Cite this paper:
Desheng ZOU, Weian CAO, Guilong LIU, Junhao NING, Xia LU, Jinjing WANG, Min CHEN, Bo LIU, Jinsheng ZHANG, Chunde WANG. Effects of acute and chronic thermal stress on survival, apoptosis, and transcriptional responses of Scapharca broughtonii[J]. Journal of Oceanology and Limnology, 2023, 41(6): 2363-2373

Effects of acute and chronic thermal stress on survival, apoptosis, and transcriptional responses of Scapharca broughtonii

Desheng ZOU1,2, Weian CAO1, Guilong LIU3, Junhao NING1,2, Xia LU1,2, Jinjing WANG1,2, Min CHEN1,2, Bo LIU4, Jinsheng ZHANG5, Chunde WANG1,3,4
1 Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai 264003, China;
2 University of Chinese Academy of Sciences, Beijing 100049, China;
3 Yantai Spring-Sea AquaSeed Co., Ltd., Yantai 264006, China;
4 Qingdao Agricultural University, Qingdao 266109, China;
5 Zhaoyuan Xiadian Agricultural Technology Promotion Station, Yantai 265415, China
Ocean warming is altering the habitats of marine invertebrates, which has resulted in an increased physiological stress to marine molluscs, especially those intertidal bivalves, such as the ark shell Scapharca broughtonii. We investigated the physiological and transcriptional responses of ark shells to acute and chronic thermal stress results showed that at 33 ℃, a significantly higher cumulative mortality (55.7%) occurred under acute thermal stress than chronic thermal stress. The apoptosis rate of hemocytes was sustained at higher levels and the necrosis rate was increased significantly in a time-dependent manner under acute thermal stress. However, under chronic thermal stress, the apoptosis and necrosis rates exhibited similar change trends: a rapid increase followed by a gradual decline and sustained at a relatively high level until the end of the experiment. The expressions of heat shock protein genes (HSP20 and HSP90), apoptosis-related genes (TRAF6, GRP78, NIX, and Casp-3), antioxidative-related genes (GST and MRP) and cellular detoxification-related genes (HbⅡ B, NOS-1, HO-1, and ENO-1) were upr-egulated significantly under both acute and chronic thermal stresses. These results demonstrated that the anti-apoptotic system, antioxidant defense system, cellular detoxification system, and heat shock proteins (HSPs) played vital roles for ark shells in response to thermal stress. As acute thermal stress can result in irreversible damage to marine molluscs, it is thus advised that chronic thermal stress should be used to select thermal-resistant ark shell strains.
Key words:    Scapharca broughtonii|thermal stress|apoptosis|necrosis|gene expression   
Received: 2022-03-11   Revised:
PDF (1760 KB) Free
Print this page
Add to favorites
Email this article to others
Articles by Desheng ZOU
Articles by Weian CAO
Articles by Guilong LIU
Articles by Junhao NING
Articles by Xia LU
Articles by Jinjing WANG
Articles by Min CHEN
Articles by Bo LIU
Articles by Jinsheng ZHANG
Articles by Chunde WANG
Bachère E, Mialhe E, Noël D et al.1995.Knowledge and research prospects in marine mollusc and crustacean immunology.Aquaculture, 132(1-2):17-32,
Bao Y B, Wang Q, Guo X M et al.2013.Structure and immune expression analysis of hemoglobin genes from the blood clam Tegillarca granosa.Genetics and Molecular Research, 12(3):3110-3123,
Brucet S, Boix D, Nathansen L W et al.2012.Effects of temperature, salinity and fish in structuring the macroinvertebrate community in shallow lakes:implications for effects of climate change.PLoS One, 7(2):e30877,
Burrows M T, Bates A E, Costello M J et al.2019.Ocean community warming responses explained by thermal affinities and temperature gradients.Nature Climate Change, 9(12):959-963,
Cheng C H, Guo Z X, Luo S W et al.2018.Effects of high temperature on biochemical parameters, oxidative stress, DNA damage and apoptosis of pufferfish (Takifugu obscurus).Ecotoxicology and Environmental Safety, 150:190-198,
Chinnadurai G, Vijayalingam S, Gibson S B.2008.BNIP3 subfamily BH3-only proteins:mitochondrial stress sensors in normal and pathological functions.Oncogene, 27 Suppl 1(S1):S114-S127,
