怒江裂腹鱼鳃的显微和超微结构
|
摘要
通过光镜、扫描电镜及透射电镜技术,研究了怒江裂腹鱼(Schizothorax nukiangensis)鳃的组织结构和超微结构。结果表明,怒江裂腹鱼鳃基本结构与其他硬骨鱼相似,均由鳃耙、鳃弓、鳃丝以及鳃小片构成,且各部分具有不同的组织结构和细胞类型。扁平上皮细胞覆盖于整个鳃表面,其表面的纹路主要有3种类型,在鳃上不同的部位具有不同的结构和功能。线粒体密集细胞主要分布于鳃小片基部,仅有一种细胞类型,顶端膜内凹呈浅滩型,细胞内具有大量圆形的线粒体。怒江裂腹鱼鳃内扁平上皮细胞和线粒体密集细胞的形态结构与其在急流中游泳和摄食活动等生活习性相适应。本研究结果丰富了怒江裂腹鱼的基础生物学资料,并为阐明鱼类鳃的结构特征与其生活习性之间的关系提供参考。
The freshwater fish Schizothorax nukiangensis is a rare, endemic and economic species, only distributed in the middle and upper reaches of the Nujiang River(Upper Salween River) in China. Potential cascade hydropower development in the Nujiang River will threaten the survival of S. nukiangensis. The potential for drastic changes in the water flow, water temperature and food supply of their habitat may lead to extinction of S. nukiangensis. Therefore, biological research on future conservation and resource utilization is imperative. Herein, the histology and ultra-structure of the gill in the teleost S. nukiangensis was investigated using the optical and electron microscopic imaging techniques. The results showed that the basic structure of the gills consisted of the gill raker, gill arch, gill filament and lamellae, which was similar to other teleost fishes. Different parts of the gill possess distinct histological structures and cell types. The pavement cells(PVC) covered the filament epithelium and lamellae of the gills, showing three distinct morphological features of micro-ridges in the different parts of the gill. There was only one type of mitochondrial rich cells(MRC) observed in the gill, which were located at the base of lamellae. All these MRC have a large number of big, round mitochondria and exhibit apical shallow-basin with microvilli. Our results suggested that the morphological feature and functional diversity of PVC and MRC in the gill of S. nukiangensis were in accordance with its habitat. These observations enrich the basic biological knowledge of S. nukiangensis and can provide a reference for clarifying the relationship between the specific structural characteristics of the fish and their living habits.
The freshwater fish Schizothorax nukiangensis is a rare, endemic and economic species, only distributed in the middle and upper reaches of the Nujiang River(Upper Salween River) in China. Potential cascade hydropower development in the Nujiang River will threaten the survival of S. nukiangensis. The potential for drastic changes in the water flow, water temperature and food supply of their habitat may lead to extinction of S. nukiangensis. Therefore, biological research on future conservation and resource utilization is imperative. Herein, the histology and ultra-structure of the gill in the teleost S. nukiangensis was investigated using the optical and electron microscopic imaging techniques. The results showed that the basic structure of the gills consisted of the gill raker, gill arch, gill filament and lamellae, which was similar to other teleost fishes. Different parts of the gill possess distinct histological structures and cell types. The pavement cells(PVC) covered the filament epithelium and lamellae of the gills, showing three distinct morphological features of micro-ridges in the different parts of the gill. There was only one type of mitochondrial rich cells(MRC) observed in the gill, which were located at the base of lamellae. All these MRC have a large number of big, round mitochondria and exhibit apical shallow-basin with microvilli. Our results suggested that the morphological feature and functional diversity of PVC and MRC in the gill of S. nukiangensis were in accordance with its habitat. These observations enrich the basic biological knowledge of S. nukiangensis and can provide a reference for clarifying the relationship between the specific structural characteristics of the fish and their living habits.
引文
[1] Schnell S,Stott L C,Hogstrand C,et al. Procedures for the reconstruction, primary culture and experimental use of rainbow trout gill epithelia[J]. Nature Protocols, 2016, 11(3):490-498.
[2] Maina J N. Structure, function and evolution of the gas exchangers:comparative perspectives[J]. Journal of Anatomy,2002, 201(4):281-304.
[3] Evans D H, Piermarini P M, Choe K P. The multifunctional fish gill:dominant site of gas exchange,osmoregulation,acid-base regulation, and excretion of nitrogenous waste[J].Physiological Reviews, 2005, 85(1):97-177.
