黑腹绒鼠能量代谢对不同季节和温度的响应
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摘要
本研究以南方常见种之一黑腹绒鼠(Eothenomeys melanogaster)为对象,测定其在不同季节以及在3个不同温度(25±1℃,15±1℃,5±1℃)中驯化0d、7d、14d、21d和28d后体重、体脂、器官重量、能量收支、基础代谢率(BMR)、非颤抖性产热(NST)与褐色脂肪组织(BAT)和肝脏的产热活性等的变化。对黑腹绒鼠在不同季节和不同温度下的生理调节模式进行了研究。主要结果和结论如下：
1.季节波动对黑腹绒鼠的体重和体脂均有显著影响。秋季黑腹绒鼠体重、体脂重量、体脂含量、胴体湿重及胴体干重最高,冬季次之,夏季最低；去脂胴体干重无季节间差异。这一季节动态受温度影响外,还可能与黑腹绒鼠繁殖、食性和栖息地的气候有关。
2.冬季黑腹绒鼠每日摄入能、每日消化能和每日可代谢能均显著高于夏季。且冬季黑腹绒鼠消化道如小肠、大肠的鲜重,胃和盲肠的鲜重及干重均显著大于夏季,表明黑腹绒鼠可能通过消化道重量的适应性提高来延长食物在消化道内的滞留时间或增加吸收面积来保持其高消化率。同时,机体最主要的能量运输器官——心脏的鲜重也在冬季相应的增加,反映了在冬季环境的胁迫中,动物整体能量代谢活性随之增强。
3.黑腹绒鼠在冬季具有较高的BMR和NST,显著高于其他季节,暗示黑腹绒鼠产热速率的调整是其适应季节变化的重要对策之一。黑腹绒鼠BAT的相对重量、线粒体蛋白含量和线粒体COX活力均在冬季显著高于其他季节,夏季为最小值。肝脏的相对重量在夏季偏高,但其线粒体蛋白含量和线粒体COX活力在冬季最高,BAT和肝脏的产热特征季节性变化与代谢率季节变化具有一致性,说明黑腹绒鼠的BAT和肝脏积极参与了季节性驯化中产热的适应性调节。
4.黑腹绒鼠体重在25±1℃、15±1℃和5±1℃分别呈现极显著增加、极显著增加和显著降低的趋势。黑腹绒鼠能量摄入各指标在25±1℃、15±1℃和5±1℃下分别不同程度地降低、增加和上升；而黑腹绒鼠消化率和可代谢能效率在25±1℃、15±1℃中无显著变化,但在5±1℃下显著提高。由此可见,暖温(25±1℃)条件下,动物保留了更多能量用于身体组织的构建和身机能的恢复；较低温度(15±1℃)能够诱导动物增加能量储存为即将来临的冬季作好准备；而低温(5±1℃)胁迫黑腹绒鼠增加能量摄入和消化效率及适量的动用身体内的脂肪以维持能量收支的平衡。
5.25±1℃驯化下,黑腹绒鼠的BMR保持相对稳定,肝脏除线粒体COX活力显著下降,其他活性指标无显著变化；15±1℃驯化中,黑腹绒鼠BMR显著增加,肝脏线粒体蛋白含量和线粒体COX活力均极显著提升；5±1℃使黑腹绒鼠BMR随时间极显著升高,肝脏各产热特征均与时间极显著相关。且通过与不同地区鼠种的比较发现,低温下黑腹绒鼠肝脏线粒体COX活力提高的水平和BMR增加的幅度具有一致性。以上结果进一步表明了肝脏产热能力的增加是BMR提高的一个重要细胞机制。
6.BAT是小型哺乳动物NST的主要产热器官这一论点在本研究中也得到证实：25±1C驯化下,黑腹绒鼠的NST呈下降趋势,BAT相对重量、线粒体蛋白含量和线粒体COX活力也有所下降,但均变化不显著；15±1℃驯化中,黑腹绒鼠NST显著提高,同时BAT各产热特征也与时间显著正相关；而5±1℃下,黑腹绒鼠NST和BAT的各项指标变化最剧烈,均随时间极显著增加。冷驯化下NST的提高幅度没有其BMR明显也不及北方的物种,充分体现了其栖息地的地理位置和气候条件特征。
7.黑腹绒鼠各生理参数在驯化过程中具有一定的时间规律：其体重、能量摄入、BMR、BAT和肝脏的相对重量、线粒体蛋白含量及线粒体COX活力值在3个温度的驯化下随时间均逐渐上升或下降,且大部分指标在21d达到最值,或在21d后仍保持先前趋势但幅度明显变小。说明21d左右可能是黑腹绒鼠新生理稳态形成所需要的时间。
8.黑腹绒鼠体重、能量摄入、代谢率、线粒体蛋白含量及酶活力随季节变化的趋势与在相应温度下的变化模式之间存在很大的关联性。如在寒冷的冬季,黑腹绒鼠体重比秋季显著降低,而低温(5±1℃)下体重也呈降低的趋势。黑腹绒鼠摄入能冬季>秋季>春季>夏季,具有随温度上升而下降的趋势；相应地,摄入能和食物的利用率在暖温(25±1℃)时下降,在较低温度(15±1℃)时显著增加,而在低温(5±1℃)时则迅速增加。以上结果在一定程度上说明了温度因子在自然季节驯化中具有至关重要的地位。
黑腹绒鼠为适应不同的季节和温度环境,通过调控自身在细胞水平、器官组织以及整体上的能量代谢和产热活力来维持恒定的体温和正常的生理机能,这对其生存、繁殖和进化具有重大的意义。黑腹绒鼠代谢和产热模式的特点与其自身的生活习性以及生境条件密切相关。温度是黑腹绒鼠生理生态特征季节变化中的一个重要诱导因子,但与其他生态因子如光周期、食物等的协同作用机制还有待于进一步深入研究。
In order to understand the physiological strategy of this specie for season and ambient temperature deeply, energy metabolism and thermogenesis were studied in Melano-bellied Oriental Vole (Eothenomys melanogaster) which is a familiar species in SouthChina, involve the energy intake, organ mass, basal metabolic rate (BMR), non-shivering thermogenesis (NST), thermogenic property of brown adipose tissue (BAT) and liver under different temperature (25±1℃,15±1℃,5±1℃) 0d,7d,14d, 21d,28d. At the same time, the seasonal changes of these parameters were measured in E. melanogaster. The main results and conclusions are as follows:
