Cite this paper:
Xuxu LIU, Xiumei ZHANG, Yihang WANG. Effects of temperature on the respiratory metabolism, feeding and expression of three heat shock protein genes in Anadara broughtonii[J]. Journal of Oceanology and Limnology, 2021, 39(2): 755-769

Effects of temperature on the respiratory metabolism, feeding and expression of three heat shock protein genes in Anadara broughtonii

Xuxu LIU1, Xiumei ZHANG2,3, Yihang WANG1
1 Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao 266003, China;
2 Fisheries College, Zhejiang Ocean University, Zhoushan 316022, China;
3 Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China
Abstract:
Anadara broughtonii is one of the main commercially important species of shellfish in northern China. A. broughtonii lives in relatively stable subtidal zone where the clam could respond to environmental changes with minimum energy. Therefore, slight fluctuations in water environment may have a great impact on physiological processes such as feeding and metabolism. Large-scale mortality often occurs during the intermediate rearing processes, and high temperatures in summer are considered the leading cause of mortality. To understand the physiological and molecular response patterns of A. broughtonii at high temperatures and to estimate the appropriate metabolism temperature for A. broughtonii, the effects of temperature on the respiratory metabolism and food intake at different growth stages were studied. The response patterns of heat shock protein genes to heat stress and post-stress recovery were also explored. Results show that the temperature and growth stage of A. broughtonii were two important factors affecting metabolism and feeding. The optimum temperature for feeding and physiological activities in each shell-length group was 24℃. The temperature at which the peak metabolic rate occurred in each shell-length group increased with the increase in shell length. With the increase in heat stress, the expression of three heat shock protein genes (Abhsp60, Abhsp70, and Abhsp90) in the tissues of two size groups of A. broughtonii increased significantly when temperature was above 24℃ and reached a peak at 30℃. After heat shock at 30℃ for 2 h, the expression of the three heat shock protein genes rapidly increased, peaked at 2 h after the heat shock, and then gradually decreased to the level of the control group at 48 h after the heat shock. The three heat shock protein genes respond rapidly to heat stress and can be used as indicators to the cellular stress response in A. broughtonii under an environmental stress.
Key words:    Anadara broughtonii|temperature|oxygen consumption rate|clearance rate|heat shock protein gene   
Received: 2019-11-30   Revised: 2020-01-04
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References:
Albentosa M, Beiras R, Camacho A P. 1994. Determination of optimal thermal conditions for growth of clam (Venerupis pullastra) seed. Aquaculture, 126(3-4):315-328, https://doi.org/10.1016/0044-8486(94)90048-5.
Aldridge D W, Payne B S, Miller A C. 1995. Oxygen consumption, nitrogenous excretion, and filtration rates of Dreissena polymorpha at acclimation temperatures between 20 and 32℃. Canadian Journal of Fisheries and Aquatic Sciences, 52(8):1 761-1 767, https://doi.org/10.1139/f95-768.
An M I, An K W, Choi C Y. 2009. Changes in antioxidant enzyme activity and physiological responses to cadmium and tributyltin exposure in the ark shell, Scapharca broughtonii. Molecular and Cellular Toxicology, 5(4):273-282.
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.
Anestis A, Pörtner H O, Lazou A, Michaelidis B. 2008.Metabolic and molecular stress responses of sublittoral bearded horse mussel Modiolus barbatus to warming sea water:implications for vertical zonation. Journal of Experimental Biology, 211(17):2 889-2 898, https://doi.org/10.1242/jeb.016782.
Bougrier S, Geairon P, Deslous-Paoli J M, Bacher C, Jonquières G. 1995. Allometric relationships and effects of temperature on clearance and oxygen consumption rates of Crassostrea gigas (Thunberg). Aquaculture, 134(1-2):143-154, https://doi.org/10.1016/0044-8486(95)00036-2.
Broom M J. 1985. The biology and culture of marine bivalve molluscs of the genus Anadara. International Center for Living Aquatic Resources Management, Manila, Philippines.
Brown A, Heilmayer O, Thatje S. 2010. Metabolic rate and growth in the temperate bivalve Mercenaria mercenaria at a biogeographical limit, from the English Channel.Journal of the Marine Biological Association of the United Kingdom, 90(5):1 019-1 023, https://doi.org/10.1017/S0025315409991470.
Brun N T, Bricelj V M, MacRae T H, Ross N W. 2008. Heat shock protein responses in thermally stressed bay scallops, Argopecten irradians, and sea scallops, Placopecten magellanicus. Journal of Experimental Marine Biology and Ecology, 358(2):151-62, https://doi.org/10.1016/j.jembe.2008.02.006.
