Metabolic Insights Into Infochemicals Induced Colony Formation and Flocculation in Scenedesmus subspicatus Unraveled by Quantitative Proteomics

Microalgae can respond to natural cues from crustacean grazers, such as Daphnia, by forming colonies and aggregations called flocs. Combining microalgal biology, physiological ecology, and quantitative proteomics, we identified how infochemicals from Daphnia trigger physiological and cellular level changes in the microalga Scenedesmus subspicatus, underpinning colony formation and flocculation. We discovered that flocculation occurs at an energy-demanding ‘alarm’ phase, with an important role proposed in cysteine synthesis. Flocculation appeared to be initially stimulated by the production of an extracellular matrix where polysaccharides and fatty acids were present, and later sustained at an ‘acclimation’ stage through mitogen-activated protein kinase (MAPK) signaling cascades. Colony formation required investment into fatty acid metabolism, likely linked to separation of membranes during cell division. Higher energy demands were required at the alarm phase, which subsequently decreased at the acclimation stage, thus suggesting a trade-off between colony formation and flocculation. From an ecological and evolutionary perspective, our findings represent an improved understanding of the effect of infochemicals on microalgae-grazers interactions, and how they can therefore potentially impact on the structure of aquatic communities. Moreover, the mechanisms revealed are of interest in algal biotechnology, for exploitation in low-cost, sustainable microalgal biomass harvesting.