Anthropogenic activities have substantially altered nutrient regimes and organic matter availability in coastal ecosystems. While harmful algal blooms (HABs) are often explained primarily by inorganic nutrient enrichment, increasing dissolved organic matter (DOM) inputs may create additional resource niches for metabolically flexible phytoplankton. However, the role of DOM utilization, particularly osmotrophic acquisition of dissolved organic substrates, in promoting mixotrophic bloom-forming dinoflagellates remains poorly constrained. Here, we tested whether anthropogenic organic matter enrichment supports the dominance and persistence of mixotrophic dinoflagellates in Chinese coastal algal blooms by providing exploitable DOM resources. We combined long-term Chinese coastal bloom records with environmental driver analyses, laboratory incubations of field-collected Prorocentrum obtusidens bloom samples, FT-ICR MS-based DOM molecular characterization, transcriptomic analyses, and culture experiments using natural seawater from contrasting coastal environments. Long-term records revealed a disproportionate contribution of mixotrophic taxa to bloom frequency, affected area, and duration. Environmental analyses linked mixotrophic bloom dynamics to temperature and aquaculture-related organic matter inputs. Incubation experiments showed that P. obtusidens could grow without external nutrient addition, and aquaculture-derived DOM enhanced its growth and photosynthetic performance. FT-ICR MS analysis revealed pronounced molecular-level DOM transformation during bloom development, characterized by selective depletion of heteroatom-containing compounds, including N-, S-, and P-containing molecules, and substantial turnover of lipid-like components. Consistently, transcriptomic analyses showed that genes related to organic substrate uptake, endocytosis-associated vesicle trafficking, lysosomal degradation, and organic nutrient assimilation were highly expressed during bloom growth and maintenance, supporting an active role of DOM utilization in sustaining P. obtusidens blooms. Together, these findings suggest that anthropogenic DOM enrichment may provide an overlooked resource pathway that favors the dominance and persistence of mixotrophic dinoflagellates. This study extends the conventional inorganic nutrient-centered view of HAB development and highlights organic matter loading and DOM quality as key dimensions for understanding and managing coastal algal blooms.
 

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