[4] Hofer R, Kuhnl M, Psenner R. Seasonal changes of the gill epithelia of Arctic char(Salvelinus alpinus)from a high mountain lake[J]. Aquatic Sciences, 2000, 62(4):297-307.
[5] Uchida K, Kaneko T,Miyazaki H,et al. Excellent salinity tolerance of Mozambique Tilapia(Oreochromis mossambicus):elevated chloride cell activity in the branchial and opercular epithelia of the fish adapted to concentrated seawater[J]. Zoological Science, 2000, 17(2):149-160.
[6] Tsai J C, Hwang P P. Effects of wheat germ agglutinin and colchicine on microtubules of the mitochondria-rich cells and Ca2+uptake in tilapia(Oreochromis mossambicus)larvae[J]. Journal of Experimental Biology, 1998, 201(15):2263-2271.
[7] Zydlewski J, Mccormick S D. Developmental and environmental regulation of chloride cells in young American shad,Alosa sapidissima[J]. Journal of Experimental Zoology, 2010,290(2):73-87.
[8] Fernandes M N,Perna S A,Moron S E. Chloride cell apical surface changes in gill epithelia of the armoured catfish Hypos tomus plecostomus during exposure to distilled water[J].Journal of Fish Biology,2010, 52(4):844-849.
[9] Li J E, Xu X J, Qu Y J, et al. Study on the gill structure and the respiratory area of chu's croaker Nibea coibor[J]. South China Fisheries Science,2008, 4(1):22-27.[李加儿,许晓娟,区又君,等.浅色黄姑鱼鳃结构及其呼吸面积的研究[J].南方水产科学,2008, 4(1):22-27.]
[10] Zhao F, Yang G, Zhang T, et al. Characters of morphology,distribution and quantity of branchial chloride cells of juvenile Acipenser sinensis acclimated in freshwater and brackish water[J]. Marine Fisheries,2016, 38(1):35-41.[赵峰,杨刚,张涛,等.淡水和半咸水条件下中华鲟幼鱼鳃上皮泌氯细胞的形态特征与数量分布[J].海洋渔业,2016, 38(1):35-41.]
[11] Bury N R, Grosell M. Waterborne iron acquisition by a freshwater teleost fish, zebrafish Danio rerio[J]. Journal of Experimental Biology, 2003, 206(19):3529-3535.
[12] Goss G G, Perry S F, Fryer J N, et al. Gill morphology and acid-base regulation in freshwater fishes[J]. Comparative Biochemistry and Physiology Part A Molecular and Integrative Physiology, 1998, 119(1):107-115.
[13] Wilson J M, Laurent P. Fish gill morphology:inside out[J].Journal of Experimental Zoology, 2002, 293(3):192-213.
[14] Perry S F. The chloride cell:structure and function in the gills of freshwater fishes[J]. Annual Review of Physiology,1997, 59(59):325-347.
[15] Yue X J, Wang D Q, Liu S P, et al. Population genetic structure of three schizothoracins from Nujiang River in southwestern China[J]. Acta Ecologica Sinica, 2010, 30(23):6418-6429.[岳兴建,汪登强,刘绍平,等.怒江三种裂腹鱼属鱼类种群遗传结构[J].生态学报,2010, 30(23):6418-6429.]
[16] Yu M, Zhang D, Hu P, et al. Divergent adaptation to Qinghai-Tibetan Plateau implicated from transciptome study of Gymnocypris dobula and Schizothorax nukiangensis[J].Biochemical Systematics and Ecology, 2017, 71(1):97-105.
[17] Chen W, Du K, He S. Genetic structure and historical demography of Schizothorax nukiangensis(Cyprinidae)in continuous habitat[J]. Ecology and Evolution, 2015, 5(4):984-995.
[18] Li W, Liu Y, Xu Q. Complete mitochondrial genome of Schizothorax nukiangensis Tsao(Cyprinidae:Schizothorax)[J]. Mitochondrial DNA Part A, 2016, 27(5):3549-3550.
[19] Fang J, Pan K C, Deng T H. A scanning electron microscopical observation of the gill of Schizothorax prenanti(Schizothorax)[J]. Journal of Sichuan Agricultural University,2004, 22(2):196-198.[方静,潘康成,邓天怀.齐口裂腹鱼鳃表面结构扫描电镜观察[J].四川农业大学学报,2004,22(2):196-198.]
