Microbial Physiological Adaptation to Biodegradable Microplastics Drives the Transformation and Reactivity of Dissolved Organic Matter in Soil

Abstract

The turnover of dissolved organic matter (DOM) in soil regulated by biodegradable microplastics (MPs) has garnered much attention due to its profound impact on the storage and stability of soil organic matter. However, the transformation and reactivity of plant-derived and microbially derived DOM by microorganisms adapted to biodegradable MPs, and the involved microbial physiological processes, remain nearly unknown. Here, we added virgin and aged polylactic acid (PLA) and polyhydroxyalkanoate (PHA) to agricultural soils and incubated for 56 days. Using stable isotope techniques, reactomics, and metagenomics, we found that the addition of both virgin and aged PLA induced hydroxylation, demethylation, and dehydrogenation of lignin-derived DOM, resulting in a 3-fold increase in their oxidation degree. PLA activated the enzymatic pathway for lignin-derived DOM decomposition and downregulated genes involved in bacterial anabolism, such as those related to protein, amino sugar, and peptidoglycan biosynthesis. In contrast, PHA increased the content of microbially derived DOM compounds such as proteins and amino sugars by 2.1-fold relative to the control with peptide chain elongation. PHA resulted in the degradation of lignin-derived DOM into pyruvate and acetyl-CoA, accelerated bacterial ATP synthesis, the de novo biosynthesis of proteins and peptidoglycan, and cell renewal and death, thereby increasing PHA- and soil organic matter-derived microbial necromass carbon. Our study provides new insights into the impact of biodegradable MPs on soil DOM transformation and underscores the importance of the microbial physiological processes involved.