Rainfall is rare in hyperarid deserts but, when it occurs, it triggers large biological responses which are considered to be essential for the long-term maintenance of biodiversity. In such environments, microbial communities have major roles in nutrient cycling, but their functional responses to short-lived resource opportunities are poorly understood. We used whole community metatranscriptomic data to demonstrate structured and sequential functional responses in desiccated desert soils to a simulated rainfall event over a seven-day time frame. Rapid transcriptional activation of Actinobacteria, Alpha-proteobacteria and phage transcripts was followed by a marked increase in protist and myxobacterial activity, before returning to the original state. In functional terms, motility systems were activated in the early phases, whereas competition-toxicity systems increased in parallel to the activity from predators and the drying of soils. The dispersal-predation dynamic was identified as a central driver of microbial community responses to watering. Carbon fixation mechanisms that were active under dry condition were rapidly down-regulated in wetted soils, and only reactivated on a return to a near-dry state, suggesting a reciprocal balance between carbon fixation and fixed-carbon acquisition processes. Water addition induced a general reduction in the transcription of stress response genes, most prominently HSP20, indicating that this chaperone is particularly important for life in desiccated ecosystems. Based on these data, we propose a rainfall response model for desert soil microbiomes.