Ignited competition: Impact of bioactive extracellular compounds on organelle functions and photosynthetic systems in harmful algal blooms

Abstract

Prevalent interactions among marine phytoplankton triggered by long-range climatic stressors are well-known environmental disturbers of community structure. Dynamic response of phytoplankton physiology is likely to come from interspecies interactions rather than direct climatic effect on single species. However, studies on enigmatic interactions among interspecies, which are induced by bioactive extracellular compounds (BECs), especially between related harmful algae sharing similar shellfish toxins, are scarce. Here, we investigated how BECs provoke the interactions between two notorious algae, Alexandrium minutum and Gymnodinium catenatum, which have similar paralytic shellfish toxin (PST) profiles. Using techniques including electron microscopy and transcriptome analysis, marked disruptions in G. catenatum intracellular microenvironment were observed under BECs pressure, encompassing thylakoid membrane deformations, pyrenoid matrix shrinkage and starch sheaths disappearance. In addition, the upregulation of gene clusters responsible for photosystem-I Lhca1/4 and Rubisco were determined, leading to weaken photon captures and CO₂ assimilation. The redistribution of lipids and proteins occurred at the subcellular level based on in situ focal plane array FTIR imaging approved the damages. Our findings illuminated an intense but underestimated interspecies interaction triggered by BECs, which is responsible for dysregulating photosynthesis and organelle function in inferior algae and may potentially account for fitness alteration in phytoplankton community.

Keywords: FPA‐FTIR; algal physiology; bioactive extracellular compounds; harmful algae; interspecies interaction; pyrenoid; thylakoid.