海洋经济贝类中Opine脱氢酶研究进展
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摘要
为研究海洋经济贝类在捕后面临无氧胁迫时的风味品质变化,从Opine脱氢酶(OpDHs)在无氧代谢中发挥的作用、OpDHs分布的物种与组织特异性、海洋经济贝类在环境胁迫下的OpDHs应答表现、OpDHs基本酶学性质4个方面对无脊椎动物无氧代谢中发挥重要作用的OpDHs进行了系统综述。无脊椎动物OpDHs主要包括Alanopine(ADH)、Octopine(ODH)、Strombine(SDH)、Tauropine(TDH)、β-Alanopine(BADH)和Lysopine(LyDH) 6种脱氧酶,在贝类中ODH活性最高;在甲壳类动物中几乎未发现ODH活性;在环节动物中只有少数动物存在ODH且活性较低,ADH和SDH起主要作用,肌肉组织中OpDHs活性最高;不同来源的OpDHs在基本酶学性质上均表现出相同或相似的性质。OpDHs具有作为活品代谢状态指标的潜力,可为捕后活品品质评价提供新思路。
The Opine dehydrogenase(OpDHs) is involved in regulation of anaerobic metabolism influencing flavor quality of marine commercial mollusks exposed to hypoxia or anoxia stress during the postharvest process. This article reviews the followings of the OpDHs: role in anaerobic metabolism, species-specific and tissue-specific distribution, OpDHs activity of different species in response to the environmental stress, and the basic enzymatic property of OpDHs in marine invertebrates, especially with the maximal activity of octopine dehydrogenase(ODH) in marine mollusks and without activity of ODH in crustacean. The high activities of alanopine dehydrogenase and strombine dehydrogenase were observed in a few annelids, with low ODH activity, and the maxiaml OpDHs activity in muscle. The OpDHs from different species showed the same or similar enzymatic properties, and have the possibility to become a potential indicator of physiological state, and to provide a new method for the quality evaluation of postharvested live products.
The Opine dehydrogenase(OpDHs) is involved in regulation of anaerobic metabolism influencing flavor quality of marine commercial mollusks exposed to hypoxia or anoxia stress during the postharvest process. This article reviews the followings of the OpDHs: role in anaerobic metabolism, species-specific and tissue-specific distribution, OpDHs activity of different species in response to the environmental stress, and the basic enzymatic property of OpDHs in marine invertebrates, especially with the maximal activity of octopine dehydrogenase(ODH) in marine mollusks and without activity of ODH in crustacean. The high activities of alanopine dehydrogenase and strombine dehydrogenase were observed in a few annelids, with low ODH activity, and the maxiaml OpDHs activity in muscle. The OpDHs from different species showed the same or similar enzymatic properties, and have the possibility to become a potential indicator of physiological state, and to provide a new method for the quality evaluation of postharvested live products.
引文
[1] 王晓雯,朱华,胡红霞,等.低氧胁迫对西伯利亚鲟幼鱼生理状态的影响[J].水产科学,2016,35(5):459-465.
[2] Seibel B A,H?fker N S,Trübenbach K,et al.Metabolic suppression during protracted exposure to hypoxia in the jumbo squid,Dosidicus gigas,living in an oxygen minimum zone[J].Journal of Experimental Biology,2014,217(14):2555-2568.
[3] G?de G.Purification and properties of tauropine dehydrogenase from the shell adductor muscle of the ormer,Haliotis lamellosa[J].European Journal of Biochemistry,1986,160(2):311-318.
[4] 郑尧,刘俊荣,周晏琳,等.捕后虾夷扇贝闭壳肌免疫因子与活品品质评价初探[J].大连海洋大学学报,2017,32(2):217-223.
[5] 杨婷婷.采捕后活品虾夷扇贝(Patinopecten yessoensis)的风味变化[D].大连:大连海洋大学,2014.
[6] 周晏琳,郑尧,刘慧慧,等.干露对活品虾夷扇贝闭壳肌SOD酶活性及其性质的影响[J].大连海洋大学学报,2018,33(5):651-657.
[7] 田元勇,刘金洋,刘慧慧,等.捕后暂养对虾夷扇贝闭壳肌硬化的影响[J].水产学报,2017,41(6):888-895.
[8] 刘金洋,刘俊荣,田元勇,等.捕后处置对活品底播虾夷扇贝生化代谢的影响[J].水产学报,2017,41(1):81-87.