Cho E S, Jung C G, Shin Y K. 2009. Genetic responses of the ark shell Scapharca broughtonii Schrenck to environmental shock:high temperatures and long exposure times. Ocean Science Journal, 44(2):61-67, https://doi.org/10.1007/s12601-009-0007-2.
Connolly M H, Hall B K. 2008. Embryonic heat shock reveals latent hsp90 translation in zebrafish (Danio rerio).International Journal of Developmental Biology, 52:71-79. https://doi.org/10.1387/ijdb.062241mc.
Conover R J. 1966. Factors affecting the assimilation of organic matter by zooplankton and the question of superfluous feeding. Limnology and Oceanography, 11(3):346-354, https://doi.org/10.4319/lo.1966.11.3.0346.
Coughlan J. 1969. The estimation of filtering rate from the clearance of suspensions. Marine Biology, 2(4):356-358, https://doi.org/10.1007/BF00355716.
Dong B, Xue Q Z, Li J. 2000. Environmental factors affecting the feeding physiological ecology of manila clam, Ruditapes philippinarum (Adams et reeve, 1850). Oceanologia et Limnologia Sinica, 31(6):636-642. (in Chinese with English abstract)
Elvin D W, Gonor J J. 1979. The thermal regime of an intertidal Mytilus californianus Conrad population on the central Oregon coast. Journal of Experimental Marine Biology andEcology,39(3):265-279, https://doi.org/10.1016/0022-0981(79)90130-8.
Famme P, Riisgård H U, Jørgensen C B. 1986. On direct measurement of pumping rates in the mussel Mytilus edulis. Marine Biology, 92(3):323-327, https://doi.org/10.1007/BF00392672.
Fan C Y, Lee S, Cyr D M. 2003. Mechanisms for regulation of Hsp70 function by Hsp40. Cell Stress and Chaperones, 8(4):309-316, https://doi.org/10.1379/1466-1268(2003)008<0309:MFROHF>2.0.CO;2.
Fan J X. 2010. Studies on Metabolism of Meretrix meretrix Linnaeus. Ningbo University, Ningbo, China. (in Chinese with English abstract)
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(1):243-282, https://doi.org/10.1146/annurev.physiol.61.1.243.
Fink J K, Hedera P. 1999. Hereditary spastic paraplegia:genetic heterogeneity and genotype-phenotype correlation. Seminars in Neurology, 19(3):301-309, https://doi.org/10.1055/s-2008-1040846.
Georgopoulos C, Welch W J. 1993. Role of the major heat shock proteins as molecular chaperones. Annual Review of Cell Biology, 9(1):601-634, https://doi.org/10.1146/annurev.cb.09.110193.003125.
Gosling E. 2015. Marine Bivalve Molluscs. 2nd edn. John Wiley & Sons, Chichester, UK, Goulletquer P, Wolowicz M, Latala A, Brown C, Cragg S. 2004. Application of a micro-respirometric volumetric method to respiratory measurements of larvae of the Pacific oyster Crassostrea gigas. Aquatic Living Resources, 17(2):195-200, https://doi.org/10.1051/alr:2004018.
Harris S F, Shiau A K, Agard D A. 2004. The crystal structure of the carboxy-terminal dimerization domain of htpG, the Escherichia coli Hsp90, reveals a potential substrate binding site. Structure, 12(6):1 087-1 097, https://doi.org/10.1016/j.str.2004.03.020.
Hartl F U, Hayer-Hartl M. 2002. Molecular chaperones in the cytosol:from nascent chain to folded protein. Science, 295(5561):1 852-1 858, https://doi.org/10.1126/science.1068408.
Hawkins A J S, Smith R F M, Bayne B L, Héral M. 1996. Novel observations underlying the fast growth of suspension-feeding shellfish in turbid environments:Mytilus edulis. Marine Ecology Progress Series, 131:179-190, https://doi.org/10.3354/meps131179.
Huang X W, Wang T F, Ye Z W, Han G D, Dong Y W. 2015. Temperature relations of aerial and aquatic physiological performance in a mid-intertidal limpet Cellana toreuma:adaptation to rapid changes in thermal stress during emersion. Integrative Zoology, 10(1):159-170, https://doi.org/10.1111/1749-4877.12107.
Husmann G, Abele D, Rosenstiel P, Clark M S, Kraemer L, Philipp E E R. 2014. Age-dependent expression of stress and antimicrobial genes in the hemocytes and siphon tissue of the Antarctic bivalve, Laternula elliptica, exposed to injury and starvation. Cell Stress and Chaperones, 19(1):15-32, https://doi.org/10.1007/s12192-013-0431-1.
