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L. C. Rome is in the Department of Biology of the University of Pennsylvania, Philadelphia, PA 19104; S. L. Lindstedt is in the Dept. of Biological Sciences at Northern Arizona University, Flagstaff, AZ 86011.
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Abstract |
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Introduction |
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 Top Introduction What's needed for speed?Rattling in snakesSpeed costs葉he trade-offs for...The trade-off for energetic...Trade-off for space葉he zero-sum...Mutually exclusive designsThe design for continuous...References |
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Perhaps the most extreme set of modifications is seen in those muscles that operate at very high frequencies. Our laboratories, both in collaboration with each other and separately (in collaboration with other groups), have been examining modifications and trade-offs in two remarkable examples of rapid muscles—the sound-producing swim bladder muscle of toadfish (which is the fastest known vertebrate muscle) and the tail shaker muscle of rattlesnake (certainly the most feared and one distinguished by its endurance).
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What's needed for speed? |
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TopIntroductionWhat's needed for speed?Rattling in snakesSpeed costs葉he trade-offs for...The trade-off for energetic...Trade-off for space葉he zero-sum...Mutually exclusive designsThe design for continuous...References |
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To better understand these modifications, we (9) examined the changes in physiological properties of different fiber types from toadfish because the muscle activation-relaxation rates vary by ~50-fold between locomotory and sonic fiber types. Toadfish red muscle (used for slow, steady swimming at ~2Hz) has a twitch half-width (time duration at the 50% force level) of ~500 ms, compared with ~200 ms for white muscle (used for burst swimming at ~5Hz) and ~10 ms for the swim bladder muscle (Fig. 1A
, top).
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, steps 1 and 4). Second, myosin cross bridges must attach to actin and generate force soon after the calcium level rises and then detach and stop generating force soon after the calcium level falls (Fig. 2, steps 2, 3, 5, and 6).
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, which shows that both durations sped up in parallel by ~50-fold between the slow-twitch red fibers and the superfast-twitch swim bladder fibers.
The significance of a fast Ca2+ transient is most apparent during repetitive stimulation. During stimulation of slow red muscle at a modest 3.5 Hz (Fig. 3), the time course of Ca2+ uptake is so slow that Ca2+ concentration ([Ca2+ ]) does not have time to return to baseline between stimuli. Even the lowest myoplasmic [Ca2+] between stimuli was above the threshold required for force generation in this fiber type, thus resulting in a partially fused tetanus. By contrast, the swim bladder's Ca2+ transient is so rapid that even with 67-Hz stimulation, the [Ca2+] return to baseline between stimuli is complete (Fig. 3; note the 50x faster time base). In addition, [Ca2+ ] is below the threshold for force generation more than one-half of the time in all but the first stimulus. Hence, the Ca2+ transient is sufficiently rapid to permit the oscillation in force required for sound production.
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, step 5). Indeed, kinetic modeling (9) indicates that if the swim bladder troponin had the same off-rate for Ca2+ (koff) estimated for fast-twitch fibers of frog (115 s-1), then occupancy of its troponin sites with Ca2+ would not decline sufficiently rapidly to permit the observed rapid fall in force. To assess possible modifications in the Ca2+ -troponin control system, the force-pCa relationship (force as a function of [Ca2+ ]) was measured in permeabilized ("skinned") muscle fibers. A right shift (decreased Ca2+ sensitivity) was found in the curves for the white fibers with respect to the red fibers, and an even lower Ca2+ sensitivity was found for the superfast fibers. On the basis of the threefold right shift of the force-pCa curve of swim bladder fibers with respect to frog fibers, these results suggest that koff of swim bladder troponin is likewise three times faster than that of frog. With this higher koff, the modeled rate of troponin deactivation no longer appears limiting. Thus the less-sensitive troponin with its more rapid koff may be another modification for faster relaxation (9).
The final requirement for force to drop quickly after the dissociation of Ca2+ from troponin is a fast cross-bridge detachment rate (Fig. 2, step 6). Indeed, the maximum velocity of shortening (Vmax, which is thought to be affected by cross-bridge detachment rate) of swim bladder muscle [~12 muscle lengths (ML)/s] is exceptionally fast, 5- and 2.5-fold faster than toadfish red and white muscle. Recently, in collaboration with Yale Goldman's laboratory, we measured the cross-bridge detachment rate directly and found that it is exceptionally fast (~170 s-1 or ~70 times faster than the toadfish red fibers and the well-studied rabbit fast fibers). This fast detachment rate would permit the rapid relaxation rate observed (5).