[9] 杨婷婷,刘俊荣,俞微微,等.活品流通过程中虾夷扇贝风味品质的变化[J].水产学报,2015,39(1):136-146.
[10] Lee A C,Lee M C,Lee Y H,et al.Candidates for a hypoxia-stress indicator in the hard clam,Meretrix lusoria[J].Aquaculture,2008,278(1-4):150-155.
[11] Carroll J L,Wells R M G.Strategies of anaerobiosis in New Zealand infaunal bivalves:adaptations to environmental and functional hypoxia[J].New Zealand Journal of Marine and Freshwater Research,1995,29(2):137-146.
[12] Müller A,Janssen F,Grieshaber M K.Putative reaction mechanism of heterologously expressed octopine dehydrogenase from the great scallop,Pecten maximus (L.)[J].FEBS Journal,2007,274(24):6329-6339.
[13] Van O N,Smits S H J,Schmitt L,et al.Control of D-octopine formation in scallop adductor muscle as revealed through thermodynamic studies of octopine dehydrogenase[J].Journal of Experimental Biology,2012,215(9):1515-1522.
[14] Livingstone D R,De Zwaan A,Leopold M,et al.Studies on the phylogenetic distribution of pyruvate oxidoreductases[J].Biochemical Systematics and Ecology,1983,11(4):415-425.
[15] Harcet M,Perina D,Ple?e B.Opine dehydrogenases in marine invertebrates[J].Biochemical Genetics,2013,51(9-10):666-676.
[16] Hochachka P W.Fuels and pathways as designed systems for support of muscle work[J].Journal of Experimental Biology,1985,115:149-164.
[17] Livingstone D R.Invertebrate and vertebrate pathways of anaerobic metabolism:evolutionary considerations[J].Journal of the Geological Society,1983,140(1):27-37.
[18] Grieshaber M K,Hardewig I,Kreutzer U,et al.Physiological and metabolic responses to hypoxia in invertebrates[M]//Reviews of Physiology,Biochemistry and Pharmacology.Berlin:Springer,1993,125:43.
[19] Chen S Q,Zhang C H,Xiong Y F,et al.A GC-MS-based metabolomics investigation on scallop (Chlamys farreri) during semi-anhydrous living-preservation[J].Innovative Food Science & Emerging Technologies,2015,31:185-195.
[20] De Zwaan A,Zandee D I.Body distribution and seasonal changes in the glycogen content of the common sea mussel Mytilus edulis[J].Comparative Biochemistry and Physiology Part A:Physiology,1972,43(1):53-58.
[21] De Zwaan A,Putzer V.Metabolic adaptations of intertidal invertebrates to environmental hypoxia (a comparison of environmental anoxia to exercise anoxia)[J].Symposia of the Society for Experimental Biology,1985,39:33-62.
[22] Sato M,Takeuchi M,Kanno N,et al.Distribution of opine dehydrogenases and lactate dehydrogenase activities in marine animals[J].Comparative Biochemistry and Physiology Part B:Comparative Biochemistry,1993,106(4):955-960.
[23] Fields J H A,Storey K B.Tissue-specific alanopine dehydrogenase from the gill and strombine dehydrogenase from the foot muscle of the cherrystone clam Mercenaria mercenaria (Linn.)[J].Journal of Experimental Marine Biology and Ecology,1987,105(2-3):175-185.
[24] Nakanishi K,Fujii T,Szekely J.Possible relationship between energy dissipation and agitation in steel processing operations[J].Ironmaking & Steelmaking,1975,2(3):193-197.
[25] Van Thoai N,Huc C,Pho D B,et al.Octopine déshydrogénase Purification et propriétés catalytiques[J].Biochimica et Biophysica Acta (BBA)-Enzymology,1969,191(1):46-57.
[26] Fields J H A,Eng A K,Ramsden W D,et al.Alanopine and strombine are novel imino acids produced by a dehydrogenase found in the adductor muscle of the oyster,Crassostrea gigas[J].Archives of Biochemistry and Biophysics,1980,201(1):110-114.
[27] Dando P R,Storey K B,Hochachka P W,et al.Multiple dehydrogenases in marine molluscs:electrophoretic analysis of alanopine dehydrogenase,strombine dehydrogenase,octopine dehydrogenase and lactate dehydrogenase[J].Marine Biology Letters,1981,28(2):261-268.