Hutchinson S, Hawkins L E. 1992. Quantification of the physiological responses of the European flat oyster Ostrea edulis L. to temperature and salinity. Journal of Molluscan Studies, 58(2):215-226, https://doi.org/10.1093/mollus/58.2.215.
Inoue T, Yamamuro M. 2000. Respiration and ingestion rates of the filter-feeding bivalve Musculista senhousia:implications for water-quality control. Journal of Marine Systems, 26(2):183-192, https://doi.org/10.1016/S0924-7963(00)00053-1
Itoh H, Komatsuda A, Ohtani H, Wakui H, Imai H, Sawada K, Otaka M, Ogura M, Suzuki A, Hamada F. 2002. Mammalian HSP60 is quickly sorted into the mitochondria under conditions of dehydration. European Journal of Biochemistry, 269(23):5 931-5 938, https://doi.org/10.1046/j.1432-1033.2002.03317.x
Jansen J M, Hummel H, Bonga S W. 2009. The respiratory capacity of marine mussels (Mytilus galloprovincialis) in relation to the high temperature threshold. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 153(4):399-402, https://doi.org/10.1016/j.cbpa.2009.03.013.
Jiang L M. 2012. Study on the Metabolic Physioiogy and Ingestive of Trachycardium flavum and its Energy Budget. Guangdong Ocean University, Guangdong, China. (in Chinese with English abstract)
Jones H D, Richards O G, Southern T A. 1992. Gill dimensions, water pumping rate and body size in the mussel Mytilus edulis L. Journal of Experimental Marine Biology and Ecology, 155(2):213-237, https://doi.org/10.1016/0022-0981(92)90064-H.
Jørgensen C B, Larsen P S, Riisgård H U. 1990. Effects of temperature on the mussel pump. Marine Ecology Progress Series, 64:89-97, https://doi.org/10.3354/meps064089.
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.
Kim B H, Min K S, Lee S J, Park K Y, An C M, Min B H. 2006. Effect of temperature on induced sexual maturation of the ark shell, Scapharca broughtonii (Schrenck) broodstock. The Korean Journal of Malacology, 22(2):176-182.
Kim B H, Shin Y K, Park K Y, Choi N J, Oh B S, Min B H. 2008. Growth and survival of the spat of arkshell, Scapharca broughtonii in intermediate culture with different shape of protective net and type of preventive net of spat loss. The Korean Journal of Malacology, 24(2):131-136.
Kim J B, Lee S Y, Jung C G, Jung C S, Son S G. 2007. The effects of the spat planting time and environmental factors in the arkshell, Scapharca broughtonii Schrenck culture. Journal of Aquaculture, 20(1):31-40.
Kim J D, Cheong S C, Kang H W. 1980. Studies on the artificial mass seed production of the ark shell Anadara broughtonii(Schrenck). II. On the intermediate culture of the artificial seed. Acta chimica, 25:45-53.
Krebs R A, Feder M E. 1997. Deleterious consequences of Hsp70 overexpression in Drosphilla melanogaster larvae. Cell Stress&Chaperones,2(1):60, https://doi.org/10.1379/1466-1268(1997)002<0060:DCOHOI>2.3.CO;2.
Kregel K C. 2002. Invited review:heat shock proteins:modifying factors in physiological stress responses and acquired thermotolerance. Journal of Applied Physiology, 92(5):2 177-2 186, https://doi.org/10.1152/japplphysiol.01267.2001.
Laing I, Utting S D, Kilada R W S. 1987. Interactive effect of diet and temperature on the growth of juvenile clams. Journal of Experimental Marine Biology and Ecology, 113(1):23-38, https://doi.org/10.1016/0022-0981(87)90080-3.
Lee J S, Cho H S, Jin Y G, Park J J, Shin Y K. 2009. Reproductive disrupting effect of organotin compound in the ark shell, Scapharca broughtonii (Bivalvia:Arcidae). Animal Cells and Systems, 13(2):223-227, https://doi.org/10.1080/19768354.2009.9647214.
Min K S, Kim B H, Lee S J, Park K Y, Kim B G. 2004. Intermediate culture of the spat of arkshell, Scapharca broughtonii in summer. The Korean Journal of Malacology, 20(2):125-130.
Morimoto R I, Santoro M G. 1998. Stress-inducible responses and heat shock proteins:new pharmacologic targets for cytoprotection. Nature Biotechnology, 16(9):833-838, https://doi.org/10.1038/nbt0998-833.