[20] Guo S H, Wang L C. A scanning electron microscopical study of the gill surface of the comon carp, Cyprinus carpio[J]. Acta Hydrobiologica Sinica, 1988, 12(1):54-58.[郭淑华,王良臣.鲤鳃表面结构扫描电镜研究[J].水生生物学报,1988, 12(1):54-58.]
[21] Luo F, Chen L Q, Kang B. Observation of uitrastructure of the gill filament in Juvenile spinibarbus sinensis with scanning electrominc microscope[J]. Journal of Sichuan Agricultural University,2011,29(4):555-559.[罗芬,陈礼强,康斌.中华倒刺鳃幼鱼鳃的扫描电镜观察[J].四川农业大学学报,2011,29(4):555-559.]
[22] Leguen I. Gills of the medaka(Oryzias latipes):a scanning electron microscopy study[J]. Journal of Morphology, 2018,279(1):97-108.
[23] Luo F, Chen L Q, Kang B. Fine structure of gills in teleost(Pelteobagrus fulvidarco)[J]. Oceanologia et Limnologia Sinica,2011,42(4):488-494.[罗芬,陈礼强,康斌.黄颡鱼(Pelteobagrus fulvidraco)鳃的超微结构研究[J].海洋与湖沼,2011,42(4):488-494.]
[24] Lee T H, Hwang P P, Lin H C, et al. Mitochondria-rich cells in the branchial epithelium of the teleost, Oreochromis mossambicus, acclimated to various hypotonic environments[J].Fish Physiology, 1996, 15(6):513-523.
[25] Pisam M, Caroff A, Rambourg A. Two types of chloride cell in the gill epithelium of a freshwater-adapted euryhaline fish,Lebistes reticulatus:their modifications during adaptation to seawater[J]. American Journal of Anatomy, 1987, 179(1):40-50.
[26] Wilson J M,Laurent P,Tufts B L,et al. NaCl uptake by the branchial epithelium in freshwater teleost fish:an immunological approach to ion-transport protein localization[J].Journal of Experimental Biology, 2000, 203(15):2279-2296.
[27] Long H,Chen J W,Fu Y S,et al. Microscopic observation in gill of six species of fish[J]. Journal of Hydroecology, 2008,28(2):39-40.[龙华,陈建武,付元帅,等. 6种鱼鳃的显微观察[J].水生态学杂志,2008, 28(2):39-40.]
[28] Wright D E. Morphology of the gill epithelium of the Lungfish, Lepidosiren paradoxa[J]. Cell and Tissue Research, 1974,153(3):365-381.
[29] Kumari U, Yashpal M, Mittal S, et al. Surface ultrastructure of gill arches and gill rakers in relation to feeding of an Indian major carp, Cirrhinus mrigala[J]. Tissue Cell, 2009,41(5):318-325.
[30] Elsheikh E H. Scanning electron microscopic studies of gill arches and rakers in relation to feeding habits of some fresh water fishes[J]. The Journal of Basic&Applied Zoology,2013,66(3):121-130.
[31] Goss G G, Adamia S, Galvez F. Peanut lectin binds to a subpopulation of mitochondria-rich cells in the rainbow trout gill epithelium[J]. Ameican Journal of Physiology, 2001,281(5):1718-1725.
[32] Pisam M, Massa F, Jammet C, et al. Chronology of the appearance of(3, A, and a mitochondria-rich cells in the gill epithelium during ontogenesis of the brown trout(Salmo trutta)[J]. The Anatomical Record, 2000, 259(3):301-311.
[33] Pisam M, Le M C, Auperin B, et al. Apical structures of"mitochondria-rich"alpha and beta cells in euryhaline fish gill:their behaviour in various living conditions[J]. The Anatomical Record, 1995,241(1):13.
[34] Foskett J K, Scheffey C. The chloride cell:definitive identification as the salt-secretory cell in teleosts[J]. Science, 1982,215(4529):164-166.
[35] Carmona R,Garcia-Gallego M,Sanz A, et al. Chloride cells and pavement cells in gill epithelia of Acipenser naccarii:ultrastructural modifications in seawater-acclimated specimens[J]. Journal of Fish Biology, 2004, 64(2):553-566.
[2] Maina J N. Structure, function and evolution of the gas exchangers:comparative perspectives[J]. Journal of Anatomy,2002, 201(4):281-304.
