Microbial mechanisms underlying complementary soil nutrient utilization regulated by maize-peanut root exudate interactions

Abstract

Root exudate-mediated interactions play a critical role in regulating below-ground ecological processes in maize-peanut intercropping systems. This study employed 16S ribosomal RNA and internal transcribed spacer sequencing to systematically investigate the effects of reciprocal root exudate irrigation on rhizosphere microbial communities, carbon-nitrogen metabolism, and plant growth. Compared to sterilized deionized water controls, peanut exudate-treated maize (PEM) showed a 35.64% reduction in rhizosphere total nitrogen (TN), with 25.71% and 25.01% increases in nitrate reductase (NR) and polyphenol oxidase (PPO) activities, respectively. Maize exudate-treated peanut (MEP) exhibited significant enhancements in NR (22.79%), PPO (14.70%), soil organic carbon (SOC, 22.32%), plant biomass (22.52%), and root nitrogen accumulation (34.15%), alongside suppressed N-acetyl-β-D-glucosaminidase and urease (URE) activities. Microbial analysis revealed significantly reduced α-diversity in PEM, accompanied by enrichment of Sphingomonas (0.43-fold) and Penicillium (3.65-fold). Random forest and variance partitioning analyses identified PEM-enriched Gemmatimonadaceae as the primary driver of NR activity variation. Notably, MEP exhibited substantial enrichment of Comamonadaceae and Oxalobacteraceae, which were respectively established as key regulators of URE and PPO activities. Phylum-level correlations demonstrated significant negative Proteobacteria-TN associations (r = −0.77) in PEM, and positive Acidobacteriota-SOC (r = 0.83), carbon-to-nitrogen ratio (r = 0.83), and PPO activity (r = 0.94) relationships in MEP. These findings suggest PEM accelerates nitrogen depletion by enhancing nitrogen mineralization and denitrification in the maize rhizosphere, while MEP improves soil fertility through carbon-nitrogen pathway inhibition, promoting SOC sequestration and nitrogen stabilization. This work provides theoretical insights into the ecological mechanisms underlying root exudate-driven complementary nutrient utilization in intercropping systems.