Cite this paper:
Xinming GAO, Haiyan YANG, Daojun TANG, Chen DU, Shan JIN, Congcong HOU, Chundan ZHANG, Junquan ZHU, Jianping WANG. Physiological and histological responses of Phascolosoma esculenta (Sipuncula: Phascolosomatidea) to acute heat stress[J]. Journal of Oceanology and Limnology, 2022, 40(2): 643-655

Physiological and histological responses of Phascolosoma esculenta (Sipuncula: Phascolosomatidea) to acute heat stress

Xinming GAO1, Haiyan YANG1, Daojun TANG1, Chen DU1, Shan JIN1, Congcong HOU1, Chundan ZHANG1, Junquan ZHU1, Jianping WANG2
1 Key Laboratory of Applied Marine Biotechnology by the Ministry of Education, School of Marine Sciences, Ningbo University, Ningbo 315211, China;
2 Ningbo Academy of Oceanology and Fisheries, Ningbo 315012, China
Abstract:
Temperature is an important factor affecting the growth, development, and survival of organisms. The effects of temperature stress on aquatic organisms have received increasing attention, as these organisms are mostly poikilotherms and their body temperature are directly corresponding changes with ambient temperature, resulting in they are easily exposed in temperature stress. However, little is known about the effects of high temperature on Sipuncula. In this study, we investigated the effects of acute heat stress on malondialdehyde (MDA) concentration, the activities of antioxidant (superoxide dismutase and glutathione peroxidase) and immunity-related (acidic and alkaline phosphatase) enzymes, heat shock protein 70 (hsp70) and hsp90 gene expression, and the histological structure of the sipunculid Phascolosoma esculenta. Within the coelom fluid, the MDA concentration and all detected antioxidant enzyme activities increased during high temperature stress; significant increases were also observed here and in the intestine in the hsp70 and hsp90 mRNA expression levels. These results indicated that acute heat stress caused oxidative stress; antioxidants and heat shock proteins probably act to protect P. esculenta against oxidative damage, constituting part of its physiological mechanism for adaptation to high temperatures. In addition, the increased activity of the acidic and alkaline phosphatases indicated effects on its nonspecific immune system. Furthermore, damaged tissue structures were observed in the body wall, retractor muscle, intestine, and nephridium after 96 h of 40-℃ stress. The damaged cells of these tissues showed obvious condensed chromatin around the nuclear membrane. This histological damage suggests that heat stress could affect movement, food absorption, digestion, and excretion in P. esculenta. These results elucidate the effects of temperature stress on P. esculenta and its physiological response mechanisms and provide practical indicators for assessing heat stress status and determining suitable culture temperatures for P. esculenta.
Key words:    heat stress|oxidation stress|enzyme activity|heat shock proteins|nonspecific immunity|histological damage   
Received: 2021-01-11   Revised:
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Articles by Xinming GAO
Articles by Haiyan YANG
Articles by Daojun TANG
Articles by Chen DU
Articles by Shan JIN
Articles by Congcong HOU
Articles by Chundan ZHANG
Articles by Junquan ZHU
Articles by Jianping WANG
References:
An M I, Choi C Y.2010.Activity of antioxidant enzymes and physiological responses in ark shell, Scapharca broughtonii, exposed to thermal and osmotic stress:effects on hemolymph and biochemical parameters.Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 155(1):34-42, https://doi.org/10.1016/j.cbpb.2009.09.008.
Beere H M, Green D R.2001.Stress management-heat shock protein-70 and the regulation of apoptosis.Trends in Cell Biology, 11(1):6-10, https://doi.org/10.1016/S0962-8924(00) 01874-2.
Chen B, Feder M E, Kang L.2018.Evolution of heat-shock protein expression underlying adaptive responses to environmental stress.Molecular Ecology, 27(15):3040-3054, https://doi.org/10.1111/mec.14769.
Chen M Y, Yang H S, Delaporte M, Zhao S J, Xing K.2007a.Immune responses of the scallop Chlamys farreri after air exposure to different temperatures.Journal of Experimental Marine Biology and Ecology, 345(1):52-60, https://doi.org/10.1016/j.jembe.2007.01.007.
Chen M Y, Yang H S, Delaporte M, Zhao S J.2007b.Immune condition of Chlamys farreri in response to acute temperature challenge.Aquaculture, 271(1-4):479-487, https://doi.org/10.1016/j.aquaculture.2007.04.051.
Cheng C H, Yang F F, Liao S A, Miao Y T, Ye C X, Wang A L, Tan J W, Chen X Y.2015.High temperature induces apoptosis and oxidative stress in pufferfish (Takifugu obscurus) blood cells.Journal of Thermal Biology, 53:172-179, https://doi.org/10.1016/j.jtherbio.2015.08.002.
Downs C A, Fauth J E, Woodley C M.2001.Assessing the health of grass shrimp (Palaemonetes pugio) exposed to natural and anthropogenic stressors:a molecular biomarker system.Marine Biotechnology, 3(4):380-397, https://doi.org/10.1007/s10126-001-0008-3.
