Phage Lysis Associated with Biodegradable Microplastics Mediates Microbial Physiological Adaptation to Transform Organic Matter in Soil

Abstract Biodegradable microplastics (MPs) profoundly impact the storage and stability of soil organic matter (SOM), yet the mechanisms by which phages mediate the transformation of plant- and microbially derived SOM under biodegradable MP perturbation remain poorly understood. This study integrated multiomics, stable isotope techniques, and phage inoculation experiments to investigate how phages mediate SOM transformation following biodegradable MP addition in agricultural soil. The results revealed that lytic phage-bacteria interactions were central to MP-dependent SOM transformation. Polylactic acid (PLA) reduced plant-derived organic molecules by 15% without affecting microbially derived carbon. PLA increased phage lysis and enriched auxiliary metabolic genes (AMGs) such as queC (2.2-fold increase), which supports phage replication and reduces microbial biomass. Pure culture experiments supported that PLA increased phage lytic infectivity. Phage inoculation further revealed that lytic phages accelerated bacteria to shift toward catabolism (e.g., lignocellulose degradation, citrate cycle) in PLA-amended soil, reducing carbon use efficiency (CUE) and accelerating decomposition of plant- and microbially derived carbon through viral shunt. In comparison, polyhydroxyalkanoates (PHA) increased microbially derived molecules by 37%, particularly amino nitrogen compounds. The higher degradability of PHA stimulated lytic phage bloom with their hosts and enriched biosynthesis-related AMGs (e.g., cysH, glmS). Phage inoculation experiments showed that surviving bacteria assimilated phage lysate products into anabolism (e.g., amino acid and amino sugar biosynthesis), enriching metabolites such as l-isoleucine and MurNAc after PHA addition. This increased CUE and accumulation of microbial organics through viral shuttle. These findings uncover phage-mediated mechanisms linking microplastic perturbation to soil carbon cycling.