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Rhizodeposition fuels carbon (C) and nutrient cycling in soil. However, changes in the dynamics of microbial growth on rhizodeposits with increasing distance from the root is not well studied. This study investigates microbial growth on individual organic components of rhizodeposits and maize root‐derived exudates and mucilage from agricultural soil. By creating a gradient of substrate concentrations, we simulated reduced microbial access to rhizosphere C with increasing distance to the root surface. We identified distinct C‐thresholds for the activation of microbial growth, and these were significantly higher for rhizodeposits than singular, simple sugars. In addition, testing for stoichiometric constraints of microbial growth by supplementing nitrogen (N) and phosphorus (P) showed accelerated and increased microbial growth by activating a larger proportion of the microbial biomass. Early and late season exudates triggered significantly different microbial growth responses. The mineralization of early‐season exudates was induced at a high C‐threshold. In contrast, the mineralization of late‐season exudates showed 'sugar‐like' properties, with a low C‐threshold, high substrate affinity, and a reduced maximum respiration rate of microorganisms growing on the added substrate. Mucilage exhibited the highest C‐threshold for the activation of microbial growth, although with a short lag‐period and with an efficient mucilage degradation comparable to that of sugars. By determining kinetic parameters and turnover times for different root‐derived substrates, our data enable the upscaling of micro‐scale processes to the whole root system, allowing more accurate predictions of how rhizodeposition drives microbial C and nutrient dynamics in the soil. [ABSTRACT FROM AUTHOR]