Contribution and regulation of Ustilago maydis in carbohydrate metabolism during maize silage fermentation

Abstract Background Corn smut disease, caused by the phytopathogenic fungus Ustilago maydis, induces gall formation, which can result in complete yield loss and nutritional deterioration. While harvesting and ensiling are effective strategies for enhancing nutritional value, the molecular mechanisms by which U. maydis infection affects silage fermentation remain unclear. This study systematically evaluated the effects of U. maydis infection on the nutritional composition, fermentation characteristics, and mycotoxin accumulation in maize from Gansu (GSHF) and Hebei (HSHF). Furthermore, it revealed the potential interference of this infection with microbial community structure and functional metabolic pathways through metagenomic sequencing. Results The results indicated that infection with U. maydis significantly reduced the content of neutral detergent fiber (NDF) and water-soluble carbohydrates (WSC) in corn plants while simultaneously increasing the levels of ether extract (EE), crude protein (CP), lactic acid bacteria (LAB), yeast, and mold. In addition, infection significantly elevated mycotoxin levels. ITS analysis revealed a decrease in microbial richness in the infected groups (GSHF, HSHF), with a notable enrichment of U. maydis and the unique presence of Fusarium in the HSHF group. After 6 months of ensiling, improvements were observed in several silage quality indicators, including increases in lactic acid (LA), dry matter (DM), WSC, LAB, and yeast levels, as well as reductions in ammonia nitrogen (NH₃–N%TN) and hemicellulose (HCEL) content. Although the ZEN content in the raw materials significantly increased—being 5.02 times and 3.47 times higher than the control group in GSHF and HSHF (P < 0.01), respectively—its content decreased by 6.5% and 51.3% compared to the control group after ensiling. Although aerobic stability decreased in both groups, the application of inoculants (3GSHF, 3HSHF) effectively prevented this decline. Metagenomic analysis revealed that both GSHF and HSHF harbored a significant amount of U. maydis, which primarily affects carbohydrate synthesis. After ensiling, U. maydis suppressed the abundance of Lentilactobacillus, reduced sugar utilization efficiency, and consequently led to an increase in WSC levels. Conclusions U. maydis primarily affects carbohydrate metabolism during the ensiling process. By inhibiting the growth of Lentilactobacillus, it reduces the efficiency of sugar utilization, which in turn increases the content of WSC. These findings provide new insights into the complex interactions between crop diseases and silage quality. Graphical Abstract