Extracellular polymeric substance mediating nanoplastics-promoted short-term Porphyridium growth disrupts marine carbon and phosphorus migration

The ecotoxicity of nanoplastics (NPs) on marine microalgae has been extensively explored recently, yet the mechanisms driving short-term growth improvement caused by NPs remain poorly understood. In the present study, we observed that a relatively high concentration (10 mg/L) of the green fluorescently labeled fresh polyamide-polymethyl methacrylate polymer blend (w/w 21:4) NPs beads (200 nm) significantly enhanced the cell density of Porphyridium cruentum (42.1%) by alleviating reactive oxygen species generation, chlorophyll degradation, and photoinhibition. An increase in the sticky bounded exopolysaccharides (b-EPs) surrounding P. cruentum surface enhanced NP adsorption within five hours of exposure, with –CH3 bond in phospholipids/glycolipids and polysaccharides of b-EPs supporting the adsorption to mitigate photoinhibition. Increased free exopolysaccharides (EPs) removed inorganic and organic carbon and 48% of dissolved organic matter, encapsulating NPs into sediments while cooperating with pH elevation. However, short-term growth promotion resulted in cell shading and phosphorous deficiency after 12 days of cultivation. Consequently, the photosynthesis-antenna proteins pathway and energy metabolites were downregulated, whereas the transmembrane transport and receptor activities of phosphate and calcium signal pathways were upregulated to maintain growth, achieving balance in the 1 mg/L group. The significantly upregulated steroid biosynthesis promoted the hydrophobicity of plasma membranes and reduced the permeability for water-soluble ions, exacerbating phosphorus deficiency. The downregulation of the Calvin cycle shifted the total carbon metabolism and carbon migration, reducing photosynthesis and respiration but accumulating starch to counteract cell shading and phosphorus deficiency. These findings provide novel insights into the mechanisms underlying the short-term growth stimulation and long-term potential toxic effects of NPs on marine microalgae, thus altering marine carbon and phosphorus cycles.