Dissolved organic carbon (DOC) can alter the availability of background nutrients by affecting the proliferation of heterotrophic bacteria, which exerts a notable influence on algal growth and metabolism. However, the mechanism of how allochthonous DOC (aDOC) precipitates shifts in bacterial-algal interactions and modulates the occurrence of cyanobacteria blooms remains inadequately elucidated. Therefore, this study investigated the relationship between bacteria and algae under aDOC stimulation. We found that excess aDOC triggered the breakdown and reestablishment of the equilibrium between Microcystis and heterotrophic bacteria. The rapid proliferation of heterotrophic bacteria led to a dramatic decrease in soluble phosphorus and thereby resulted in the inhibition of the Microcystis growth. When the available DOC was depleted, the rapid death of heterotrophic bacteria released large amounts of dissolved phosphorus, which provided sufficient nutrients for the recovery of Microcystis. Notably, Microcystis rejuvenated and showed higher cell density compared to the carbon-absent group. This phenomenon can be ascribed that Microcystis regulated the compositions of extracellular polymeric substances (EPS) and the expression of relevant proteins to adapt to a nutrient-limited environment. Using time of flight secondary ion mass spectrometry (TOF-SIM) and proteomic analysis, we observed an enhancement of the signal of organic matter and metal ions associated with P complexation in EPS. Moreover, Microcystis upregulated proteins related to organic phosphorus transformation to increase the availability of phosphorus in various forms. In summary, this study emphasized the role of DOC in algal blooms, revealing the underestimated enhancement of Microcystis nutrient utilization through DOC-induced heterotrophic competition and providing valuable insights into eutrophication management and control.