[28] Sato M,G?de G.Rhodoic acid dehydrogenase:a novel amino acid-linked dehydrogenase from muscle tissue of Haliotis species[J].Naturwissenschaften,1986,73(4):207-209.
[29] Sato M,Takahara M,Kanno N,et al.Isolation of a new opine,β-alanopine,from the extracts of the muscle of the marine bivalve mollusc,Scapharca broughtonii[J].Comparative Biochemistry and Physiology Part B:Comparative Biochemistry,1964,88(3):803-806.
[30] Livingstone D R,Stickle W B,Kapper M A,et al.Further studies on the phylogenetic distribution of pyruvate oxidoreductase activities[J].Comparative Biochemistry and Physiology Part B:Comparative Biochemistry,1990,97(4):661-666.
[31] Wongso S,Ushio H,Ohshima T,et al.Changes in content of octopine,acidic opines,related amino acids and phosphoarginine in the adductor muscle of three species of scallop during storage[J].Journal of Food Biochemistry,1998,22(1):65-81.
[32] Artigaud S,Lacroix C,Richard J,et al.Proteomic responses to hypoxia at different temperatures in the great scallop (Pecten maximus)[J].Peer J,2015,3:e871.
[33] Beardall C H,Johnston I A.Lysosomal enzyme activities in muscle following starvation and refeeding in the saithe Pollachius virens L.[J].European Journal of Cell Biology,1985,39(1):112-117.
[34] Ivanina A V,Froelich B,Williams T,et al.Interactive effects of cadmium and hypoxia on metabolic responses and bacterial loads of eastern oysters Crassostrea virginica Gmelin[J].Chemosphere,2011,82(3):377-389.
[35] Speers-Roesch B,Callaghan N I,Maccormack T J,et al.Enzymatic capacities of metabolic fuel use in cuttlefish (Sepia officinalis) and responses to food deprivation:insight into the metabolic organization and starvation survival strategy of cephalopods[J].Journal of Comparative Physiology B,2016,186(6):711-725.
[36] Fields J H,Hochachka P W.Purification and properties of alanopine dehydrogenase from the adductor muscle of the oyster,Crassostrea gigas (Mollusca,Bivalvia)[J].European Journal of Biochemistry,1981,114(3):615-621.
[37] Storey K B.Tissue-specific alanopine dehydrogenase and strombine dehydrogenase from the sea mouse,Aphrodite aculeata (Polychaeta)[J].Journal of Experimental Zoology,1983,225(3):369-378.
[38] G?de G,Zebe E. über den Anaerobiosestoffwechsel von Molluskenmuskeln[J].Journal of Comparative Physiology,1973,85(3):291-301.
[39] Meinardus-Hager G,G?de G.The pyruvate branch point in the anaerobic energy metabolism of the jumping cockle Cardium tuberculatum L.:D-lactate formation during environmental anaerobiosis versus octopine formation during exercise[J].Experimental Biology,1986,45(2):91-110.
[40] G?de G,Weeda E,Gabbott P A.Changes in the level of octopine during the escape responses of the scallop,Pecten maximus (L.)[J].Journal of Comparative Physiology,1978,124(2):121-127.
[41] Wongso S,Ushio H,Yamanaka H.Glycolytic enzymes in the tissues of three species of scallop (Bivalvia:Pectinidae)[J].Fisheries Science,1999,65(1):123-128.
[42] Mulcahy P,Griffin T,O'Carra P.Biospecific affinity chromatographic purification of octopine dehydrogenase from molluscs[J].Protein Expression and Purification,1997,9(1):109-114.
[43] Lee A C,Lee K T,Pan L Y.Purification and kinetic characteristics of strombine dehydrogenase from the foot muscle of the hard clam (Meretrix lusoria)[J].Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology,2011,158(1):38-45.
[44] Carvajal N,Kessi E.Properties of octopine dehydrogenase from the foot muscle of Concholepas concholepas[J].Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology,1988,90(1):77-79.
[45] Urich K.Comparative Animal Biochemistry[M].Berlin Heidelberg:Springer,1994:263-264.
[46] Plaxton W C,Storey K B.Alanopine dehydrogenase:purification and characterization of the enzyme from Littorina littorea foot muscle[J].Journal of Comparative Physiology,1982,149(1):57-65.