Clark M S, Peck L S, Thyrring J.2021.Resilience in Greenland intertidal Mytilus:the hidden stress defense.Science of the Total Environment, 767:144366,
De La Fuente M, Victor V.2000.Anti-oxidants as modulators of immune function.Immunology & Cell Biology, 78(1):49-54,
Eriksson S P, Hernroth B, Baden S P.2013.Stress biology and immunology in Nephrops norvegicus.Advances in Marine Biology, 64:149-200,
Feder M E, Hofmann G E.1999.Heat-shock proteins, molecular chaperones, and the stress response:evolutionary and ecological physiology.Annual Review of Physiology, 61:243-282,
Free C M, Thorson J T, Pinsky M L et al.2019.Impacts of historical warming on marine fisheries production.Science, 363(6430):979-983,
Gao G D, Marin M, Feng M et al.2020.Drivers of marine heatwaves in the East China Sea and the South Yellow Sea in three consecutive summers during 2016-2018.Journal of Geophysical Research:Oceans, 125(8):e2020JC016518,
Geuken E, Buis C I, Visser D S et al.2005.Expression of heme oxygenase-1 in human livers before transplantation correlates with graft injury and function after transplantation.American Journal of Transplantation, 5(8):1875-1885,
Hachfi L, Simide R, Richard S et al.2012.Effect of water temperature increase on HO-1 expression in European sea bass (Dicentrarchus labrax L.) tissues.Cellular and Molecular Biology, Suppl 58:OL1752-6,
Hayes J D, Pulford D J.1995.The glutathione S-transferase supergene family:regulation of GST and the contribution of the lsoenzymes to cancer chemoprotection and drug resistance Part I.Critical Reviews in Biochemistry and Molecular Biology, 30(6):445-520,
Haynes V, Elfering S, Traaseth N et al.2004.Mitochondrial nitric-oxide synthase:enzyme expression, characterization, and regulation.Journal of Bioenergetics and Biomembranes, 36(4):341-346,
Hoegh-Guldberg O, Mumby P J, Hooten A J et al.2007.Coral reefs under rapid climate change and ocean acidification.Science, 318(5857):1737-1742,
IPCC.2013.Climate change 2013:the physical science basis.In:Stocker T F, Qin D, Plattner G K et al.eds.Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.Cambridge University Press, Cambridge.p.1535.
Jiang W W, Li J Q, Gao Y P et al.2016.Effects of temperature change on physiological and biochemical responses of Yesso scallop, Patinopecten yessoensis.Aquaculture, 451:463-472,
Kim M, Ahn I Y, Kim H et al.2009.Molecular characterization and induction of heat shock protein 90 in the Antarctic bivalve Laternula elliptica.Cell Stress and Chaperones, 14(4):363-370,
Konstantinov A S, Pushkar' V Y, Aver'yanova O V.2003.Effects of fluctuations of abiotic factors on the metabolism of some hydrobionts.Biology Bulletin of the Russian Academy of Sciences, 30(6):610-616,
Kumar G, Hummel K, Noebauer K et al.2018.Proteome analysis reveals a role of rainbow trout lymphoid organs during Yersinia ruckeri infection process.Scientific Reports, 8(1):13998,
Lesser M P.2006.Oxidative stress in marine environments:biochemistry and physiological ecology.Annual Review of Physiology, 68:253-278,
Li S K, Zhang Z, Li C B et al.2012.Molecular cloning and expression profiles of nitric oxide synthase (NOS) in mud crab Scylla paramamosain.Fish & Shellfish Immunology, 32(4):503-512,
Li Y F, Yang X Y, Cheng Z Y et al.2020.Near-future levels of ocean temperature weaken the byssus production and performance of the mussel Mytilus coruscus.Science of the Total Environment, 733:139347,
Lim H J, Kim B M, Hwang I J et al.2016.Thermal stress induces a distinct transcriptome profile in the Pacific oyster Crassostrea gigas.Comparative Biochemistry and Physiology Part D:Genomics and Proteomics, 19:62-70,
Lin Y, Mao F, Zhang X Y et al.2020.TRAF6 suppresses the apoptosis of hemocytes by activating pellino in Crassostrea hongkongensis.Developmental & Comparative Immunology, 103:103501,
Liu Z G, Wang H, Li Z M et al.2007.Upper incipient lethal temperature of Argopecten irradians concentricus Say.Journal of Fishery Sciences of China, 14(5):778-785.(in Chinese with English abstract)
Livak K J, Schmittgen T D.2001.Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method.Methods, 25(4):402-408,
