Department of Biology, University of Pennsylvania, Philadelphia, PA.
The Whitman Center, Marine Biological Laboratory, Woods Hole, MA.
J Gen Physiol. 2018 Jan 2;150(1):127-143. doi: 10.1085/jgp.201711760. Epub 2017 Dec 19.
Type I males of the Pacific midshipman fish () vibrate their swimbladder to generate mating calls, or "hums," that attract females to their nests. In contrast to the intermittent calls produced by male Atlantic toadfish (), which occur with a duty cycle (calling time divided by total time) of only 3-8%, midshipman can call continuously for up to an hour. With 100% duty cycles and frequencies of 50-100 Hz (15°C), the superfast muscle fibers that surround the midshipman swimbladder may contract and relax as many as 360,000 times in 1 h. The energy for this activity is supported by a large volume of densely packed mitochondria that are found in the peripheral and central regions of the fiber. The remaining fiber cross section contains contractile filaments and a well-developed network of sarcoplasmic reticulum (SR) and triadic junctions. Here, to understand quantitatively how Ca is managed by midshipman fibers during calling, we measure (a) the Ca pumping-versus-pCa and force-versus-pCa relations in skinned fiber bundles and (b) changes in myoplasmic free [Ca] (Δ[Ca]) during stimulated activity of individual fibers microinjected with the Ca indicators Mag-fluo-4 and Fluo-4. As in toadfish, the force-pCa relation in midshipman is strongly right-shifted relative to the Ca pumping-pCa relation, and contractile activity is controlled in a synchronous, not asynchronous, fashion during electrical stimulation. SR Ca release per action potential is, however, approximately eightfold smaller in midshipman than in toadfish. Midshipman fibers have a larger time-averaged free [Ca] during activity than toadfish fibers, which permits faster Ca pumping because the Ca pumps work closer to their maximum rate. Even with midshipman's sustained release and pumping of Ca, however, the Ca energy cost of calling (per kilogram wet weight) is less than twofold more in midshipman than in toadfish.
太平洋鲭鱼()的 I 型雄性通过振动鳔来产生求爱声,即“嗡嗡声”,吸引雌性到它们的巢中。与大西洋蟾蜍鱼()产生的间歇叫声不同,后者的占空比(呼叫时间除以总时间)仅为 3-8%,鲭鱼可以连续鸣叫长达一个小时。在 100%占空比和 50-100 Hz(15°C)的频率下,包围鲭鱼鳔的超快肌肉纤维可能在 1 小时内收缩和放松多达 360,000 次。这种活动的能量由大量密集堆积的线粒体提供,这些线粒体存在于纤维的外周和中央区域。纤维的剩余横截面包含收缩丝和发达的肌浆网(SR)和三联体结网络。在这里,为了定量了解鲭鱼纤维在鸣叫过程中如何管理 Ca,我们测量了(a)去垢纤维束中的 Ca 泵浦与 pCa 和力与 pCa 关系,以及(b)用 Ca 指示剂 Mag-fluo-4 和 Fluo-4 微注射单个纤维刺激活动期间细胞浆游离 [Ca](Δ[Ca])的变化。与蟾蜍鱼一样,鲭鱼的力-pCa 关系相对于 Ca 泵浦-pCa 关系强烈右移,并且在电刺激期间以同步而不是异步的方式控制收缩活性。然而,与蟾蜍鱼相比,每一个动作电位的 SR Ca 释放大约小 8 倍。与蟾蜍鱼纤维相比,活动期间鲭鱼纤维的平均游离 [Ca] 较大,这使得 Ca 泵能够更快地工作,因为 Ca 泵更接近其最大速率。然而,即使鲭鱼持续释放和泵出 Ca,其鸣叫的 Ca 能量成本(每公斤湿重)也比蟾蜍鱼低不到两倍。