[47] Vollmer M,Hochachka P W,Mommsen T P.Octopine dehydrogenase and phosphoarginine kinase in squid mantle:cooperation of two enzymes at the arginine branch point in cephalopod muscle[J].Canadian Journal of Zoology,1981,59(7):1447-1453.
[48] Grieshaber M,Kronig E,Koormann R.A photometric estlmation of phospho-L-arginine,arginine and octopine using homogenous octopine dehydrogenase isoenzyme 2 from the squid,Loligo vulgaris Lam[J].Hoppe-Seyler's Zeitschrift für physiologische Chemie,1978,359(1):133-136.
[49] G?de G,Carlsson K H.Purification and characterisation of octopine dehydrogenase from the marine nemertean Cerebratulus lacteus (Anopla:Heteronemerta):comparison with scallop octopine dehydrogenase[J].Marine Biology,1984,79(1):39-45.
[50] Lee A C,Lee K T.The enzyme activities of opine and lactate dehydrogenase in the gills,mantle,foot,and adductor of the hard clam Meretrix lusoria[J].Journal of Marine Science & Technology,2011,19(4):361-367.
[51] Strahl J,Dringen R,Schmidt M M,et al.Metabolic and physiological responses in tissues of the long-lived bivalve Arctica islandica to oxygen deficiency[J].Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology,2011,158(4):513-519.
[52] Murphy J W A,Richmond R H.Changes to coral health and metabolic activity under oxygen deprivation[J].Peer J,2016,4(2):e1956.
[2] Seibel B A,H?fker N S,Trübenbach K,et al.Metabolic suppression during protracted exposure to hypoxia in the jumbo squid,Dosidicus gigas,living in an oxygen minimum zone[J].Journal of Experimental Biology,2014,217(14):2555-2568.
[3] G?de G.Purification and properties of tauropine dehydrogenase from the shell adductor muscle of the ormer,Haliotis lamellosa[J].European Journal of Biochemistry,1986,160(2):311-318.
[4] 郑尧,刘俊荣,周晏琳,等.捕后虾夷扇贝闭壳肌免疫因子与活品品质评价初探[J].大连海洋大学学报,2017,32(2):217-223.
[5] 杨婷婷.采捕后活品虾夷扇贝(Patinopecten yessoensis)的风味变化[D].大连:大连海洋大学,2014.
[6] 周晏琳,郑尧,刘慧慧,等.干露对活品虾夷扇贝闭壳肌SOD酶活性及其性质的影响[J].大连海洋大学学报,2018,33(5):651-657.
[7] 田元勇,刘金洋,刘慧慧,等.捕后暂养对虾夷扇贝闭壳肌硬化的影响[J].水产学报,2017,41(6):888-895.
[8] 刘金洋,刘俊荣,田元勇,等.捕后处置对活品底播虾夷扇贝生化代谢的影响[J].水产学报,2017,41(1):81-87.
[9] 杨婷婷,刘俊荣,俞微微,等.活品流通过程中虾夷扇贝风味品质的变化[J].水产学报,2015,39(1):136-146.
[10] Lee A C,Lee M C,Lee Y H,et al.Candidates for a hypoxia-stress indicator in the hard clam,Meretrix lusoria[J].Aquaculture,2008,278(1-4):150-155.
[11] Carroll J L,Wells R M G.Strategies of anaerobiosis in New Zealand infaunal bivalves:adaptations to environmental and functional hypoxia[J].New Zealand Journal of Marine and Freshwater Research,1995,29(2):137-146.
[12] Müller A,Janssen F,Grieshaber M K.Putative reaction mechanism of heterologously expressed octopine dehydrogenase from the great scallop,Pecten maximus (L.)[J].FEBS Journal,2007,274(24):6329-6339.
[13] Van O N,Smits S H J,Schmitt L,et al.Control of D-octopine formation in scallop adductor muscle as revealed through thermodynamic studies of octopine dehydrogenase[J].Journal of Experimental Biology,2012,215(9):1515-1522.
[14] Livingstone D R,De Zwaan A,Leopold M,et al.Studies on the phylogenetic distribution of pyruvate oxidoreductases[J].Biochemical Systematics and Ecology,1983,11(4):415-425.
[15] Harcet M,Perina D,Ple?e B.Opine dehydrogenases in marine invertebrates[J].Biochemical Genetics,2013,51(9-10):666-676.
