li, Yuhang Zou, Wei Yang & Deqi **ong

  2. National Marine Environmental Monitoring Center, Dalian, 116023, China

    Zhonglei Ju, Guoxiang Liao, **shan Li & Yuhang Zou

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  1. Zhonglei Ju
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Contributions

Conceptualization, G.L., D.X., Z.J. and X.L.; methodology, G.L., Z.J and X.L.; software, Z.J.; validation, Z.J, X.L., N.L. and Y.Z.; formal analysis, Z.J; investigation, Z.J., X.L., N.L., W.Y. and Y.Z.; resources, G.L. and D.X.; data curation, Z.J.; writing-original draft preparation, Z.J.; writing-review and editing, Z.J., X.L. and G.L.; visualization, Z.J. and G.L.; supervision, G.L. and D.X.; project administration, G.L.; funding acquisition, G.L. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Deqi **ong.

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Ju, Z., Liao, G., Zhang, Y. et al. Oxidative stress responses in the respiratory tree and the body wall of sea cucumber Apostichopus japonicus (Selenka) to high temperature. Environ Sci Pollut Res 30, 21288–21298 (2023). https://doi.org/10.1007/s11356-022-23308-x

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