Matey Victoria, Richards Jeffrey G, Wang Yuxiang, Wood Chris M, Rogers Joe, Davies Rhiannon, Murray Brent W, Chen X-Q, Du Jizeng, Brauner Colin J
Department of Biology, San Diego State University, San Diego, CA, USA.
J Exp Biol. 2008 Apr;211(Pt 7):1063-74. doi: 10.1242/jeb.010181.
Goldfish and crucian carp at low temperature exhibit plasticity in gill morphology during exposure to hypoxia to enhance gas exchange. Hypoxia-induced changes in gill morphology and cellular ultrastructure of the high altitude scaleless carp from Lake Qinghai, China, were investigated to determine whether this is a general characteristic of cold water carp species. Fish were exposed to acute hypoxia (0.3 mg O2 l(-1)) for 24 h followed by 12 h recovery in normoxic water (6 mg O2 l(-1) at 3200 m altitude), with no mortality. Dramatic alterations in gill structure were initiated within 8 h of hypoxia and almost complete by 24 h, and included a gradual reduction of filament epithelial thickness (>50%), elongation of respiratory lamellae, expansion of lamellar respiratory surface area (>60%) and reduction in epithelial water-blood diffusion distance (<50%). An increase in caspase 3 activity in gills occurred following 24 h exposure to hypoxia, indicating possible involvement of apoptosis in gill remodeling. Extensive gill mucous production during hypoxia may have been part of a general stress response or may have played a role in ion exchange and water balance. The large increase in lamellar surface area and reduction in diffusion distance presumably enhances gas transfer during hypoxia (especially in the presence of increased mucous production) but comes with an ionoregulatory cost, as indicated by a 10 and 15% reduction in plasma [Na+] and [Cl-], respectively, within 12-24 h of hypoxia. Within 12 h of hypoxia exposure, ;wavy-convex'-mitochondria rich cells (MRCs) with large apical crypts and numerous branched microvilli were transformed into small ;shallow-basin' cells with a flattened surface. As the apical membrane of MRCs is the site for active ion uptake from the water, a reduction in apical crypt surface area may have contributed to the progressive reduction in plasma [Na+] and [Cl-] observed during hypoxia. The changes in the macro- and ultra-structure of fish gills, and plasma [Na+] and [Cl-] during hypoxia were reversible, showing partial recovery by 12 h following return to normoxia. Although the large morphological changes in the gill observed in the scaleless carp support the hypothesis that gill remodeling during hypoxia is a general characteristic of cold water carp species, the reduced magnitude of the response in scaleless carp relative to goldfish and crucian carp may be a reflection of their more active lifestyle or because they reside in a moderately hypoxic environment at altitude.
金鱼和鲫鱼在低温环境下暴露于低氧环境时，鳃形态会表现出可塑性以增强气体交换。本研究调查了中国青海湖高海拔裸鲤在低氧环境下鳃形态和细胞超微结构的变化，以确定这是否是冷水性鲤科鱼类的普遍特征。将鱼暴露于急性低氧（0.3 mg O₂ l⁻¹）环境中24小时，随后在常氧水中（海拔3200米处6 mg O₂ l⁻¹）恢复12小时，期间无死亡情况。低氧暴露8小时内鳃结构开始发生显著变化，24小时时几乎完成，包括鳃丝上皮厚度逐渐减少（>50%）、呼吸薄片伸长、薄片呼吸表面积增加（>60%）以及上皮水 - 血扩散距离缩短（<50%）。低氧暴露24小时后鳃中半胱天冬酶3活性增加，表明细胞凋亡可能参与了鳃的重塑过程。低氧期间大量的鳃黏液分泌可能是一般应激反应的一部分，或者在离子交换和水平衡中发挥了作用。薄片表面积的大幅增加和扩散距离的缩短可能增强了低氧期间的气体传输（特别是在黏液分泌增加的情况下），但这伴随着离子调节成本，低氧暴露12 - 24小时内，血浆[Na⁺]和[Cl⁻]分别降低了10%和15%。低氧暴露12小时内，具有大顶端隐窝和许多分支微绒毛的“波浪 - 凸起”型富含线粒体细胞（MRCs）转变为表面扁平的小“浅盆”细胞。由于MRCs的顶端膜是从水中主动摄取离子的部位，顶端隐窝表面积的减少可能导致了低氧期间观察到的血浆[Na⁺]和[Cl⁻]的逐渐降低。低氧期间鱼鳃的宏观和超微结构变化以及血浆[Na⁺]和[Cl⁻]的变化是可逆的，恢复到常氧后12小时部分恢复。尽管裸鲤鳃部观察到的大形态变化支持了低氧期间鳃重塑是冷水性鲤科鱼类普遍特征的假设，但裸鲤相对于金鱼和鲫鱼反应程度的降低可能反映了它们更活跃的生活方式，或者是因为它们生活在海拔适度低氧的环境中。
