Aerobic granular sludge technology is attractive for intensified biological nutrient removal from wastewater and secondary clarification in single sequencing batch reactors. A methodology combining molecular fingerprinting, pyrosequencing-based identification of phylotypes with PyroTRF-ID, and multivariate statistics was developed to investigate on the long run, with high resolution, the dynamics of bacterial populations involved in nutrient removal in this wastewater treatment system. The predominant and flanking populations present in aerobic granules belonged to the core bacteriome of activated sludge removing nutrients biologically, and were structured in two major opponent clusters. Members of the first cluster, mainly related to Accumulibacter and Nitrospira, were favored under conditions leading to efficient nutrient removal. Members of the second cluster, mainly related to Competibacter, Sphingobacteriales, Cytophaga, and Intrasporangiaceae, proliferated during periods of low performances. A third transitory cluster mainly populated by Aminobacter and abundant Xanthomonadaceae relatives was identified with weak correlations to process parameters. Based on the physiological properties referenced in literature for the detected organisms, a tentative conceptual model of the bacterial ecosystem of aerobic granules was developed. This ecological model highlighted the presence of a broad denitrifying community that was not restricted to Accumulibacter and Competibacter only, and of populations involved in the metabolism of extracellular polymeric substances. Further research will determine how these putative denitrifiers and EPS producers and consumers can thrive in the aerobic granule ecosystem under anaerobic-aerobic conditions.