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Rainfall is rare in hyperarid deserts but, when it occurs, it triggers large biological responses essential for the long-term maintenance of the ecosystem. In drylands, microbes play major roles in nutrient cycling, but their responses to short-lived opportunity windows are poorly understood. Due to its ephemeral nature, mRNA is ideally suited to study microbiome dynamics upon abrupt changes in the environment. We analyzed microbial community transcriptomes after simulated rainfall in a Namib Desert soil over 7 days. Using total mRNA from dry and watered plots we infer short-term functional responses in the microbiome. A rapid two-phase cycle of activation and return to basal state was completed in a short period. Motility systems activated immediately, whereas competition–toxicity increased in parallel to predator taxa and the drying of soils. Carbon fixation systems were downregulated, and reactivated upon return to a near-dry state. The chaperone HSP20 was markedly regulated by watering across all major bacteria, suggesting a particularly important role in adaptation to desiccated ecosystems. We show that transcriptomes provide consistent and high resolution information on microbiome processes in a low-biomass environment, revealing shared patterns across taxa. We propose a structured dispersal–predation dynamic as a central driver of desert microbial responses to rainfall.