Riverine plastic litter restructures microbial vitamin B12 metabolism and generates functional heterogeneity

Abstract

Rivers transport most land-derived plastic waste to the ocean, yet how this reshapes microbial metabolic potential remains poorly resolved. We characterized plastisphere and water-column communities across 14 stations along the River Rhine, integrating ATR-FTIR polymer characterization, 16S/18S rRNA amplicon profiles, and 120 metagenome-assembled genomes. Plastisphere communities were taxonomically distinct from water communities (PERMANOVA R² = 0.258, p = 0.0001) and, despite no overall shift in functional centroid (R² = 0.245, p = 0.125), were markedly more heterogeneous in functional composition across sites (permutest p = 0.0047). Aerobic corrin ring synthesis, the core B12 biosynthetic pathway, was among the most differentially dispersed functions and enriched on plastic at all seven paired stations (Wilcoxon exact test, W = 3, p = 0.004079). This signal coincided with a diatom-dominated eukaryotic plastisphere community; diatoms cannot synthesize B12 and depend on bacterial provisioning, linking functional and taxonomic restructuring via a plausible cross-domain mechanism. Plastisphere communities were also less tightly coupled to the river’s dissolved nutrient gradient than water communities (envfit R² = 0.64 vs. 0.82). Together, these results indicate that riverine plastic litter does not merely accumulate biomass passively but actively restructures specific metabolic capacities of its colonizers, exemplified by vitamin B12 metabolism. Originality-Significance Statement This study presents a genome-resolved, transect-scale comparison of plastisphere and free-living microbial communities across a major European river, integrating polymer characterization, rRNA amplicon profiling, and 120 metagenome-assembled genomes. We show that plastic substrates partially decouple community assembly from the river’s dissolved nutrient gradient while selectively enriching vitamin B₁₂ biosynthetic potential, linking this functional restructuring to a co-occurring diatom-dominated eukaryotic community that depends on bacterial B₁₂ provisioning. By identifying a specific, testable metabolic mechanism underlying plastisphere functional distinctiveness, this work moves beyond descriptive taxonomic comparisons toward a mechanistic understanding of how plastic pollution reshapes microbial biogeochemical function in freshwater systems.