In parallel with vertebrates, cephalopod molluscs (octopuses, cuttlefish and their kin) have evolved a ‘closed’ circulatory system, composed of pumps and pipes, that more closely resembles our own cardiovascular system than the unplumbed (‘open’) circulations of other invertebrates. During their evolutionary path, cephalopods have also acquired several cardiovascular peculiarities, including possessing three hearts, two of which are dedicated to supplying blood to the gills (the branchial hearts), and one (systemic) heart that pumps blood around the body. Nevertheless, cephalopod hearts share common building blocks with those of vertebrate hearts, so by investigating the cardiac physiology of these molluscs, it may be possible to reveal the foundations of heart function in animals.
Like vertebrate hearts, cephalopod hearts must be tuned to the metabolic demands of the animal, but very little is known about how this may be achieved. In a recent study, Tyson MacCormack and a team of researchers based in Canada and Portugal decided to investigate the compound taurine. Taurine is an amino acid that accumulates in tissues throughout the body and exerts diverse physiological effects in a wide range of organisms. In mammals, it elicits complex effects on the heart: it increases contractility when extracellular calcium levels are low, but at high calcium concentration (as is typical in cephalopod blood) it decreases contractility. In addition, it boosts oxygen consumption and glucose usage of mammalian heart muscle. MacCormack and his colleagues knew that the amino acid had been detected at strikingly high levels in the blood of their chosen cephalopod species, the cuttlefish (Sepia officinalis), so they investigated the impact of taurine on both cardiac mechanical performance and metabolism.
The team developed a method in which the systemic heart was perfused by tubes containing artificial cuttlefish ‘blood’, allowing them to continuously monitor cardiac output (the amount of blood pumped per minute). Having confirmed that the cuttlefish heart was functioning normally, the authors applied taurine to it and the cardiac output halved – as they had expected, knowing that the amino acid decreases contractility when calcium levels are high in mammals. The team then refined this discovery in the next series of experiments, which examined the force production of isolated muscle from both the systemic and branchial hearts. Here, taurine impaired cardiac muscle relaxation, at least when the muscle was electrically stimulated to contract at high rates. Together, these results showed that taurine can considerably depress contractility in the cuttlefish heart, similar to its role in the mammalian heart.
When MacCormack and his colleagues measured the effects of taurine on oxygen consumption in systemic heart muscle, they did not see an obvious impact, although they observed that taurine doubled glucose usage. As this latter effect is similar to that previously reported in mammalian hearts, it suggests that some of the metabolic modulations provided by taurine may have evolved deep in evolutionary history.
By studying an invertebrate, MacCormack and his team provide a refreshing context in which to understand cardiac evolution. Taurine has complicated actions on the heart, and it seems that some of these effects may well be shared across the animal kingdom.
- © 2016. Published by The Company of Biologists Ltd