[16] Hochachka P W.Fuels and pathways as designed systems for support of muscle work[J].Journal of Experimental Biology,1985,115:149-164.
[17] Livingstone D R.Invertebrate and vertebrate pathways of anaerobic metabolism:evolutionary considerations[J].Journal of the Geological Society,1983,140(1):27-37.
[18] Grieshaber M K,Hardewig I,Kreutzer U,et al.Physiological and metabolic responses to hypoxia in invertebrates[M]//Reviews of Physiology,Biochemistry and Pharmacology.Berlin:Springer,1993,125:43.
[19] Chen S Q,Zhang C H,Xiong Y F,et al.A GC-MS-based metabolomics investigation on scallop (Chlamys farreri) during semi-anhydrous living-preservation[J].Innovative Food Science & Emerging Technologies,2015,31:185-195.
[20] De Zwaan A,Zandee D I.Body distribution and seasonal changes in the glycogen content of the common sea mussel Mytilus edulis[J].Comparative Biochemistry and Physiology Part A:Physiology,1972,43(1):53-58.
[21] De Zwaan A,Putzer V.Metabolic adaptations of intertidal invertebrates to environmental hypoxia (a comparison of environmental anoxia to exercise anoxia)[J].Symposia of the Society for Experimental Biology,1985,39:33-62.
[22] Sato M,Takeuchi M,Kanno N,et al.Distribution of opine dehydrogenases and lactate dehydrogenase activities in marine animals[J].Comparative Biochemistry and Physiology Part B:Comparative Biochemistry,1993,106(4):955-960.
[23] Fields J H A,Storey K B.Tissue-specific alanopine dehydrogenase from the gill and strombine dehydrogenase from the foot muscle of the cherrystone clam Mercenaria mercenaria (Linn.)[J].Journal of Experimental Marine Biology and Ecology,1987,105(2-3):175-185.
[24] Nakanishi K,Fujii T,Szekely J.Possible relationship between energy dissipation and agitation in steel processing operations[J].Ironmaking & Steelmaking,1975,2(3):193-197.
[25] Van Thoai N,Huc C,Pho D B,et al.Octopine déshydrogénase Purification et propriétés catalytiques[J].Biochimica et Biophysica Acta (BBA)-Enzymology,1969,191(1):46-57.
[26] Fields J H A,Eng A K,Ramsden W D,et al.Alanopine and strombine are novel imino acids produced by a dehydrogenase found in the adductor muscle of the oyster,Crassostrea gigas[J].Archives of Biochemistry and Biophysics,1980,201(1):110-114.
[27] Dando P R,Storey K B,Hochachka P W,et al.Multiple dehydrogenases in marine molluscs:electrophoretic analysis of alanopine dehydrogenase,strombine dehydrogenase,octopine dehydrogenase and lactate dehydrogenase[J].Marine Biology Letters,1981,28(2):261-268.
[28] Sato M,G?de G.Rhodoic acid dehydrogenase:a novel amino acid-linked dehydrogenase from muscle tissue of Haliotis species[J].Naturwissenschaften,1986,73(4):207-209.
[29] Sato M,Takahara M,Kanno N,et al.Isolation of a new opine,β-alanopine,from the extracts of the muscle of the marine bivalve mollusc,Scapharca broughtonii[J].Comparative Biochemistry and Physiology Part B:Comparative Biochemistry,1964,88(3):803-806.
[30] Livingstone D R,Stickle W B,Kapper M A,et al.Further studies on the phylogenetic distribution of pyruvate oxidoreductase activities[J].Comparative Biochemistry and Physiology Part B:Comparative Biochemistry,1990,97(4):661-666.
[31] Wongso S,Ushio H,Ohshima T,et al.Changes in content of octopine,acidic opines,related amino acids and phosphoarginine in the adductor muscle of three species of scallop during storage[J].Journal of Food Biochemistry,1998,22(1):65-81.
[32] Artigaud S,Lacroix C,Richard J,et al.Proteomic responses to hypoxia at different temperatures in the great scallop (Pecten maximus)[J].Peer J,2015,3:e871.
[33] Beardall C H,Johnston I A.Lysosomal enzyme activities in muscle following starvation and refeeding in the saithe Pollachius virens L.[J].European Journal of Cell Biology,1985,39(1):112-117.