[3] Evans D H, Piermarini P M, Choe K P. The multifunctional fish gill:dominant site of gas exchange,osmoregulation,acid-base regulation, and excretion of nitrogenous waste[J].Physiological Reviews, 2005, 85(1):97-177.
[4] Hofer R, Kuhnl M, Psenner R. Seasonal changes of the gill epithelia of Arctic char(Salvelinus alpinus)from a high mountain lake[J]. Aquatic Sciences, 2000, 62(4):297-307.
[5] Uchida K, Kaneko T,Miyazaki H,et al. Excellent salinity tolerance of Mozambique Tilapia(Oreochromis mossambicus):elevated chloride cell activity in the branchial and opercular epithelia of the fish adapted to concentrated seawater[J]. Zoological Science, 2000, 17(2):149-160.
[6] Tsai J C, Hwang P P. Effects of wheat germ agglutinin and colchicine on microtubules of the mitochondria-rich cells and Ca2+uptake in tilapia(Oreochromis mossambicus)larvae[J]. Journal of Experimental Biology, 1998, 201(15):2263-2271.
[7] Zydlewski J, Mccormick S D. Developmental and environmental regulation of chloride cells in young American shad,Alosa sapidissima[J]. Journal of Experimental Zoology, 2010,290(2):73-87.
[8] Fernandes M N,Perna S A,Moron S E. Chloride cell apical surface changes in gill epithelia of the armoured catfish Hypos tomus plecostomus during exposure to distilled water[J].Journal of Fish Biology,2010, 52(4):844-849.
[9] Li J E, Xu X J, Qu Y J, et al. Study on the gill structure and the respiratory area of chu's croaker Nibea coibor[J]. South China Fisheries Science,2008, 4(1):22-27.[李加儿,许晓娟,区又君,等.浅色黄姑鱼鳃结构及其呼吸面积的研究[J].南方水产科学,2008, 4(1):22-27.]
[10] Zhao F, Yang G, Zhang T, et al. Characters of morphology,distribution and quantity of branchial chloride cells of juvenile Acipenser sinensis acclimated in freshwater and brackish water[J]. Marine Fisheries,2016, 38(1):35-41.[赵峰,杨刚,张涛,等.淡水和半咸水条件下中华鲟幼鱼鳃上皮泌氯细胞的形态特征与数量分布[J].海洋渔业,2016, 38(1):35-41.]
[11] Bury N R, Grosell M. Waterborne iron acquisition by a freshwater teleost fish, zebrafish Danio rerio[J]. Journal of Experimental Biology, 2003, 206(19):3529-3535.
[12] Goss G G, Perry S F, Fryer J N, et al. Gill morphology and acid-base regulation in freshwater fishes[J]. Comparative Biochemistry and Physiology Part A Molecular and Integrative Physiology, 1998, 119(1):107-115.
[13] Wilson J M, Laurent P. Fish gill morphology:inside out[J].Journal of Experimental Zoology, 2002, 293(3):192-213.
[14] Perry S F. The chloride cell:structure and function in the gills of freshwater fishes[J]. Annual Review of Physiology,1997, 59(59):325-347.
[15] Yue X J, Wang D Q, Liu S P, et al. Population genetic structure of three schizothoracins from Nujiang River in southwestern China[J]. Acta Ecologica Sinica, 2010, 30(23):6418-6429.[岳兴建,汪登强,刘绍平,等.怒江三种裂腹鱼属鱼类种群遗传结构[J].生态学报,2010, 30(23):6418-6429.]
[16] Yu M, Zhang D, Hu P, et al. Divergent adaptation to Qinghai-Tibetan Plateau implicated from transciptome study of Gymnocypris dobula and Schizothorax nukiangensis[J].Biochemical Systematics and Ecology, 2017, 71(1):97-105.
[17] Chen W, Du K, He S. Genetic structure and historical demography of Schizothorax nukiangensis(Cyprinidae)in continuous habitat[J]. Ecology and Evolution, 2015, 5(4):984-995.
[18] Li W, Liu Y, Xu Q. Complete mitochondrial genome of Schizothorax nukiangensis Tsao(Cyprinidae:Schizothorax)[J]. Mitochondrial DNA Part A, 2016, 27(5):3549-3550.
