Nanoplastics reprogram fungal metabolism to reshape extracellular microenvironments and manganese biomineralization

Microbially mediated manganese (Mn) biomineralization is crucial for environmental redox buffering and metal cycling, but its response to nanoplastic (NP) pollution remains unclear. Here, the Mn(II)-oxidizing fungus Acremonium strictum KR21-2 was used to evaluate NP effects across a wide concentration gradient. Across all NP treatments, fungal dry weight decreased by less than 20%. Moreover, NP exposure reprogrammed fungal metabolism and gradually remodeled bound extracellular polymeric substances (B-EPS). At low doses (1 and 10 mg/L), NPs redirected cellular metabolism toward glycolysis and biosynthetic pathways and promoted the accumulation of polysaccharide (PS)-rich B-EPS. This adaptive extracellular matrix maintained Mn(II) oxidation while modifying the extracellular nucleation microenvironment, thereby enhancing the crystallinity of birnessite-like biogenic Mn oxides. At 50 and 100 mg/L NPs, B-EPS underwent further functional remodeling, characterized by protein (PN) enrichment, elevated PN/PS ratios, and extracellular superoxide accumulation, suggesting a transition toward an oxidatively stressed microenvironment. This remodeling, in conjunction with suppressed Mn-oxidizing enzyme expression, resulted in the loss of Mn(II) oxidation. These findings indicate that B-EPS forms a crucial yet delicate regulatory network that connects intracellular metabolic reprogramming to extracellular Mn(II) oxidation. B-EPS is sensitive to low-dose NP perturbations, undergoing substantial alterations before the inhibition of Mn biomineralization. Considering that Mn biomineralization is a typical biologically induced mineralization process regulated by the extracellular microenvironment, even minor changes in B-EPS may be magnified and significantly influence the biomineralization pathway and product structure. Therefore, risk assessments based solely on organism-level toxicity may underestimate the ecological impacts of NPs.