Navarro J M, Gonzalez C M. 1998. Physiological responses of the Chilean scallop Argopecten purpuratus to decreasing salinities. Aquaculture, 167(3-4):315-327, https://doi.org/10.1016/S0044-8486(98)00310-X.
Navarro J M, Leiva G E, Martinez G, Aguilera C. 2000. Interactive effects of diet and temperature on the scope for growth of the scallop Argopecten purpuratus during reproductive conditioning. Journal of Experimental Marine Biology and Ecology, 247(1):67-83, https://doi.org/10.1016/S0022-0981(00)00140-4.
Nollen E A A, Morimoto R I. 2002. Chaperoning signaling pathways:molecular chaperones as stress-sensing ‘heat shock’ proteins. Journal of Cell Science, 115(14):2 809-2 816.
Palmisano A N, Winton J R, Dickhoff W W. 1999. Sequence features and phylogenetic analysis of the stress protein hsp90α in chinook salmon (Oncorhynchus tshawytscha), a poikilothermic vertebrate. Biochemical and Biophysical Research Communications, 258(3):784-791, https://doi.org/10.1006/bbrc.1999.0707.
Pan L Q, Fan D P, Ma S, Huang S L. 2002. Influence of environmental factors on the filtration rate of Sinonovacula constricta. Journal of Fisheries of China, 26(3):226-230.(in Chinese with English abstract)
Peck L S, Conway L Z. 2000. The myth of metabolic cold adaptation:oxygen consumption in stenothermal Antarctic bivalves. Geological Society, London, Special Publications, 177(1):441-450, https://doi.org/10.1144/GSL.SP.2000.177.01.29.
Peck L S, Morley S A, Pörtner H O, Clark M S. 2007. Thermal limits of burrowing capacity are linked to oxygen availability and size in the Antarctic clam Laternula elliptica. Oecologia, 154(3):479-484, https://doi.org/10.1007/s00442-007-0858-0.
Peck L S, Pörtner H O, Hardewig I. 2002. Metabolic demand, oxygen supply, and critical temperatures in the Antarctic bivalve Laternula elliptica. Physiological and Biochemical Zoology, 75(2):123-133, https://doi.org/10.1086/340990.
Philipp E E R, Abele D. 2010. Masters of longevity:lessons from long-lived bivalves:a mini-review. Gerontology, 56(1):55-65, https://doi.org/10.1159/000221004.
Philipp E, Brey T, Pörtner H O, Abele D. 2005. Chronological and physiological ageing in a polar and a temperate mud clam. Mechanisms of ageing and Development, 126(5):598-609, https://doi.org/10.1016/j.mad.2004.12.003.
Philipp E, Husmann G, Abele D. 2011. The impact of sediment deposition and iceberg scour on the Antarctic soft shell clam Laternula elliptica at King George Island, Antarctica.Antarctic Science, 23(2):127-138, https://doi.org/10.1017/S0954102010000970.
Qiang J, Yang H, Wang H, Wu 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)
Riisgård H U. 2001. On measurement of filtration rate in bivalves-the stony road to reliable data:review and interpretation. Marine Ecology Progress Series, 211:275-291, https://doi.org/10.3354/meps211275.
Rodhouse P G. 1978. Energy transformations by the oyster Ostrea edulis L. in a temperate estuary. Journal of Experimental Marine Biology and Ecology, 34(1):1-22, https://doi.org/10.1016/0022-0981(78)90053-9.
Sarge K D, Murphy S P, Morimoto R I. 1993. Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Molecular and Cellular Biology, 13(3):1392-1407. https://doi.org/10.1128/MCB.13.3.1392.
Schulte E H. 1975. Influence of algal concentration and temperature on the filtration rate of Mytilus edulis. Marine Biology,30(4):331-341, https://doi.org/10.1007/BF00390638.
Sedova L G, Kalinina M V, Sokolenko D A, Rachkov V I. 2012. Resources and habitat conditions of the bivalve mollusk Anadara broughtonii in the northern part of Amur Bay (Sea of Japan). Oceanology, 52(4):488-494, https://doi.org/10.1134/S000143701204008X.
Shin Y K, Kim B H, Choi N J, Jung C J, Park M W. 2008. Influence of temperature, salinity and hypoxia on survival and metabolic rate in the ark shell, Scapharca broughtonii. The Korean Journal of Malacology, 24(1):59-66.
Shin Y K, Kim B H, Oh B S, Jung C G, Sohn S G, Lee J S. 2006. Physiological responses of the ark shell Scapharca broughtonii (Bivalvia:Arcidae) to decreases in salinity. Fisheries and Aquatic Sciences, 9(4):153-159, https://doi.org/10.5657/fas.2006.9.4.153.
