Predator lipids induce paralytic shellfish toxins in bloom-forming algae

Abstract

Interactions among microscopic planktonic organisms underpin the functioning of open ocean ecosystems. With few exceptions, these organisms lack advanced eyes and thus rely largely on chemical sensing to perceive their surroundings. However, few of the signaling molecules involved in interactions among marine plankton have been identified. We report a group of eight small molecules released by copepods, the most abundant zooplankton in the sea, which play a central role in food webs and biogeochemical cycles. The compounds, named copepodamides, are polar lipids connecting taurine via an amide to isoprenoid fatty acid conjugate of varying composition. The bloom-forming dinoflagellate Alexandrium minutum responds to pico- to nanomolar concentrations of copepodamides with up to a 20-fold increase in production of paralytic shellfish toxins. Different copepod species exude distinct copepodamide blends that contribute to the species-specific defensive responses observed in phytoplankton. The signaling system described here has far reaching implications for marine ecosystems by redirecting grazing pressure and facilitating the formation of large scale harmful algal blooms.

Keywords: Alexandrium; harmful algal bloom; inducible defense; lipid signaling; paralytic shellfish toxin.

Fig. 1.

Structures of copepodamides A–H (MW, molecular weight), with effective copepodamide concentrations for doubling of saxitoxins concentrations calculated from dose–response data after 2-d exposure of Alexandrium cells to each individual copepodamide (Fig. 2).

Fig. 2.

(A) Dose–response curves showing induction of toxicity following exposure of Alexandrium cells to individual, pure copepodamides A–H. Each symbol represents the mean of three independent replicates ± SE. Curves represent nonlinear least square fits to the Michaelis–Menten equation. At doses near 2,000 nM, copepodamide H was even less active than at 60–300 nM (n = 3 independent replicates per copepodamide per concentration; symbols represent mean values ± SE). (B) PCA representation of copepodamides A–F in whole body extracts of common marine copepods Calanus sp., Centropages typicus, and Pseudocalanus sp. (n = 4 extracts of 5–10 individuals for each species).

Fig. 3.

Exudation rate of copepodamides into seawater by live, field-collected Calanus copepods. Each bar represents the mean of three experimental units of two to three copepods each + SE.

Fig. 4.

(A) Copepod density and copepodamide concentration interpolated from three replicate depth profiles (0–30 m depth) at the same location, obtained over a 1.5-d time period (time = 0 equals 1600 hours). Both copepods and copepodamides were sampled at seven depths (0, 1.5, 5, 10, 15, 20, and 30 m) for each profile. (B) Averaged values of copepod density and copepodamides over the 1.5-d time period for each depth ± SE of mean (n = 3, r² = 0.34).