The toadfish experiments have thus identified three kinetic variables that change progressively as twitch speed increases from the slow twitch of red fibers to the superfast twitch of swim bladder fibers. 1) The duration of the Ca2+ transient must become shorter, which in turn requires more rapid Ca2+ release and reuptake. As discussed in more detail below, this is achieved principally by an increased density of SR Ca2+ pumps (1). 2) Troponin needs a faster off-rate for Ca2+, which requires molecular modification of troponin to a lower affinity type. 3) Cross bridges must detach more rapidly, which involves molecular modification of myosin (5).
Changes in all of these parameters in concert enable swim bladder fibers to perform mechanical work at high operating frequencies. Sound production requires mechanical work to produce sound energy and to overcome frictional losses in the sound-producing system. Work-loop experiments show that swim bladder fibers can perform work at oscillation frequencies in excess of 200 Hz at 25°C, the highest frequency for work production recorded for any vertebrate muscle (9). By contrast, locomotory muscles lack the combination of fast Ca+2 pumping and fast cross-bridge cycling necessary to generate work at these high frequencies. The highest frequency for vertebrate locomotory muscles is an order of magnitude lower, 25–30 Hz for mouse and lizard fast-twitch muscles at 35°C, whereas the red and white muscle of toadfish cannot generate work at >15 Hz.
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Rattling in snakes |
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TopIntroductionWhat's needed for speed?Rattling in snakesSpeed costs葉he trade-offs for...The trade-off for energetic...Trade-off for space葉he zero-sum...Mutually exclusive designsThe design for continuous...References |
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At 16°C, the shaker fibers have a very rapid Ca2+ transient (half-width = 4–5 ms), which is only 1–2 ms slower than that of the swim bladder (Fig. 1B, top). However, the twitch duration of the shaker muscle twitch is far longer (half-width = 25 vs. 10 ms) than that of swim bladder (Fig. 1B, top). This slower twitch likely reflects the effects of a slower cross-bridge detachment (the shaker Vmax of ~7 ML/s is only about one-half that of the swim bladder) and probably a slower troponin koff. This analysis suggests that in fact all three systems, not just the Ca+2 transient, must be very rapid to produce the fastest contractions. Thus, at 15°C, shaker fibers can be stimulated up to only ~20 Hz before force begins to summate. Accordingly, rattling frequency at 15°C is only ~30 Hz, although unlike toadfish, these snakes may never be active at temperatures this low.
To provide faster contractions and rattling frequencies, these reaction rates must be sped up. This is accomplished by an increase in muscle temperature. At 35°C, at which snakes rattle at 90 Hz, the Ca2+ transient (Fig. 1) and Vmax (18 ML/s) are even faster than those of the swim bladder muscle at 15°C. In addition, koff is likely very rapid as well. The resulting briefer twitch (half-width = 8–9 ms; Fig. 1B) enables the shaker fibers to be stimulated at high frequencies without complete fusion of force and to perform the requisite mechanical work at 90 Hz. The similarity of the modifications in this sound-producing muscle to those in toadfish is suggestive of convergent evolution, supporting the contention that these modifications are necessary for high-frequency operation. Although somewhat slower than the swim bladder at a given temperature, the shaker muscle can operate continuously for hours, which, as we will see, requires additional modifications.
