Biofilms are ubiquitous in nature, forming diverse adherent microbial communities that perform a plethora of functions. Here, we operated two laboratory-scale sequence batch reactors enriched with Candidatus Accumulibacter phosphatis (Accumulibacter) performing enhanced biological phosphorus removal (EBPR). Reactors formed two distinct biofilms, a floccular biofilm, consisting of small, loose, microbial aggregates, and a granular biofilm, forming larger, dense, spherical aggregates. Using metaproteomic methods we investigated the proteomic differences between these two biofilm communities, identifying a total of 2022 unique proteins. Both biofilms contained proteins that were indicative of core EBPR metabolisms and cellular function. To understand the proteomic differences between floccular and granular biofilm communities, we compared protein abundances that were statistically enriched in both biofilm states (alpha level = 0.05). Floccular biofilms were enriched with pathogenic secretion systems suggesting a previously unrecognized, highly competitive, mixed microbial community. Comparatively, granular biofilms revealed a high stress environment with evidence of nutrient starvation, phage predation pressure, extracellular polymeric substance (EPS) synthesis, and increased cell lysis. Granular biofilms enriched outermembrane transport proteins to scavenge the extracellular milieu for amino acids and other metabolites, likely released through cell lysis, to supplement core EBPR metabolic pathways. This study provides the first detailed proteomic comparison between Accumulibacter–enriched floccular and granular biofilm communities, proposes a conceptual model for the granule biofilm, and offers novel insights into granule biofilm formation and stability.