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Biochemistry

Toxic meal: Chemical cues from copepods increase red-tide toxicity

The Paper:

Selander, E., Kubanek, J., Hamberg, M., Andersson, M. X., Cervin, G., & Pavia, H. (2015). Predator lipids induce paralytic shellfish toxins in bloom-forming algae. Proceedings of the National Academy of Sciences, 201420154 DOI: 10.1073/pnas.1420154112.

Background:

Phytoplankton are responsible for almost half of Earth’s photosynthesis and provide a nice meal for hungry zooplankton like krill, copepods and jellyfish. In order to detect and capture their prey in the vast ocean, predators require special chemical adaptations. Zooplankton predators are able to recognize chemical cues from potential prey and determine if the prey is appetizing. Zooplankton prefer certain prey (similar to how we act in a buffet line). The palatability of an algal species depends on various characteristics like cell shape, size, chemical composition, and overall nutritional quality (zooplankton must hate those empty calories). Chemical communication may also be beneficial to the prey. Predator-derived chemical cues can bring about defense mechanisms in phytoplankton prey. For example, potential prey may alter their cell shape, increase their motility (swim away from predator), or increase toxicity.

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Figure 1: A) Red-tide formed by the B) dinoflagellate, Alexandrium minutum (10 µm in length). C) Common shellfish that may be intoxicated by the dinoflagellate.

Some phytoplankton naturally produce toxins. The dinoflagellate, Alexandrium minutum, is one such species that is known to form large and toxic blooms. When a zooplankton copepod is in the neighborhood, A. minutum will dramatically increase its toxicity. While it may seem that this is due to physical grazing by the copepod, it seems more likely that phytoplankton cells can chemically identify the copepod before it starts to munch! The more toxic cells become less appealing to grazers. Without a willing predator, A. minutum can grow to form giant red-algal blooms (also known as red-tides) (Fig. 1A, B). While beneficial to the reproductive success of A. minutum, these blooms spell trouble for other organisms. A. minutum produces a mixture of potent neurotoxic alkaloids called saxitoxins. These toxins accumulate in food webs and can negatively affect the health of zooplankton, bivalves, fish, seabirds, and marine mammals. Though rare, even humans can become intoxicated via fish and shellfish consumption. To date, there is no anecdote for paralytic shellfish poisoning in humans (Fig. 1C). Therefore, a better understanding of saxitoxin and the methods leading to its production in the ocean is vital.

Study and Results:

In this study, researchers set out to isolate and identify potential cueing compounds released by copepods (are these chemicals really there and what are they?). In addition, they tested the response of the toxin-producing A. minutum to these compounds and measured the concentration of compounds in the ocean.

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Figure 2: Increase in toxicity following exposure of A. minutum to copepodamides A-H. Each symbol is the mean of three independent replicates.

The copepod, Centropages typicus, was collected and put through a series of extractions (better access to compounds). Mass spectroscopy was used to identify compounds remaining in the copepod extracts (for more detail, see the “Materials and Methods”). These extracts contained eight polar lipids (insoluble fats), which were named copepodamides A-H. A. minutum was exposed to varying concentrations of the different copepodamides to see if they were associated with toxin production. Indeed, copepodamides caused A. minutum to increase toxin production, especially compounds A-C (Fig. 2). It took incredibly small concentrations (six orders of magnitude smaller than your typical phytoplankton) of copepodamides to increase toxicity. Thus, the presence of minute doses of copepodamides encouraged A. minutum to release more toxins.

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Figure 3: A) Raw data and B) averages of copepod density and copepodamide concentration with depth at the same location.

 

What about the prevalence of these cueing compounds in natural ocean samples? Copepodamides were measured in field-collected seawater from seven distinct depths (0-30m) at a site in the Northeast Atlantic Ocean. Copepodamide concentration (A-F) ranged from below the detection limit to 0.34 picomolar (again, insanely small). Both copepodamide concentration and copepod density were highest in the surface above 15m (Fig. 3A). Averaged values from the seven depths are shown in Fig. 3B and show a stronger correlation between copepod density (red line) and copepodamides (blue line). In the ocean, copepodamides appear to be higher in the surface and associated with copepods.

 

 

Conclusion and Significance:

Chemical communication is critical in the ocean. It helps predators locate and ingest tasty prey, while allowing some lucky prey to escape. A. minutum is able to identify chemical cues of nearby copepods and increase production of saxitoxins. Copepodamides represent the first discovery of chemical cues between marine zooplankton and their phytoplankton prey! In the laboratory, A. minutum produced high amounts of saxitoxin when exposed to microscopic copepodamide doses. Field experiments showed that copepodamides were in surface waters and positively related to copepod density. This seems reasonable given the direct release of copepodamides from copepods. Small amounts of copepodamides could easily double the toxicity of A. minutum in the upper water column.

The saxitoxins formed by A. minutum can intoxicate other organisms in the food web. High concentrations of saxitoxins can be detrimental and even fatal to humans who consume contaminated shellfish and fish. Though rare, there is no cure for paralytic shellfish poisoning in humans. The identification and isolation of copepodamides is a breakthrough, mainly because these compounds cause such a significant increase in saxitoxin production. The benefit of this knowledge is two-fold. It allows us to better understand ecosystem interactions on the smallest scale and aids our understanding of saxitoxin production in the ocean. The discovery of copepodamides opens the door for future research on other potential toxin-inducing chemical cues.

Share your thoughts: What are your thoughts on red-tides in the ocean? Did you know chemical cues could have such an impact on toxin production?

Sean Anderson
I am a first year MS candidate at the University of Rhode Island, Graduate School of Oceanography. I am interested in plankton ecology and the dynamics within plankton food webs. My research interests include the behavioral and physiological responses of phytoplankton and heterotrophic predators.

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