Farmer E E, Muelle M J.2013.ROS-mediated lipid peroxidation and RES-activated signaling.Annual Review of Plant Biology, 64:429-450, https://doi.org/10.1146/annurev-arplant-050312-120132.
Fu D K, Chen J H, Zhang Y, Yu Z N.2011.Cloning and expression of a heat shock protein (HSP) 90 gene in the haemocytes of Crassostrea hongkongensis under osmotic stress and bacterial challenge.Fish & Shellfish Immunology, 31(1):118-125, https://doi.org/10.1016/j.fsi.2011.04.011.
Halliwell B.1999.Antioxidant defence mechanisms:from the beginning to the end (of the beginning).Free Radical Research, 31(4):261-272, https://doi.org/10.1080/10715769900300841.
Hong M L, Chen L Q, Gu S Y, Liu C, Zhang L, Li E C.2007.Effect of temperature change on immunochemical indexes of Eriocheir sinensis.Chinese Journal of Applied and Environmental Biology, 13(6):818-822. (in Chinese with English abstract)
Hu M H, Li L S, Sui Y M, Li Y M, Wang Y J, Lu W Q, Dupont S.2015.Effect of pH and temperature on antioxidant responses of the thick shell mussel Mytilus coruscus.Fish& Shellfish Immunology, 46(2):573-583, https://doi.org/10.1016/j.fsi.2015.07.025.
Jiang W W, Fang J G, Li J Q, Jiang Z J, Mao Y Z, Du M R, Gao Z K, Chen Q L.2017.Effects of temperature change on physiological and biochemical activities of Haliotis discus hannai Ino.Journal of Fishery Sciences of China, 24(2):220-230. (in Chinese with English abstract)
Jiang W W, Li J Q, Gao Y P, Mao Y Z, Jiang Z J, Du M R, Zhang Y, Fang J G.2016.Effects of temperature change on physiological and biochemical responses of Yesso scallop, Patinopecten yessoensis.Aquaculture, 451:463-472, https://doi.org/10.1016/j.aquaculture.2015.10.012.
Kashiwagi A, Kashiwagi K, Takase M, Hanada H, Nakamura M.1997.Comparison of catalase in diploid and haploid Rana rugosa using heat and chemical inactivation techniques.Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 118(3):499-503, https://doi.org/10.1016/S0305-0491(97) 00216-2.
Kiang J G, Tsokos G C.1998.Heat shock protein 70 kDa:molecular biology, biochemistry, and physiology.Pharmacology & Therapeutics, 80(2):183-201, https://doi.org/10.1016/S0163-7258(98) 00028-X.
Lan G B, Yang S F, Xie T S, Shi D S.2007.Advance in phyletic studies of the phylum Sipuncula.Guangxi Sciences, 14(2):186-192. (in Chinese with English abstract)
Lei S Y, Lu M M, Ding L F, Zhu J Q.2013.The morphology of the digestive tract of Phascoloma esculenta.Journal of Biology, 30(2):33-36, 39. (in Chinese with English abstract)
Liu S L, Jiang X L, Hu X K, Gong J, Hwang H, Mai K S.2004.Effects of temperature on non-specific immune parameters in two scallop species:Argopecten irradians (Lamarck 1819) and Chlamys farreri (Jones & Preston 1904).Aquaculture Research, 35(7):678-682, https://doi.org/10.1111/j.1365-2109.2004.01065.x.
Liu Y F, Ma D Y, Zhao C Y, Wang W Q, Zhang X L, Liu X, Liu Y, Xiao Z Z, Xu S H, Xiao Y S, Liu Q H.2014.Histological and enzymatic responses of Japanese flounder (Paralichthys olivaceus) and its hybrids (P.olivaceus♀×P.dentatus♂) to chronic heat stress.Fish Physiology and Biochemistry, 40(4):1031-1041, https://doi.org/10.1007/s10695-013-9903-6.
Long L L, Sheng Z, Lu M M, Ding L F, Zhu J Q.2014.Structural features of musculature in the nephridium of Phascolosoma esculenta.Journal of Biology, 31(2):9-12. (in Chinese with English abstract)
Lu X, Wang C, Liu B Z.2015.The role of Cu/Zn-SOD and Mn-SOD in the immune response to oxidative stress and pathogen challenge in the clam Meretrix meretrix.Fish & Shellfish Immunology, 42(1):58-65, https://doi.org/10.1016/j.fsi.2014.10.027.
Madeira D, Mendonça V, Dias M, Roma J, Costa P M, Larguinho M, Vinagre C, Diniz M S.2015.Physiological, cellular and biochemical thermal stress response of intertidal shrimps with different vertical distributions:Palaemon elegans and Palaemon serratus.Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 183:107-115, https://doi.org/10.1016/j.cbpa.2014.12.039.
Martins Y S, Melo R M C, Campos-Junior P H A, Santos J C E, Luz R K, Rizzo E, Bazzoli N.2014.Salinity and temperature variations reflecting on cellular PCNA, IGF-I and II expressions, body growth and muscle cellularity of a freshwater fish larvae.General and Comparative Endocrinology, 202:50-58, https://doi.org/10.1016/j.ygcen.2014.03.047.
