Anyone who remembers their basic biology lessons can tell you that adenosine triphosphate (ATP) is a critically important molecule. It’s difficult to envision organic life, as we know it, without this cornerstone of cellular metabolism taking center stage. While alternative molecules might theoretically be able to walk in its shoes, it’s efficiency, scalability, and elegance are such that it’s no mystery how it achieved its highly-conserved ancestral dominance in the tree of life. It’s phosphate lightning in a bottle.
Now, this role as the celebrated “energy currency of cells” is all very well documented and understood but ATP plays another unusual and esoteric role in the waters off the western coast of North America. Here, extracellular ATP takes on a fascinating, new dimension in the interactions between a ubiquitous marine arthropod and its next meal.
One of my favorite courses at UCLA—where I earned my degree in Ecology, Behavior, and Evolution (EBE)—was Chemical Communication, taught by Professor Richard Zimmer. Part of that class centered around some research Prof. Zimmer performed in the 1980s and 1990s involving spiny lobsters, specifically, Panulirus interruptus. Though less well-known than their Maine lobster cousins, spiny lobsters are very easy to find in the waters off the coast of Monterey Bay, California down to the Gulf of Tehuantepec, Mexico. There, they cluster among crevices in rocky reefs; hiding during the day and emerging at night to forage and feed.
In the years before these humble commonplace lobsters caught Zimmer’s attention, another researcher, William E.S. Carr, discovered that a relative of P. interruptus named Panulirus argus possessed olfactory chemoreceptors capable of detecting ATP. Carr, however, stopped short of exploring the broader implications of that finding. He seemed more interested in using that information to explore his hypothesis that, in his own words, the receptors for “transmitters and modulators existing in internal tissues may have evolved from external chemoreceptors of primitive unicellular organisms.“
Zimmer, however, thought Carr’s findings only scratched the surface. There had to be more to it than that, right? Zimmer soon postulated that these ATP receptors might be responsible for mediating behavior in response to environmental signals, particularly signals related to foraging. To that end, Zimmer and his colleagues embarked on a series of rigorous experiments to try and connect ATP sensing to the daily foraging activities of spiny lobsters.
Ultimately, his work would reveal a previously unexplored dimension of ATP’s function in biological systems. When it leaks into the environment, ATP serves as a molecular signal to stimulate spiny lobsters’ search for food. Even a small amount was enough to send the lobsters in the experiments scrambling about in search of the source. Naturally, that finding begged the question: what was it about ATP that made it such a potent and powerful feeding cue for this marine crustaceans?
Zimmer concluded that part of the answer lay in the relative scarcity of ATP within the marine column. In other words, it has a high signal to noise ratio. Though omnipresent inside cells, ATP is exceedingly rare in the external environment. It sticks out like a bright signal among all the other molecular noise swirling about the rocky reefs these lobsters frequent. Detecting it is an unmistakable “x marks the spot” moment and the lobster’s sensory organs are finely tuned to capitalize on it.
Furthermore, Zimmer proposed that the lobsters may have evolved such a strong environmental ATP because of its connection to food quality. When an animal dies and its tissues begin to decompose, the ATP contained within its cells is rapidly transformed into adenine monophosphate (AMP). The same instability that makes ATP such an efficient energy carriers also makes it extremely short lived in dead tissue. Consequently, the presence of ATP in the water column clearly signifies a fresh or injured/vulnerable food source.
The discovery of ATP’s extracellular function out among the rocky reefs of Calfornia and northern Mexico underscores just how much is still out there, waiting to be discovered. Even the most familiar of animals and most ubiquitous of molecules can take on unexpected roles and add so much color to the grand tapestry of life here on Earth.
References and Further Reading
- Fuzessery, Z. M., Carr, W. E., & Ache, B. W. (1978). Antennular chemosensitivity in the spiny lobster, Panulirus argus: studies of taurine sensitive receptors. The Biological Bulletin, 154(2), 226-240. (PDF)
- Johnson, B. R., & Ache, B. W. (1978). Antennular chemosensitivity in the spiny lobster, Panulirus argus: amino acids as feeding stimuli. Marine & Freshwater Behaviour & Phy, 5(2), 145-157.
- Kamerlin SC, Sharma PK, Prasad RB, Warshel A. Why nature really chose phosphate. Q Rev Biophys. 2013 Feb;46(1):1-132. doi: 10.1017/S0033583512000157. Epub 2013 Jan 15. PMID: 23318152; PMCID: PMC7032660.
- Reeder, P. B., & Ache, B. W. (1980). Chemotaxis in the Florida spiny lobster, Panulirus argus. Animal Behaviour, 28(3), 831-839. (PDF)
- Schmidt, M., & Derby, C. D. (2005). Non-olfactory chemoreceptors in asymmetric setae activate antennular grooming behavior in the Caribbean spiny lobster Panulirus argus. Journal of Experimental Biology, 208(2), 233-248. (PDF)
- Zimmer-Faust, R. K. (1993). ATP: A potential prey attractant evoking carnivory. Limnology and oceanography, 38(6), 1271-1275. (PDF)
- Zimmer-Faust, R. K., Gleeson, R. A., & Carr, W. E. (1988). The behavioral response of spiny lobsters to ATP: evidence for mediation by P2-like chemosensory receptors. The Biological Bulletin, 175(1), 167-174. (PDF)
- Zimmer-Faust, R. K. (1987). Crustacean chemical perception: towards a theory on optimal chemoreception. The Biological Bulletin, 172(1), 10-29. (PDF)
- Zimmer-Faust, R. K., Michel, W. C., Tyre, J. E., & Case, J. F. (1984). Chemical induction of feeding in California spiny lobster, Panulirus interruptus (Randall). Journal of chemical ecology, 10(6), 957-971.
- Zimmer-Faust, R. K., & Case, J. F. (1983). A proposed dual role of odor in foraging by the California spiny lobster, Panulirus interruptus (Randall). The Biological Bulletin, 164(2), 341-353. (PDF)