Metabolomic insights into the successional transition from dinoflagellate to cyanobacterial blooms: Dual roles of phytohormones and allelochemicals

Abstract

Understanding the succession patterns among harmful microalgae is crucial for managing freshwater ecosystems. The succession from dinoflagellate (Peridinium umbonatum, Pu) to cyanobacterial (Microcystis aeruginosa, Ma) blooms is a common phenomenon，which is often mainly attributed to complex allelopathic interactions. However, the specific chemical compounds driving these interactions and their precise functional roles remain largely unknown. To address this gap, we employed non-targeted UHPLC-MS metabolomics with targeted absolute quantification (LC-QQQ-MS/MS) and functional validation assays to investigate the potential chemical mediators of this interaction. Our results demonstrated a paradoxical, bidirectional relationship: Ma competitively excluded Pu, while Pu's exudates promoted Ma's growth. Through rigorous structural validation with authentic standards (MSI Level 1), we identified key candidate molecules that may potentially mediating this dynamic. Exogenous validation assays suggested that the promotion of Ma is potentially linked to the phytohormone Kinetin 9-riboside and the central metabolite alpha-Ketoglutaric acid secreted by Pu. Conversely, Ma's dominance was likely facilitated by its release of inhibitory allelochemicals, specifically 3-Hydroxykynurenine and a homoisoflavonoid derivative (a Methylophiopogonanone A-like compound). This study moves beyond describing general allelopathy to proposing a potential chemical mediated dual-mechanism for complex microalgal interactions. These findings suggest a sophisticated chemical strategy for competitive dominance and highlight the hypothesized role of phytohormones in mediating phytoplankton community dynamics, offering new insights for predicting and managing harmful algal blooms.