Meng X L, Liu P, Li J, Gao B Q, Chen P.2014.Physiological responses of swimming crab Portunus trituberculatus under cold acclimation:antioxidant defense and heat shock proteins.Aquaculture, 434:11-17, https://doi.org/10.1016/j.aquaculture.2014.07.021.
Mosser D D, Caron A W, Bourget L, Denis-Larose C, Massie B.1997.Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis.Molecular and Cellular Biology, 17(9):5317-5327, https://doi.org/10.1128/MCB.17.9.5317.
Park M S, Jo P G, Choi Y K, An K W, Choi C Y.2009.Characterization and mRNA expression of Mn-SOD and physiological responses to stresses in the Pacific oyster Crassostrea gigas.Marine Biology Research, 5(5):453-463, https://doi.org/10.1080/17451000802626554.
Peng G G, Zhao W, Shi Z G, Chen H R, Liu Y, Wei J, Gao F Y.2016.Cloning HSP70 and HSP90 genes of kaluga (Huso dauricus) and the effects of temperature and salinity stress on their gene expression.Cell Stress & Chaperones, 21(2):349-359, https://doi.org/10.1007/s12192-015-0665-1.
Qiang J, Yang H, Wang H, Xu P, He J.2012.The effect of acute temperature stress on biochemical indices and expression of liver Hsp70 mRNA in gift nile tilapia juveniles(Oreochromis niloticus).Oceanologia et Limnologia Sinica, 43(5):943-953. (in Chinese with English abstract)
Ravagnan L, Gurbuxani S, Susin S A, Maisse C, Daugas E, Zamzami N, Mak T, Jäättelä M, Penninger J M, Garrido C, Kroemer G.2001.Heat-shock protein 70 antagonizes apoptosis-inducing factor.Nature Cell Biology, 3(9):839-843, https://doi.org/10.1038/ncb0901-839.
Selong J H, McMahon T E, Zale A V, Barrows F T.2001.Effect of temperature on growth and survival of bull trout, with application of an improved method for determining thermal tolerance in fishes.Transactions of the American Fisheries Society, 130(6):1026-1037, https://doi.org/10.1577/1548-8659(2001) 130<1026:EOTOGA>2.0.CO;2.
Simon H U, Haj-Yehia A, Levi-Schaffer F.2000.Role of reactive oxygen species (ROS) in apoptosis induction.Apoptosis, 5(5):415-418, https://doi.org/10.1023/A:1009616228304.
Spallholz J E.1990.Selenium and glutathione peroxidase:essential nutrient and antioxidant component of the immune system.In:Bendich A, Phillips M, Tengerdy R P eds.Advances in Experimental Medicine and Biology.
Springer, Boston.p.145-158, https://doi.org/10.1007/978-1-4613-0553-8_12.
Su X R, Du L L, Li Y Y, Li Y, Zhou J, Li T W.2010.Cloning and expression of HSP70 gene of sipuncula Phascolosoma esculenta.Fish & Shellfish Immunology, 28(3):461-466, https://doi.org/10.1016/j.fsi.2009.12.014.
Van Cruchten S, Van den Broeck W.2002.Morphological and biochemical aspects of apoptosis, oncosis and necrosis.Anatomia Histologia Embryologia, 31(4):214-223, https://doi.org/10.1046/j.1439-0264.2002.00398.x.
Verlecar X N, Jena K B, Chainy G B N.2007.Biochemical markers of oxidative stress in Perna viridis exposed to mercury and temperature.Chemico-Biological Interactions, 167(3):219-226, https://doi.org/10.1016/j.cbi.2007.01.018.
Wang T S, Zhou X, Zhao Z Y, Xu Z H, Shui Y.2012.Activity of immunity-related enzymes under different temperature in Procambarus clarkii.Jiangsu Agricultural Sciences, 40(12):239-241. (in Chinese)
Xu D X, Sun L N, Liu S L, Zhang L B, Yang H S.2015.Histological, ultrastructural and heat shock protein 70(HSP70) responses to heat stress in the sea cucumber Apostichopus japonicus.Fish & Shellfish Immunology, 45(2):321-326, https://doi.org/10.1016/j.fsi.2015.04.015.
Yan J, Liang X, Zhang Y, Li Y, Cao X J, Gao J.2017.Cloning of three heat shock protein genes (HSP70, HSP90α and HSP90β) and their expressions in response to thermal stress in loach (Misgurnus anguillicaudatus) fed with different levels of vitamin C.Fish & Shellfish Immunology, 66:103-111, https://doi.org/10.1016/j.fsi.2017.05.023.
Zhang C N, Tian H Y, Li X F, Zhu J, Cai D S, Xu C, Wang F, Zhang D D, Liu W B.2014.The effects of fructooligosaccharide on the immune response, antioxidant capability and HSP70 and HSP90 expressions in blunt snout bream (Megalobrama amblycephala Yih) under high heat stress.Aquaculture, 433:458-466, https://doi.org/10.1016/j.aquaculture.2014.07.007.
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