[19] Fang J, Pan K C, Deng T H. A scanning electron microscopical observation of the gill of Schizothorax prenanti(Schizothorax)[J]. Journal of Sichuan Agricultural University,2004, 22(2):196-198.[方静,潘康成,邓天怀.齐口裂腹鱼鳃表面结构扫描电镜观察[J].四川农业大学学报,2004,22(2):196-198.]
[20] Guo S H, Wang L C. A scanning electron microscopical study of the gill surface of the comon carp, Cyprinus carpio[J]. Acta Hydrobiologica Sinica, 1988, 12(1):54-58.[郭淑华,王良臣.鲤鳃表面结构扫描电镜研究[J].水生生物学报,1988, 12(1):54-58.]
[21] Luo F, Chen L Q, Kang B. Observation of uitrastructure of the gill filament in Juvenile spinibarbus sinensis with scanning electrominc microscope[J]. Journal of Sichuan Agricultural University,2011,29(4):555-559.[罗芬,陈礼强,康斌.中华倒刺鳃幼鱼鳃的扫描电镜观察[J].四川农业大学学报,2011,29(4):555-559.]
[22] Leguen I. Gills of the medaka(Oryzias latipes):a scanning electron microscopy study[J]. Journal of Morphology, 2018,279(1):97-108.
[23] Luo F, Chen L Q, Kang B. Fine structure of gills in teleost(Pelteobagrus fulvidarco)[J]. Oceanologia et Limnologia Sinica,2011,42(4):488-494.[罗芬,陈礼强,康斌.黄颡鱼(Pelteobagrus fulvidraco)鳃的超微结构研究[J].海洋与湖沼,2011,42(4):488-494.]
[24] Lee T H, Hwang P P, Lin H C, et al. Mitochondria-rich cells in the branchial epithelium of the teleost, Oreochromis mossambicus, acclimated to various hypotonic environments[J].Fish Physiology, 1996, 15(6):513-523.
[25] Pisam M, Caroff A, Rambourg A. Two types of chloride cell in the gill epithelium of a freshwater-adapted euryhaline fish,Lebistes reticulatus:their modifications during adaptation to seawater[J]. American Journal of Anatomy, 1987, 179(1):40-50.
[26] Wilson J M,Laurent P,Tufts B L,et al. NaCl uptake by the branchial epithelium in freshwater teleost fish:an immunological approach to ion-transport protein localization[J].Journal of Experimental Biology, 2000, 203(15):2279-2296.
[27] Long H,Chen J W,Fu Y S,et al. Microscopic observation in gill of six species of fish[J]. Journal of Hydroecology, 2008,28(2):39-40.[龙华,陈建武,付元帅,等. 6种鱼鳃的显微观察[J].水生态学杂志,2008, 28(2):39-40.]
[28] Wright D E. Morphology of the gill epithelium of the Lungfish, Lepidosiren paradoxa[J]. Cell and Tissue Research, 1974,153(3):365-381.
[29] Kumari U, Yashpal M, Mittal S, et al. Surface ultrastructure of gill arches and gill rakers in relation to feeding of an Indian major carp, Cirrhinus mrigala[J]. Tissue Cell, 2009,41(5):318-325.
[30] Elsheikh E H. Scanning electron microscopic studies of gill arches and rakers in relation to feeding habits of some fresh water fishes[J]. The Journal of Basic&Applied Zoology,2013,66(3):121-130.
[31] Goss G G, Adamia S, Galvez F. Peanut lectin binds to a subpopulation of mitochondria-rich cells in the rainbow trout gill epithelium[J]. Ameican Journal of Physiology, 2001,281(5):1718-1725.
[32] Pisam M, Massa F, Jammet C, et al. Chronology of the appearance of(3, A, and a mitochondria-rich cells in the gill epithelium during ontogenesis of the brown trout(Salmo trutta)[J]. The Anatomical Record, 2000, 259(3):301-311.
[33] Pisam M, Le M C, Auperin B, et al. Apical structures of"mitochondria-rich"alpha and beta cells in euryhaline fish gill:their behaviour in various living conditions[J]. The Anatomical Record, 1995,241(1):13.
[34] Foskett J K, Scheffey C. The chloride cell:definitive identification as the salt-secretory cell in teleosts[J]. Science, 1982,215(4529):164-166.
[35] Carmona R,Garcia-Gallego M,Sanz A, et al. Chloride cells and pavement cells in gill epithelia of Acipenser naccarii:ultrastructural modifications in seawater-acclimated specimens[J]. Journal of Fish Biology, 2004, 64(2):553-566.