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Speed costs—the trade-offs for speed |
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TopIntroductionWhat's needed for speed?Rattling in snakesSpeed costs葉he trade-offs for...The trade-off for energetic...Trade-off for space葉he zero-sum...Mutually exclusive designsThe design for continuous...References |
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The trade-off for energetic cost of contraction |
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TopIntroductionWhat's needed for speed?Rattling in snakesSpeed costs葉he trade-offs for...The trade-off for energetic...Trade-off for space葉he zero-sum...Mutually exclusive designsThe design for continuous...References |
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). Fibers used for high frequencies have extraordinarily high ATP utilization rates when active because the rate of ATP utilization by both of these components is extremely rapid. For instance, swim bladder fibers appear to pump Ca2+ back into the SR at ~50 times the rate of red muscle (9). Thus the swim bladder fiber Ca2+ pumps use ATP 50-fold faster than those of the red muscle. We have further found that the cross bridges of swim bladder fibers use ATP about six times faster (when expressed on a volume basis) than red muscle fibers (5). Thus, during rapid stimulation (where Ca2+ is being continuously pumped and cross bridges are continuously generating force and splitting ATP), the swim bladder will use ATP at a rate between 6- and 50-fold faster than the red muscle (because the relative contribution of Ca2+ pumps and cross bridges to the total ATP utilization is unknown, only a range can be given.) |
Trade-off for space—the zero-sum game |
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TopIntroductionWhat's needed for speed?Rattling in snakesSpeed costs葉he trade-offs for...The trade-off for energetic...Trade-off for space葉he zero-sum...Mutually exclusive designsThe design for continuous...References |
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Only a very small volume of the muscle fiber is typically devoted to fuel storage. The combined volume of lipids and glycogen is usually under 3%. The remainder of the muscle fiber volume is occupied by three structures—myofibrils, SR, and mitochondria in various proportions. Because these structures collectively make up nearly 100% of the fiber, every muscle fiber type must exist as a point on a single plane of a three-dimensional graph depicting these muscle components (Fig. 4). Hence, any increase in one structure (and its concomitant function) must be at the expense of another.
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The SR is important for turning muscle on and off. The speed of relaxation, and more particularly, the speed at which Ca2+ is pumped back into the SR, is critical in setting the maximum frequency at which a muscle can operate. Although there are different Ca2+ pump isoforms (named SERCA1 and SERCA2; Ref. 12), in general the speed at which Ca2+ is pumped back into the SR is set by the number of Ca2+ pumps. Because the Ca2+ pump density on the SR membrane is often maximal in fast fibers, the number of Ca2+ pumps is tightly correlated to the volume taken up by the SR. Thus the swim bladder fibers' ability to sequester Ca2+ 50 times faster than red fibers requires a high SR volume (30%) (1). Similarly, the SR volume in shaker fibers of rattlesnakes is ~26% (10).
Finally, if the activity is to be sustained rather than intermittent, aerobic metabolism is required to replenish the ATP used during contraction. The amount of O2 consumed and ATP produced is again tightly coupled to the mitochondrial volume. In mammals, in which it has been studied most extensively, mitochondria on average consume 5 ml O2 per cm3 of mitochondria per minute. Assuming a P-to-O2 ratio of 6, this is equivalent to an ATP production rate of 1.3 mM ATP
cm-3min-1. The requirement of continuous operation obviously requires increased mitochondria volume, which in turn comes at the cost of space for myofibrils. Toadfish call intermittently. Hence, they do not rely heavily on aerobic metabolism, and only 4% of their muscle volume is devoted to mitochondria (1). By contrast, rattlesnakes shake their tails continuously for hours at a time, requiring a very high mitochondrial density—26% (10).
In a sense, cellular structures are competing for space in muscle fibers. Increases in SR and mitochondrial volumes necessarily translate into reduced myofibrillar volume and hence, lower force. In muscle fibers used at low frequencies, however, the rate of Ca2+ uptake is sufficiently slow, so that relatively little SR is required, thus effectively removing the SR from the space competition. Furthermore, because the SR uses little ATP, few mitochondria are necessary to supply ATP to the Ca2+ pumps. Thus, even in highly aerobic muscle such as the slow-twitch red muscle of swimming fish, the myofilament volume is reduced only to ~70%—still allowing for significant force generation.