[34] Ivanina A V,Froelich B,Williams T,et al.Interactive effects of cadmium and hypoxia on metabolic responses and bacterial loads of eastern oysters Crassostrea virginica Gmelin[J].Chemosphere,2011,82(3):377-389.
[35] Speers-Roesch B,Callaghan N I,Maccormack T J,et al.Enzymatic capacities of metabolic fuel use in cuttlefish (Sepia officinalis) and responses to food deprivation:insight into the metabolic organization and starvation survival strategy of cephalopods[J].Journal of Comparative Physiology B,2016,186(6):711-725.
[36] Fields J H,Hochachka P W.Purification and properties of alanopine dehydrogenase from the adductor muscle of the oyster,Crassostrea gigas (Mollusca,Bivalvia)[J].European Journal of Biochemistry,1981,114(3):615-621.
[37] Storey K B.Tissue-specific alanopine dehydrogenase and strombine dehydrogenase from the sea mouse,Aphrodite aculeata (Polychaeta)[J].Journal of Experimental Zoology,1983,225(3):369-378.
[38] G?de G,Zebe E. über den Anaerobiosestoffwechsel von Molluskenmuskeln[J].Journal of Comparative Physiology,1973,85(3):291-301.
[39] Meinardus-Hager G,G?de G.The pyruvate branch point in the anaerobic energy metabolism of the jumping cockle Cardium tuberculatum L.:D-lactate formation during environmental anaerobiosis versus octopine formation during exercise[J].Experimental Biology,1986,45(2):91-110.
[40] G?de G,Weeda E,Gabbott P A.Changes in the level of octopine during the escape responses of the scallop,Pecten maximus (L.)[J].Journal of Comparative Physiology,1978,124(2):121-127.
[41] Wongso S,Ushio H,Yamanaka H.Glycolytic enzymes in the tissues of three species of scallop (Bivalvia:Pectinidae)[J].Fisheries Science,1999,65(1):123-128.
[42] Mulcahy P,Griffin T,O'Carra P.Biospecific affinity chromatographic purification of octopine dehydrogenase from molluscs[J].Protein Expression and Purification,1997,9(1):109-114.
[43] Lee A C,Lee K T,Pan L Y.Purification and kinetic characteristics of strombine dehydrogenase from the foot muscle of the hard clam (Meretrix lusoria)[J].Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology,2011,158(1):38-45.
[44] Carvajal N,Kessi E.Properties of octopine dehydrogenase from the foot muscle of Concholepas concholepas[J].Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology,1988,90(1):77-79.
[45] Urich K.Comparative Animal Biochemistry[M].Berlin Heidelberg:Springer,1994:263-264.
[46] Plaxton W C,Storey K B.Alanopine dehydrogenase:purification and characterization of the enzyme from Littorina littorea foot muscle[J].Journal of Comparative Physiology,1982,149(1):57-65.
[47] Vollmer M,Hochachka P W,Mommsen T P.Octopine dehydrogenase and phosphoarginine kinase in squid mantle:cooperation of two enzymes at the arginine branch point in cephalopod muscle[J].Canadian Journal of Zoology,1981,59(7):1447-1453.
[48] Grieshaber M,Kronig E,Koormann R.A photometric estlmation of phospho-L-arginine,arginine and octopine using homogenous octopine dehydrogenase isoenzyme 2 from the squid,Loligo vulgaris Lam[J].Hoppe-Seyler's Zeitschrift für physiologische Chemie,1978,359(1):133-136.
[49] G?de G,Carlsson K H.Purification and characterisation of octopine dehydrogenase from the marine nemertean Cerebratulus lacteus (Anopla:Heteronemerta):comparison with scallop octopine dehydrogenase[J].Marine Biology,1984,79(1):39-45.
[50] Lee A C,Lee K T.The enzyme activities of opine and lactate dehydrogenase in the gills,mantle,foot,and adductor of the hard clam Meretrix lusoria[J].Journal of Marine Science & Technology,2011,19(4):361-367.
[51] Strahl J,Dringen R,Schmidt M M,et al.Metabolic and physiological responses in tissues of the long-lived bivalve Arctica islandica to oxygen deficiency[J].Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology,2011,158(4):513-519.
[52] Murphy J W A,Richmond R H.Changes to coral health and metabolic activity under oxygen deprivation[J].Peer J,2016,4(2):e1956.
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