Mejdoub Z, Fahde A, Loutfi M et al.2017.Oxidative stress responses of the mussel Mytilus galloprovincialis exposed to emissary's pollution in coastal areas of Casablanca.Ocean & Coastal Management, 136:95-103,
Meng X L, Liu P, Li J et al.2014.Physiological responses of swimming crab Portunus trituberculatus under cold acclimation:antioxidant defense and heat shock proteins.Aquaculture, 434: 11-17,
Naegel L C A, López-Rocha J A.2007.Effect of temperature on growth of the intertidal purple snail Plicopurpura pansa (Gould 1853) under laboratory conditions.Aquaculture Research, 38(5):493-497,
Ning J H, Chang Y Q, Liu W et al.2015.Stress responses to mild and acute temperature decrease for two strains of sea cucumber Apostichopus japonicus.Aquaculture, 448:552-563,
Ning J H, Zou D S, Lu X et al.2021.Transcriptomic analyses provide insights into the adaptive responses to heat stress in the ark shells, Scapharca subcrenata.Comparative Biochemistry and Physiology Part D:Genomics and Proteomics, 38:100813,
Nover L, Scharf K D.1997.Heat stress proteins and transcription factors.Cellular and Molecular Life Sciences CMLS, 53(1):80-103,
Pan X, Sheng X Q, Zhang W X et al.2022.Effects of short-term temperature changes on the physiology, biochemistry and feeding behaviour of the juvenile yellow seahorse-Hippopotamus kuda Bleeker.Aquaculture Research, 53(3):1084-1097,
Pechenik J A, Chaparro O R, Lazarus Z M et al.2020.Impact of short-term elevated temperature stress on winter-acclimated individuals of the marine gastropod Crepidula fornicata.Marine Environmental Research, 162:105180,
Qin Y P, Zhang Y H, Li X Y et al.2020.Characterization and functional analysis of a caspase 3 gene:evidence that ChCas 3 participates in the regulation of apoptosis in Crassostrea hongkongensis.Fish & Shellfish Immunology, 98:122-129,
Reddy R K, Mao C H, Baumeister P et al.2003.Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors-Role of ATP binding site in suppression of caspase-7 activation.Journal of Biological Chemistry, 278(23):20915-20924, 28200.
Sanford E, Kelly M W.2011.Local adaptation in marine invertebrates.Annual Review of Marine Science, 3:509-535,
Santana P A, Álvarez C A, Sáenz-Martínez D E et al.2021.New insight to the rol of α-enolase (Eno-1) as immunological marker in rainbow trout fry.Developmental & Comparative Immunology, 123:104163,
Schutte B, Nuydens R, Geerts H et al.1998.Annexin V binding assay as a tool to measure apoptosis in differentiated neuronal cells.Journal of Neuroscience Methods, 86(1):63-69,
Srivastava P.2002.Roles of heat-shock proteins in innate and adaptive immunity.Nature Reviews Immunology, 2(3):185-194,
Stillman J H.2003.Acclimation capacity underlies susceptibility to climate change.Science, 301(5629):65,
Wang Y, Wu Z H, Li H Y et al.2013.Analysis and evaluation of nutrition composition in soft tissue of Anadara uropygimelana.Progress in Fishery Sciences, 34(1):133-139.(in Chinese with English abstract)
Wang Z L, Qu Y X, Zhuo X L et al.2019.Investigating the physiological responses of Pacific white shrimp Litopenaeus vannamei to acute cold-stress.PeerJ, 7:e7381,
Yampolsky L Y, Schaer T M M, Ebert D.2014.Adaptive phenotypic plasticity and local adaptation for temperature tolerance in freshwater zooplankton.Proceedings of the Royal Society B:Biological Sciences, 281(1776):20132744,
Yang C Y, Gao Q, Liu C et al.2017.The transcriptional response of the Pacific oyster Crassostrea gigas against acute heat stress.Fish & Shellfish Immunology, 68:132-143,
Zhang G F, Fang X D, Guo X M et al.2012.The oyster genome reveals stress adaptation and complexity of shell formation.Nature, 490(7418):49-54,
Zhou Z, Liu Z Q, Wang L G et al.2019.Oxidative stress, apoptosis activation and symbiosis disruption in giant clam Tridacna crocea under high temperature.Fish & Shellfish Immunology, 84:451-457,
Zou D S, Ning J H, Lu X et al.2021.Physiological and transcriptional responses to acute and chronic thermal stress in the ark shell Scapharca subcrenata.Frontiers in Marine Science, 8:739662,
Copyright © Haiyang Xuebao