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

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β-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 β-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 β-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 β-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 β-cyclocitral/cell), corresponding to a calculated maximum intracellular concentration of 2.2 mM. The behavioral response of Daphnia magna to β-cyclocitral was evaluated in a bbe© Daphnia toximeter, where β-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 β-cyclocitral. The minimum VOC concentration (odor threshold) that elicited a significant grazer response was 750 nM β-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 β-cyclocitral microzone around Microcystis colonies, thus acting as both a powerful repellent and signal of poor quality food to grazers.

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Acknowledgements

F.J. thanks J. Pernthaler, Limnological Station, University of Zürich, for continuous support.

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Authors and Affiliations

  1. University of Zürich, Limnological Station, CH-8802, Kilchberg, Switzerland

    Friedrich Jüttner

  2. Aquatic Ecosystem Management Research Canada Centre for Inland Waters, Environment Canada, 867, Lakeshore Rd, Burlington, ON, Canada

    Susan B. Watson

  3. University of Cologne, Cologne Biocentre, Zülpicher Strasse 47b, 50674, Köln, Germany

    Eric von Elert

  4. Zürich Water Supply (WVZ), Hardhof 9, P.O. Box 1179, CH-8021, Zürich, Switzerland

    Oliver Köster

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  1. Friedrich Jüttner
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Correspondence to Friedrich Jüttner.

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Jüttner, F., Watson, S.B., von Elert, E. et al. β-Cyclocitral, a Grazer Defence Signal Unique to the Cyanobacterium Microcystis . J Chem Ecol 36, 1387–1397 (2010). https://doi.org/10.1007/s10886-010-9877-0

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