Like many children, I was fascinated with the ocean and its wildlife, whether along the beach and jetties, or in tidepools, coral reefs, submarine-explored depths, and surface waters. Few of the teleost types captured my imagination as did the billfish: marlins, spearfish, sailfish, and swordfish. Swift, strong, and sleek, a billfish was exactly the kind of swimmer that I wished to be, in my local summer competitions and meets. What a shame that these beautiful wild animals so frequently end up struggling at the end of a Hemingway-wannabe fisherman’s line, dying on the deck of a fishing boat, or mounted, staring in glassy-eyed reproach, on the wall of a sports bar.
Blue Marlin, Makaira nigricans
Watercolor sketch by Barn Owl
Although billfish, unlike birds and mammals, are ectothermic, they are capable of generating heat through specializations of certain muscle cells, a process called non-shivering thermogenesis. In the billfish families Xiphiidae and Istiophoridae, the extraocular superior rectus muscle, which in most vertebrates acts to move the eyeball, has undergone evolutionary modifications, such that some of its cells act as heaters for the retinas and brain. In an ultrastructural and biochemical study, Block and colleagues (1994) showed that the proteins required to produce cycles of calcium release and reuptake are located in the sarcoplasmic reticulum of the specialized heater cells of Blue Marlins (Makaira nigricans) and Swordfish (Xiphias gladius). In most skeletal muscle cells, calcium fluxes are used to generate the force of contraction; in billfish heater cells, calcium fluxes are proposed to increase respiration by the mitochondria, thus generating heat. Heater organs can warm the temperature of the brain and eyes of a billfish 14°C above ambient temperature, an essential anatomical and physiological adaptation in these pelagic predators.
Muscles in all animals produce heat to some extent, but in the billfish heater cells, non-shivering thermogenesis occurs at the expense of contractile force. Accordingly, heater cells lack the orderly arrays of myofibrils, which are characteristic of force-generating skeletal muscle. To identify other adaptations in the heater cells that occurred in the evolutionary transformation from fast-contracting extraocular muscle fibers to thermogenic organ, Morrissette and colleagues (2003) characterized calcium transport proteins, calcium fluxes, and neurotransmission in heater organs isolated from Blue Marlins. First, they showed that the ryanodine receptor expressed in heater cells was the same type (RyR1-slow) as that expressed in slow-twitch skeletal muscles of other fish species. Heater cells were also shown to express the SERCA1 isoform of the calcium-ATPase pump, similar to that found in the fast-twitch swimming muscles of Blue Marlins and Bluefin Tuna. RyR1 and SERCA1 are both located in the sarcoplasmic reticulum (SR) of muscle cells and the modified heater cells, where they function to release sequestered calcium (RyR1), and pump it back into this organelle (SERCA1). The researchers visualized calcium cycling in SR vesicles isolated from marlin heater cells, using the fluorescent dye fura-2, and their analyses led them to propose the model diagrammed below.
Model for thermogenesis in heater cells (from Morrissette et al., 2003)
In billfish, the heater organs are located between the two superior rectus muscles that move the eyeballs, and like these extraocular muscles, receive innervation from the oculomotor nerve (cranial nerve III). Morrissette and colleagues used antibodies against acetylcholine receptors (AChR), as well as fluorescent alpha-bungarotoxin, to characterize the synapse between heater cells and the oculomotor nerve. They found that, much like skeletal muscle fibers, the heater cells contain large clusters of AChR on their surface, in the form of “endplates” to maximize electrical coupling with the oculomotor nerve endings. This allows for neural control of thermogenesis, through depolarization of the heater cells, followed by calcium cycling and ATP turnover in the abundant mitochondria. The marlin heater cell study also has relevance to the human muscle disorder, malignant hyperthermia, which is caused by a mutation in a ryanodine receptor gene.
>=++> First in the “Fish on Friday” series
Block, B.A., O’Brien, J., and Meissner, G. (1994). Characterization of the sarcoplasmic reticulum proteins in the thermogenic muscles of fish. J. Cell Biology 127(5), 1275-1287.
Morrissette, J.M. (2003). Characterization of ryanodine receptor and Ca2+-ATPase isoforms in the thermogenic heater organ of blue marlin (Makaira nigricans). Journal of Experimental Biology, 206(5), 805-812. DOI: 10.1242/jeb.00158