1. The seasonal variation effected the body mass and body fat mass chang significantly in E. melanogaster. The body mass, body fat mass, the percentage of body fat, wet carcass mass and dry carcass mass showed higher in fall than in winter, lowest is summer except fat-free carcass mass which had no seasonal variation. These dynamic change may be influened not only by environment temperature but also propagate, feeding habit and climate in the habitat of E. melanogaster.
2. E. melanogaster in winter showed higher energy intake, digested energy and metabolizable energy than in other seasons as well as digestive track mass increased significantly in winter involved wet mass of big intestine and small intestine, wet and dry mass of stomach and ceacum, which indicates that shape of digestive track may help E. melanogaster have more digestive area for food or more time for food to stay in tract thus kept its high digestibility. Heart mass which is the most important power organ also showed highest level in winter, which could indicate that the metabolic rate in Melano-bellied Oriental Vole improved under pressure of winter.
3. Significant difference of metabolic rate was found among different seasons in E. melanogaster. The BMR and NST were all highest in winter, and lowest in summer which showed that heat produce is one of important countermeasure for adapting environmental variation. The relative mass, content of mitochondrial protein (MP) and cytochrome C oxidase (COX) activity of mitochondria in brown adipose tissue (BAT) are on higher level in winter. Though the relative mass of liver increased in summer, the COX activity and MP content of liver all increased to highest in winter. The seasonl change of BAT and liver keeped consistent with metabolic rate in E. melanogaster, which indicates BAT and liver participate in adjusting of thermogenesis.
4. Increasing, increasing and decreasing trend were found in body mass respectively under 25±1℃,15±1℃and 5±1℃. Energy intake under 25±1℃,15±1℃and 5±1℃shows decreas, increase and increase respectively. Digestibility and efficiency of metabolizable energy intake didn't show any change under 25±1℃and 15±1℃, but improved significantly after cold acclimation (5±1℃). From this, it can be seen that E. melanogaster could save enough energy for organism construction and functional recovery when under warm temperature, store up more energy to prepeare for coming winter when under lower temperature, reduce body mass and increase energy intake also digestibility to keep balance between energy in and out when under low temperature.
