β-Cyclocitral, a Grazer Defence Signal Unique to the Cyanobacterium Microcystis

beta-Cyclocitral is often present in eutrophic waters and is a well known source of airborne and drinking water malodor, but its production and functional ecology are unresolved. This volatile organic compound (VOC) is derived from the catalytic breakdown of beta-carotene, and evidence indicates that it is produced by the activation of a specific carotene oxygenase by all species of the bloom-forming cyanobacterium Microcystis. Previous work has shown that beta-cyclocitral affects grazer behavior, but the nature of this interaction and its influence on predator-prey dynamics was unresolved. The present study combined analytical and behavioral studies to evaluate this interaction by using Microcystis NRC-1 and Daphnia magna. Results showed that beta-cyclocitral was undetectable in live Microcystis cells, or present only at extremely low concentrations (2.6 amol/cell). In contrast, cell rupture activated a rapid carotene oxygenase reaction, which produced high amounts (77+/-5.5 amol beta-cyclocitral/cell), corresponding to a calculated maximum intracellular concentration of 2.2 mM. The behavioral response of Daphnia magna to beta-cyclocitral was evaluated in a bbe (c) Daphnia toximeter, where beta-cyclocitral treatments induced a marked increase in swimming velocity. Acclimation took place within a few minutes, when Daphnia returned to normal swimming velocity while still exposed to beta-cyclocitral. The minimum VOC concentration (odor threshold) that elicited a significant grazer response was 750 nM beta-cyclocitral, some 2,900 times lower than the per capita yield of a growing Microcystis cell after activation. Under natural conditions, initial grazer-related or other mode of cell rupture would lead to the development of a robust beta-cyclocitral microzone around Microcystis colonies, thus acting as both a powerful repellent and signal of poor quality food to grazers.