In contrast, the "zero-sum game" becomes a significant factor in muscles designed to operate at high frequencies, both because of the large volume that must be devoted to SR and because of the large number of mitochondria necessary to supply ATP to the Ca2+ pumps and the cross bridges. For instance, the aerobic, high-frequency shaker muscle of rattlesnake, because of the large volume devoted to SR and mitochondria, has only 31% myofilaments (this muscle also contains an extraordinary amount of glycogen, which makes up the bulk of the ~17% of the muscle volume not accounted for by myofibrils, SR, and mitochondria). The faster (500 Hz) aerobic sound-producing muscle of cicadas (6) has even fewer myofibrils (22%). The swim bladder muscle of toadfish has a comparatively high myofibrillar volume, 50%, because very few mitochondria are required for its intermittent use (note that the fibers have an unusual annular deposition of myofilaments—the center of which is devoid of myofilaments; Ref. 1). In all three cases, the reduced myofilament volume results in reduction in force.
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Mutually exclusive designs |
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TopIntroductionWhat's needed for speed?Rattling in snakesSpeed costs葉he trade-offs for...The trade-off for energetic...Trade-off for space葉he zero-sum...Mutually exclusive designsThe design for continuous...References |
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P/force). This is caused by both the rapid rate of ATP utilization (ATP) and the low force produced. However, the force produced may be even lower than expected on the basis of the reduced volume of myofibrils because myosin designed to operate at very high speed may intrinsically generate low forces. In collaboration with Yale Goldman's laboratory, we found that in toadfish swim bladder fibers the force generated per cross section of myofibrils is only about one-fourth that generated by locomotory fibers (5). As mentioned above, to relax quickly swim bladder fibers need a high myosin cross-bridge detachment rate constant (g). In locomotory muscles, the attachment rate constant (f) > g, and 60–70% of the cross bridges are attached during isometric contraction, whereas in swim bladder fibers g >> f, and thus only ~10% of the cross bridges are attached [the number of attached cross bridges is equal to f/(f + g)]. Thus, although the force per attached cross bridge is similar for all fiber types, the force production in swim bladder fibers is very low because there are few attached cross bridges. Low force per cross section of myofibril also has been observed in synchronous sound-producing muscle of insects (6), suggesting that this finding may be a general phenomenon.
The fact that necessary trade-offs can lead to mutually exclusive designs is vividly illustrated in toadfish. Neither the red nor the white swimming muscle can physically produce high-frequency sounds because they cannot relax fast enough and thus produce a fused tetanus when stimulated at high frequencies (Fig. 3). By contrast, the combination of high energetic cost and low force production in swim bladder fibers makes their cost of generating force at least 30-fold higher than in red fibers. Hence, these fibers would be incapable of efficiently powering swimming movements that occur at low frequencies (2–5 Hz). Thus both the qualitative and quantitative modifications of muscle necessary for one activity likely make it unsuitable for another activity.
Furthermore, solutions to the competition for space within the fiber may exclude certain designs altogether. Because of the zero-sum game, high performance in certain attributes precludes high performance in other attributes; the underlying structures cannot physically occupy the same space (4, 7). For instance, as seen graphically in Fig. 4, muscle designed to generate the highest forces must necessarily be used at low frequencies and anaerobically (and thus be used intermittently). By contrast, muscles designed to operate continuously at high frequencies must necessarily generate low force. Thus, as shown in Fig. 4, high force (and power) output, continuous aerobic operation, and high-frequency operation are seemingly mutually exclusive. It would seem to be impossible for an animal's muscle to have all three attributes—yet that is precisely what they must have to fly. How is it done?
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The design for continuous high power at high frequencies—beating the zero-sum game |
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TopIntroductionWhat's needed for speed?Rattling in snakesSpeed costs葉he trade-offs for...The trade-off for energetic...Trade-off for space葉he zero-sum...Mutually exclusive designsThe design for continuous...References |
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). Through evolutionary time, important strategies for circumventing the zero-sum game have emerged. In collaboration with Kevin Conley's lab, we have been investigating three general ways that the "game has been beaten." The first two are found in vertebrates, whereas the third, and perhaps the most significant, evolved only in insects.
Temperature increases rates for a fixed volume.
The rates of many biological reactions are very temperature sensitive. Thus any increase in operating temperature results in greater rates for the same amount of structure. This has great importance in two of the systems.