5. E. melanogaster under the acclimation of 25±1℃showed stable level in BMR, relative mass and MP content of liver, however reduced in mitochondrial COX activity. Under 15±1℃, BMR increased when the MP content as well as mitochondrial COX activity. Low temperature (5±1℃) induced Melano-bellied Oriental Vole increase BMR and thermogenic capability of liver according to the time of acclimation. Compared with speices in other area, it will be found that the increasing rate of BMR have big relationship with the improving degree of COX activity in liver. What is said above confirmed that change of liver property is one of important cellular mechanism for BMR.
6. BAT is the main heat-producing organ for NST, that was also proved in this study. Decreasing trend was found in NST as well as relative mass and mitochondrial COX activity of BAT but all without significant difference under 25±1℃acclimation. Incresing trend was detected in NST by 15±1℃acclimation when every property of BAT showed marked increase. Cold acclimation (5±1℃) induced either NST or BAT activity increase largely. It was also found that the changing range of NST in cold acclimation in E. melanogaster was smaller than their BMR and also smaller than NST in species of NorthChina. It reflected the character of geography and climate in the habitat of Melano-bellied oriental vole.
7. The experiment showed that every parameter had rule in the acclimated-time. The parameters increased or decreased while the time of acclimation delayed involve body mass, BMR relative mass, MP content, mitochondrial COX activity of liver and BAT in E. melanogaster,then all of them went to maxi-value when 21 days, or went slower after 21 days. It means that Melano-bellied oriental vole need about 21 days to form new physiological steady state.
8. There is a great relationship between seasonal variation and change in different temperature in E. melanogaster. For example, body mass in E. melanogaster decrease in cold winter versus fall, when it also showed decrease under cold acclimation (5±1℃). The energy intake in E. melanogaster showed winter>fall> spring> summer which means it increase with temperatre decrease. Accordingly, the energy intake and digestibility showed decrease in warm temperature (25±1℃), increase in lower temperature (15±1℃) and increase largely in cold acclimation (5±1℃). It indicated to a certain degree that temperature may play an indispensable and crucial role in seasonal acclimation.
In short, in order to retain body temperature and normal physiological function in different season and temperature, E. melanogaster exhibited adaptive physiological regulations from organism to cellular levels, which is of great significance for animal to survive, reproduce and evolve in natural environment. There was a special mode of metabolic and thermogenic mode in E. melanogaster, which close connect with its life style and habitat environment. Temperature is an important inducement for seasonal variation in animal's physiological ecology, however, it needs further investigation to study mechanism of concerted reaction between temperature and other ecological factor like food, photoperiod and so on.
