Plant-microbe interactions involve complex resource-use trade-offs, yet their responses to combined changes in precipitation frequency and nitrogen (N) deposition remain poorly understood. This knowledge gap limits our ability to predict grassland carbon (C) cycling under global change. We conducted a 4-year field experiment manipulating precipitation frequency (50% reduction, DPF) and N addition (10 g N m-2 year-1) to examine their interactive effects on cumulative soil respiration (SR) and its heterotrophic (HR) and autotrophic (AR) components in a semi-arid grassland. DPF-induced contrasting responses: surface soil drying suppressed microbial activity and HR, while increased subsoil moisture from larger, less frequent rain events enhanced root redistribution and AR, demonstrating a decoupling of the two respiration components. Nitrogen addition mitigated HR suppression by improving soil water retention and altering the microbial community. The initial drought transiently favoured fungi, but subsequent DPF-driven drying-rewetting pulses, particularly under N addition, promoted Gram-positive bacteria, increasing C-cycling enzyme activity and facilitating HR recovery through microbial adaptation to pulsed moisture. Over time, the initial enhancement of AR attenuated. This was likely due to intensified plant-microbe competition for limited surface water, which constrained sustained increases in root respiration. Our findings demonstrate how altered precipitation regimes and N deposition reshape plant-soil microbe adaptive strategies, which in turn regulate the components of soil C cycling. Integrating these dynamic adaptive processes is critical for accurately predicting ecosystem C balance under future global change.Read the free Plain Language Summary for this article on the Journal blog.