Because mitochondria have an apparent Q10 of 2.2, increasing body temperature from 30 to 40°C results in a 2.2-fold increase in ATP synthetic rates. Functionally, this is equivalent to doubling the effective volume density of mitochondria within the cell. Hence, one reason that many insects are unable to fly without warming up is that they are unable to produce ATP at an adequate rate to power flight (3). High temperature also permits Ca2+ pumps to pump faster, resulting in faster Ca2+ transients and faster relaxing muscles capable of operating at a higher frequency for a given SR volume (Fig. 1). This factor is no doubt important for high-wingbeat-frequency birds (i.e., hummingbirds, 40 Hz) and large insects using synchronous muscle contractions—but as we will see below, even more drastic measures are required for the smallest flying insects, which have frequencies approaching 1,000 Hz (4).
Double-packed mitochondria.
In many flying animals, the sustained weight-specific power requirements of flight muscles are extreme. In hummingbirds, for instance, the flight muscles account for 25% of the animal's body mass and are composed of ~35% mitochondria. When one divides the total O2 consumption by the volume of mitochondria, they consume O2 at about twice the rate of mammals (7–10 vs. 4–5 ml O2cm-3min-1) (11). If hummingbird mitochondria were identical to those of mammals, the flight muscle would have to contain ~70% mitochondria to produce the required ATP for flight, but this would not leave a sufficient volume of myofibrils to generate the required lift. Hummingbirds appear to have achieved the higher mitochondrial O2 consumption rate by having twice the packing of mitochondrial inner membranes (cristae) as is found in mammalian mitochondria. It remains a mystery why this "double packing" is not the norm for mitochondria in general. Importantly, all flying insects have densely packed mitochondria as well, allowing more space to be devoted to myofibrils (2).
Asynchronous muscle.
Although the above two factors help to beat the zero-sum game, it is evidently still not adequate for animals to fly at the highest wingbeat frequencies. No animal can fly at frequencies of >100 Hz with synchronous muscle (6). Perhaps the single greatest space- and energy-saving modification in skeletal muscle is the development of asynchronous muscle. In synchronous muscle, the muscle is activated by release of Ca2+ and deactivated by Ca2+ reuptake, that is, there must be one Ca2+ release and one Ca2+ reuptake for each cycle (Figs. 2,3). By contrast in asynchronous muscle, a single Ca2+ release can keep the muscle "turned on" for many activation-relaxation cycles. The muscle becomes activated by "stretch activation" and becomes deactivated by "shortening deactivation," all this in the presence of nearly constant myoplasmic [Ca2+].
As noted by Josephson and Young (6), insects possessing this type of muscle save space in two ways. The first is a direct saving of space that would otherwise be occupied by SR. For example, synchronous sonic muscles in cicadas, which operate at 500 Hz, have ~34% SR. Asynchronous muscles have <1/10th that volume of SR (6). The second savings is indirect. As noted above, a large amount of ATP is required to release and resequester Ca2+ at high frequencies, and this may rival the amount of ATP that cross bridges use. Thus, in continuously used synchronous muscles, a large volume of mitochondria must be present simply for supplying ATP to the SR for pumping Ca2+. By slowing the Ca2+ pumping rate in asynchronous muscles by more than an order of magnitude, the space occupied by these mitochondria is freed up and can be replaced by both force-generating myofibrils and additional mitochondria whose sole function is supplying ATP for the cross bridges. In this regard it is interesting to note that flight muscles in all flying animals have at least 50% myofibrils (3).
Finally, reducing the amount of ATP used to power Ca2+ pumping not only saves space but also reduces energetic cost (6). This makes work generation during flight cheaper and thus more efficient. This, too, may be an important requirement from an ecological viewpoint.
To conclude, muscles are called on to power a vast array of motor activities. Muscles can be configured in an equally vast number of types by altering important protein isoforms, amounts of structure, and even modes of activation-relaxation (synchronous vs. asynchronous). Because of inherent design trade-offs, configuring a muscle to perform one activity necessarily reduces its ability to perform another activity. At the extremes, this leads to mutually exclusive designs. Thus no one muscle fiber type can perform all activities effectively—a fact that explains why muscle may show the greatest diversity of any tissue.
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Acknowledgments |
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References |
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TopIntroductionWhat's needed for speed?Rattling in snakesSpeed costs葉he trade-offs for...The trade-off for energetic...Trade-off for space葉he zero-sum...Mutually exclusive designsThe design for continuous...References |
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