1.季节波动对黑腹绒鼠的体重和体脂均有显著影响。秋季黑腹绒鼠体重、体脂重量、体脂含量、胴体湿重及胴体干重最高,冬季次之,夏季最低；去脂胴体干重无季节间差异。这一季节动态受温度影响外,还可能与黑腹绒鼠繁殖、食性和栖息地的气候有关。
2.冬季黑腹绒鼠每日摄入能、每日消化能和每日可代谢能均显著高于夏季。且冬季黑腹绒鼠消化道如小肠、大肠的鲜重,胃和盲肠的鲜重及干重均显著大于夏季,表明黑腹绒鼠可能通过消化道重量的适应性提高来延长食物在消化道内的滞留时间或增加吸收面积来保持其高消化率。同时,机体最主要的能量运输器官——心脏的鲜重也在冬季相应的增加,反映了在冬季环境的胁迫中,动物整体能量代谢活性随之增强。
3.黑腹绒鼠在冬季具有较高的BMR和NST,显著高于其他季节,暗示黑腹绒鼠产热速率的调整是其适应季节变化的重要对策之一。黑腹绒鼠BAT的相对重量、线粒体蛋白含量和线粒体COX活力均在冬季显著高于其他季节,夏季为最小值。肝脏的相对重量在夏季偏高,但其线粒体蛋白含量和线粒体COX活力在冬季最高,BAT和肝脏的产热特征季节性变化与代谢率季节变化具有一致性,说明黑腹绒鼠的BAT和肝脏积极参与了季节性驯化中产热的适应性调节。
4.黑腹绒鼠体重在25±1℃、15±1℃和5±1℃分别呈现极显著增加、极显著增加和显著降低的趋势。黑腹绒鼠能量摄入各指标在25±1℃、15±1℃和5±1℃下分别不同程度地降低、增加和上升；而黑腹绒鼠消化率和可代谢能效率在25±1℃、15±1℃中无显著变化,但在5±1℃下显著提高。由此可见,暖温(25±1℃)条件下,动物保留了更多能量用于身体组织的构建和身机能的恢复；较低温度(15±1℃)能够诱导动物增加能量储存为即将来临的冬季作好准备；而低温(5±1℃)胁迫黑腹绒鼠增加能量摄入和消化效率及适量的动用身体内的脂肪以维持能量收支的平衡。
5.25±1℃驯化下,黑腹绒鼠的BMR保持相对稳定,肝脏除线粒体COX活力显著下降,其他活性指标无显著变化；15±1℃驯化中,黑腹绒鼠BMR显著增加,肝脏线粒体蛋白含量和线粒体COX活力均极显著提升；5±1℃使黑腹绒鼠BMR随时间极显著升高,肝脏各产热特征均与时间极显著相关。且通过与不同地区鼠种的比较发现,低温下黑腹绒鼠肝脏线粒体COX活力提高的水平和BMR增加的幅度具有一致性。以上结果进一步表明了肝脏产热能力的增加是BMR提高的一个重要细胞机制。
6.BAT是小型哺乳动物NST的主要产热器官这一论点在本研究中也得到证实：25±1C驯化下,黑腹绒鼠的NST呈下降趋势,BAT相对重量、线粒体蛋白含量和线粒体COX活力也有所下降,但均变化不显著；15±1℃驯化中,黑腹绒鼠NST显著提高,同时BAT各产热特征也与时间显著正相关；而5±1℃下,黑腹绒鼠NST和BAT的各项指标变化最剧烈,均随时间极显著增加。冷驯化下NST的提高幅度没有其BMR明显也不及北方的物种,充分体现了其栖息地的地理位置和气候条件特征。
7.黑腹绒鼠各生理参数在驯化过程中具有一定的时间规律：其体重、能量摄入、BMR、BAT和肝脏的相对重量、线粒体蛋白含量及线粒体COX活力值在3个温度的驯化下随时间均逐渐上升或下降,且大部分指标在21d达到最值,或在21d后仍保持先前趋势但幅度明显变小。说明21d左右可能是黑腹绒鼠新生理稳态形成所需要的时间。
8.黑腹绒鼠体重、能量摄入、代谢率、线粒体蛋白含量及酶活力随季节变化的趋势与在相应温度下的变化模式之间存在很大的关联性。如在寒冷的冬季,黑腹绒鼠体重比秋季显著降低,而低温(5±1℃)下体重也呈降低的趋势。黑腹绒鼠摄入能冬季>秋季>春季>夏季,具有随温度上升而下降的趋势；相应地,摄入能和食物的利用率在暖温(25±1℃)时下降,在较低温度(15±1℃)时显著增加,而在低温(5±1℃)时则迅速增加。以上结果在一定程度上说明了温度因子在自然季节驯化中具有至关重要的地位。
黑腹绒鼠为适应不同的季节和温度环境,通过调控自身在细胞水平、器官组织以及整体上的能量代谢和产热活力来维持恒定的体温和正常的生理机能,这对其生存、繁殖和进化具有重大的意义。黑腹绒鼠代谢和产热模式的特点与其自身的生活习性以及生境条件密切相关。温度是黑腹绒鼠生理生态特征季节变化中的一个重要诱导因子,但与其他生态因子如光周期、食物等的协同作用机制还有待于进一步深入研究。
In order to understand the physiological strategy of this specie for season and ambient temperature deeply, energy metabolism and thermogenesis were studied in Melano-bellied Oriental Vole (Eothenomys melanogaster) which is a familiar species in SouthChina, involve the energy intake, organ mass, basal metabolic rate (BMR), non-shivering thermogenesis (NST), thermogenic property of brown adipose tissue (BAT) and liver under different temperature (25±1℃,15±1℃,5±1℃) 0d,7d,14d, 21d,28d. At the same time, the seasonal changes of these parameters were measured in E. melanogaster. The main results and conclusions are as follows:
1. The seasonal variation effected the body mass and body fat mass chang significantly in E. melanogaster. The body mass, body fat mass, the percentage of body fat, wet carcass mass and dry carcass mass showed higher in fall than in winter, lowest is summer except fat-free carcass mass which had no seasonal variation. These dynamic change may be influened not only by environment temperature but also propagate, feeding habit and climate in the habitat of E. melanogaster.