Somero G N. 2010. The physiology of climate change:how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. Journal of Experimental Biology, 213(6):912-920, https://doi.org/10.1242/jeb.037473.
Suja N. 2007. Metabolism in the baby clam Marcia opima. Journal of Marine Biological Association of India, 49(1):100-102.
Sukhotin A A, Lajus D L, Lesin P A. 2003. Influence of age and size on pumping activity and stress resistance in the marine bivalve Mytilus edulis L. Journal of Experimental Marine Biology and Ecology, 284(1-2):129-144, https://doi.org/10.1016/S0022-0981(02)00497-5.
Tang Q S, Qiu X Y, Wang J, Guo X W, Yang A G. 1994. Resource enhancement of arkshell (Scapharca (Anadara) broughtonii) in Shandong offshore waters. Chinese Journal of Applied Ecology, 5(4):396-402. (in Chinese with English abstract)
Underwood A J. 1997. Experiments in Ecology:their Logical Design and Interpretation Using Analysis of Variance. Cambridge University Press, USA, https://doi.org/10.1017/CBO9780511806407.
Viant M R, Werner I, Rosenblum E S, Gantner A S, Tjeerdema R S, Johnson M L. 2003. Correlation between heat-shock protein induction and reduced metabolic condition in juvenile steelhead trout (Oncorhynchus mykiss) chronically exposed to elevated temperature. Fish Physiology and Biochemistry, 29(2):159-171, https://doi.org/10.1023/B:FISH.0000035938.92027.81.
Wang J S, Wei Y H, Li X M, Cao H, Xu M Q, Dai J Y. 2007. The identification of heat shock protein genes in goldfish(Carassius auratus) and their expression in a complex environment in Gaobeidian Lake, Beijing, China. Comparative Biochemistry and Physiology Part C:Toxicology & Pharmacology, 145(3):350-362, https://doi.org/10.1016/j.cbpc.2007.01.018.
Watanabe T, Shibata K, Kera Y, Takahashi S, Yamada R. 2005. Effects of hypoxic and osmotic stress on the free D-aspartate level in the muscle of blood shell Scapharca broughtonii. Amino Acids, 28(3):291-296, https://doi.org/10.1007/s00726-005-0188-7.
Widdows J, Staff F. 2006. Biological effects of contaminants:measurement of scope for growth in mussels. Ices Techniques in Marine Environmental Sciences, 40:1-34.https://doi.org/10.17895/ices.pub.5064.
Widdows J. 1978. Combined effects of body size, food concentration and season on the physiology of Mytilus edulis. Journal of the Marine Biological Association of the United Kingdom, 58(1):109-124, https://doi.org/10.1017/S0025315400024449.
Winter J E. 1969. Über den Einfluß der Nahrungskonzentration und anderer Faktoren auf Filtrierleistung und Nahrungsausnutzung der Muscheln Arctica islandica und Modiolus modiolus. Marine Biology, 4(2):87-135, https://doi.org/10.1007/BF00347037.
Wu G H, Chen P J, Jiang R S, Yang S Y, Shen J L. 2002. Influence of salinity and day and night rhythm on feeding rate (FR) of Ruditapes philippinarum. Journal of Oceanography in Taiwan Strait, 21(1):72-77. (in Chinese with English abstract)
Wu S N, Liu D W, Liu Y, Hu B Q, Zhang J Q, Wang Y, Wang T. 2014. Cloning and expression analysis of heat shock protein 60 gene from hyriopsis cumingii. Acta Hydrobiologica Sinica, 38(5):897-902. (in Chinese with English abstract)
Xu Q Q, Liu J, Huang H W. 2005. Effects of temperature on oxygen consumption rate and ammonia excretion rate of Solenaia oleivora. Journal of Zhanjiang Ocean University, 25(1):51-55. (in Chinese with English abstract)
Xu Y P, Zheng G W, Dong S Z, Liu G F, Yu X P. 2014. Molecular cloning, characterization and expression analysis of HSP60, HSP70 and HSP90 in the golden apple snail, Pomacea canaliculata. Fish & Shellfish Immunology, 41(2):643-653, https://doi.org/10.1016/j.fsi.2014.10.013.
Zhang J, Zhang Q Z, Zhang Z H, Cui M. 2009. HSC70 gene and its tissue expression analysis in yellow catfish. Acta Hydrobiologica Sinica, 33(3):426-434. (in Chinese with English abstract)
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