2. E. melanogaster in winter showed higher energy intake, digested energy and metabolizable energy than in other seasons as well as digestive track mass increased significantly in winter involved wet mass of big intestine and small intestine, wet and dry mass of stomach and ceacum, which indicates that shape of digestive track may help E. melanogaster have more digestive area for food or more time for food to stay in tract thus kept its high digestibility. Heart mass which is the most important power organ also showed highest level in winter, which could indicate that the metabolic rate in Melano-bellied Oriental Vole improved under pressure of winter.
3. Significant difference of metabolic rate was found among different seasons in E. melanogaster. The BMR and NST were all highest in winter, and lowest in summer which showed that heat produce is one of important countermeasure for adapting environmental variation. The relative mass, content of mitochondrial protein (MP) and cytochrome C oxidase (COX) activity of mitochondria in brown adipose tissue (BAT) are on higher level in winter. Though the relative mass of liver increased in summer, the COX activity and MP content of liver all increased to highest in winter. The seasonl change of BAT and liver keeped consistent with metabolic rate in E. melanogaster, which indicates BAT and liver participate in adjusting of thermogenesis.
4. Increasing, increasing and decreasing trend were found in body mass respectively under 25±1℃,15±1℃and 5±1℃. Energy intake under 25±1℃,15±1℃and 5±1℃shows decreas, increase and increase respectively. Digestibility and efficiency of metabolizable energy intake didn't show any change under 25±1℃and 15±1℃, but improved significantly after cold acclimation (5±1℃). From this, it can be seen that E. melanogaster could save enough energy for organism construction and functional recovery when under warm temperature, store up more energy to prepeare for coming winter when under lower temperature, reduce body mass and increase energy intake also digestibility to keep balance between energy in and out when under low temperature.
5. E. melanogaster under the acclimation of 25±1℃showed stable level in BMR, relative mass and MP content of liver, however reduced in mitochondrial COX activity. Under 15±1℃, BMR increased when the MP content as well as mitochondrial COX activity. Low temperature (5±1℃) induced Melano-bellied Oriental Vole increase BMR and thermogenic capability of liver according to the time of acclimation. Compared with speices in other area, it will be found that the increasing rate of BMR have big relationship with the improving degree of COX activity in liver. What is said above confirmed that change of liver property is one of important cellular mechanism for BMR.
6. BAT is the main heat-producing organ for NST, that was also proved in this study. Decreasing trend was found in NST as well as relative mass and mitochondrial COX activity of BAT but all without significant difference under 25±1℃acclimation. Incresing trend was detected in NST by 15±1℃acclimation when every property of BAT showed marked increase. Cold acclimation (5±1℃) induced either NST or BAT activity increase largely. It was also found that the changing range of NST in cold acclimation in E. melanogaster was smaller than their BMR and also smaller than NST in species of NorthChina. It reflected the character of geography and climate in the habitat of Melano-bellied oriental vole.
7. The experiment showed that every parameter had rule in the acclimated-time. The parameters increased or decreased while the time of acclimation delayed involve body mass, BMR relative mass, MP content, mitochondrial COX activity of liver and BAT in E. melanogaster,then all of them went to maxi-value when 21 days, or went slower after 21 days. It means that Melano-bellied oriental vole need about 21 days to form new physiological steady state.
8. There is a great relationship between seasonal variation and change in different temperature in E. melanogaster. For example, body mass in E. melanogaster decrease in cold winter versus fall, when it also showed decrease under cold acclimation (5±1℃). The energy intake in E. melanogaster showed winter>fall> spring> summer which means it increase with temperatre decrease. Accordingly, the energy intake and digestibility showed decrease in warm temperature (25±1℃), increase in lower temperature (15±1℃) and increase largely in cold acclimation (5±1℃). It indicated to a certain degree that temperature may play an indispensable and crucial role in seasonal acclimation.
In short, in order to retain body temperature and normal physiological function in different season and temperature, E. melanogaster exhibited adaptive physiological regulations from organism to cellular levels, which is of great significance for animal to survive, reproduce and evolve in natural environment. There was a special mode of metabolic and thermogenic mode in E. melanogaster, which close connect with its life style and habitat environment. Temperature is an important inducement for seasonal variation in animal's physiological ecology, however, it needs further investigation to study mechanism of concerted reaction between temperature and other ecological factor like food, photoperiod and so on.
引文
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